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Comparative approach to infochemical use by parasitoids for the case of Cotesia glomerata and Cotesia rubecula

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... This may indicate that at close range the parasitoid is able to find the infested part of the plant. A similar result was reported by Dicke et al. (1993) who found that predatory mites preferred hostdamaged leaves when offered versus undamaged leaves which emitted herbivoreinduced synomones in response to an endogenous elicitor. A factor that induces the systemic response seems to be present in the regurgitate of the larva. ...
... Some recent studies have focused on the elicitor that triggers the systemic response of herbivore-infested plants. Dicke et al. (1993) extracted an elicitor that is transported from infested leaves to uninfested leaves. could induce the production of plant volatiles by placing maize seedlings in diluted regurgitate from several species of caterpillars and a grasshopper. ...
... He found that the two populations of B. philenor were equally capable to learn visual cues (leaf shape) of a particular host species. The macro-evolutionary approach, where the learning abilities of different species are compared, has been used, for instance to compare the learning abilities of specialist and generalist parasitoids Poolman Simons et al., 1992;Geervliet et al., 1993). A species comparative approach can also be used for parasitoids attacking stemborer larvae. ...
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Classical biological control involves the introduction of an exotic natural enemy to control an introduced pest species. In 1991 the department of Entomology of the Wageningen Agricultural University started a collaborative project with the International Centre for Insect Physiology and Ecology (ICIPE) in Nairobi Kenya, on the biological control of stemborers in Africa. The gregarious endoparasitoid Cotesiaflavipes (Hymenoptera: Braconidae) was chosen as the natural enemy to be introduced against the accidentally introduced pest Chilopartellus (Lepidoptera: Pyralidae) in East-Africa (Overholt et al., 1994; Omwega et al., 1996). The research described in this thesis was related to this project and addressed several aspects of the behavioral ecology of this parasitoid. In the first part, gaps in the knowledge on behavioral ecology of C.flavipes are studied which include the longand short-range searching behavior, some aspects of the life history and host discrimination abilities. The second part focuses on the intraspecific variability in C.flavipes behavior and here we determine to what extent the reported plant and host specificity in C.flavipes has a genetic basis or is due to phenotypic plasticity through learning.Micro-habitat and host location in CotesiaflavipesThe first part addresses the origin of the olfactory stimuli involved in hostmicrohabitat location (chapter 2) and the contact stimuli involved in tunnel and host location on a stemborer infested plant (chapter 3). In chapter 2 it is demonstrated that a major source of the attractive volatiles from the plant-host- complex is the stemborer-injured stem, including the frass produced by the feeding larvae. Moreover, the production of volatiles attractive to a parasitoid is not restricted to the infested stem-part but occurs systemically throughout the plant. The uninfested leaves of a stemborer-infested plant emit volatiles that attract female C.flavipes . An exogenous elicitor of this systemic plant response is situated in the regurgitate of a stemborer larva. When a minor amount of regurgitate is inoculated into the stem of an uninfested plant, the leaves of the treated plant emit volatiles which attract female C.flavipes . Evidence is accumulating that plants are actively involved in attracting natural enemies Dicke 1994). However, whether plants have specifically evolved the ability to release volatiles that attract natural enemies of the herbivore that is attacking them remains a matter of debate (Bruin et al. 1995).Foraging behavior on stemborer infested plantOnce a female C.flavipes has located a stemborer infested plant, it has to locate the concealed host inside the plant stem. In chapter 3 the behavior of female C.flavipes on stemborer infested plants was investigated. It is demonstrated that larval frass, caterpillar regurgitate and holes in the stem are used in host location by C.flavipes . After locating the exit hole of the stemborer tunnel, where larval frass has accumulated, the parasitoid female tries to enter the stemborer tunnel. This can take a long time because the tunnel is often blocked by larval frass and the female sometimes has to squeeze through small holes. The response to host products by C.flavipes seems not to be host species specific. Female C.flavipes respond to frass from four different stemborer species and one leaf feeder. No differences are found in the behavior of C.flavipes on maize plants infested with the suitable host, Chilopartellus (Lepidoptera: Pyralidae), or the unsuitable host, Busseola fusca (Lepidoptera: Noctuidae). Attacking a concealed stemborer larvae in the confined space of stemborer tunnel is not only time consuming but also risky. It is demonstrated that 30-40% of the parasitoids is killed by the spitting and biting stemborer larva. Takasu and Overholt (1996) showed that a female parasitoid has a high probability (0.9) to be bitten to death when it approaches the host towards the head. However, the majority of the females were first able to successfully parasitize its offensive host before being killed. A female C.flavipes needs only a few seconds to inject around 45 eggs into its host. The high probability of mortality at each host encounter results in a very low expectation of the number of lifetime host encounters. The possible consequences of this low lifetime host encounter rate for the evolution of life history- and foraging strategies formed the basis of a large part of this thesis.Life history ofCotesiaflavipesC.flavipes is relatively short lived: without food the parasitoids die within two days, with food and under high humidity conditions they die within 5-6 days. In chapter 3 the fecundity and clutch size allocation of C.flavipes was investigated. It is demonstrated that C.flavipes is pro-ovigenic and has around 150 eggs available for oviposition. In the first encountered hosts 35-45 eggs per host are laid. Thus, a relatively large proportion of the available egg load (20-25%) is allocated to each host, and a female C.flavipes is equipped with an eggload to parasitize 3-4 hosts only. Especially for animals whose lifetime reproductive success is limited by opportunities to reproduce, clutch size theory predicts a maximization of the fitness gain per clutch (Godfray, 1987). This may be true for C. flavipes, which has a short lifespan and a high mortality risk at each host encounter, resulting in a low number of expected lifetime host encounters (Chapter 3). In chapter 4 it is demonstrated that the number of produced adults from superparasitized hosts is equal to that of singly parasitized hosts. This indicates that female C.flavipes indeed lay an optimal clutch size in fourth instar C. partellus larvae.Host- and host-sitediscriminationThe fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes are described in chapter 4 . Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 hours previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she has parasitized a host. The function of the avoidance of superparasitism. in C.flavipes is clear: a discriminating female saves searching time, avoids the wastage of eggs and avoids a direct mortality risk. The mechanism of host discrimination is the recognition of a chemical mark on the tunnel substrate.The role of learning in hostforagingMany studies have shown that parasitoids can learn visual or olfactory stimuli associated with successful host location and use these odours in subsequent foraging decisions (reviewed by Turlings et al., 1993; Vet et al., 1995). The ability to learn has now been demonstrated in more than 20 different parasitoid species and learning in parasitoids seems to be the rule rather than the exception (Turlings et al., 1993). In chapter 5 the role of learning in host foraging in C.flavipes was investigated. Using experimental procedures similar to other parasitoid learning studies, the role of the learning mechanisms priming (i.e. increase in response) and preference-induction in the foraging of C.flavipes was determined. No evidence was found that C.flavipes uses odour learning in hostmicrohabitat location. There was no significant effect of the development and emergence environment on the response level or preference towards infested plant odours. Neither was any evidence found that experience with a particular plant-host-complex during foraging influences subsequent foraging decisions in C.flavipes females.Recent discussions of animal learning emphasize the importance of considering an animals ecology when studying and interpreting its learning abilities. Recently, it has been hypothesized that the adaptive value of learning in foraging is dependent on the predictability of the environment (Stephens, 1993) and the number of lifetime foraging decisions (Roitberg et al., 1993). Learning is not expected when the foraging environment is highly predictable (i.e. the resource is constant) and when animals make only a few decisions while foraging. Taking the ecology of C.flavipes into account it is hypothesized that two factors may be responsible for the lack of learning in foraging in C.flavipes : a predictable foraging environment and the restricted number of lifetime foraging decisions.EVOLUTION OF LIFE HISTORY AND FORAGING STRATEGIESEvolutionary ecological theory concentrates on the interpretation of form and function of individuals as adaptations to their environment. Theories of life history evolution predict what sorts of life history should evolve in specified ecological circumstances (e.g. Steams, 1992; Roff, 1992) and optimal foraging theory addresses the problem of choice among resources or habitats (e.g. Krebs and Davies, 1981; Stephens and Krebs, 1986). It is tempting to relate the ecology of C.flavipes with its life history characteristics and its foraging tactics. The stemborer parasitoid C.flavipes has a peculiar ecology. It not only forages for hosts in a relatively homogeneous and predictable habitat, but it also has a risky attack tactic resulting in a low number of expected lifetime host encounters.The small C.flavipes attacks stemborer larvae by entering the stemborer tunnel (chapter 3). To reach the host, the parasitoid female has to squeeze through small holes in the tunnel which is filled with larval frass. It has been suggested that the dorso-ventral body shape, which is typical of the Cotesia species belonging to the Cotesiaflavipes complex is an adaptation to this ingress behavior (Kimani, pers. comm.). Attacking a host in the confined space of a stemborer tunnel is not without risk for the female parasitoid. At each host attack the female has a considerable risk to be killed by its aggressive host (chapter 3). The short oviposition time (around 40 eggs in 3-4 seconds) may be an adaptation to this mortality risk. The majority of the females that are killed have already successfully parasitized their host.The relatively high mortality risk at each host encounter in combination with the short lifespan results in a very low number of expected lifetime host encounters. This is reflected in the eggload of a female at emergence, which is just enough to parasitize 3-4 hosts (chapter 3). When the probability of surviving to find another host is small, optimal progeny allocation models predicts an optimal 'Lack' clutch size, where fitness is maximized per host (Waage & Godfray, 1985; Godfray 1987). Although it was not tested in depth the results of the superparasitism experiments (chapter 4) indicated that C.flavipes lays an optimal clutch size.The foraging environment of a female C.flavipes can be envisaged as a homogeneous and stable habitat, consisting of a field of perennial grasses with a few prevalent stemborer species. In chapter 5 it is hypothesized that this predictable foraging environment together with the low number of expected lifetime host encounters plays a part in the absence of (odor) learning in C.flavipes host foraging. In chapter 4 it is demonstrated that female C.flavipes leave an external mark on the tunnel substrate after parasitization. It is generally hypothesized that marking evolved as a means for individuals to avoid superparasitizing hosts they themselves previously parasitized (Roitberg and Prokopy, 1987). A female C.flavipes saves time and avoids a superfluous mortality risk by avoiding utilized host tunnels.When a parasitoid has a high mortality risk at each oviposition, life history theory predicts a high selectivity to avoid waste of progeny (Iwasa et al., 1984; Ward, 1992). The parasitoid should not risk her life for low quality hosts, such as unsuitable hosts or already parasitized hosts. However, naive female C.flavipes (no oviposition experience) seem to have a very opportunistic host selection behavior. In chapter 3 it is demonstrated that C.flavipes did attack the (new) unsuitable host B. fusca and in chapter 5 it is found that naive females did utilize a previously parasitized host. The lack of an innate ability or willingness to avoid low quality hosts in C.flavipes may be due to the constrained opportunities to find and parasitize hosts. Each animal faces a evolutionary trade off between reproducing now or in the future, whereby survival chances play a determining role. The best strategy for a recently emerged naive female C.flavipes is to accept the first encountered host, irrespective its quality. Superparasitism pays when future expectancy of host encounter rate is very low. The lower fitness increment of superparasitism (in comparison with single parasitism) will always outweigh the fitness penalty of not finding any unparasitized host.In chapter 5 it is demonstrated, however, that females with oviposition experience do avoid previously utilized stemborer tunnels. The increased choosiness after an oviposition experience in an unparasitized host may be due to the fact that, the parasitoids assessment of host availability has changed. When there is a high chance of finding unparasitized hosts it does pay to reject. Furthermore, in contrast to naive females, oviposition experienced females that superparasitize run the risk to encounter a host they themselves previously parasitized (Van Alphen and Visser, 1990). A safe strategy of females that have already parasitized one or more hosts may be to avoid any already parasitized host to avoid competition among her own progeny.VARIATION IN PARASITOID BEHAVIOR AND BIOLOGICAL CONTROLIn biological control the performance of a released parasitoid population in the field is dependent on the ability of individual females to locate hosts. The behaviour of parasitoids is not fixed and predictable, but most of the times highly variable. This variation in behaviour can be an obstacle in the effective use of natural enemies in biological control, so it is necessary to understand the sources of variation in behavior (Vet et al., 1990; Lewis et al., 1990). In this way we can predict the general behavior of the natural enemy population in the field better and we may even be able to manipulate it.Behavioral variation may exist because individuals differ genetically in propensity to find or accept different hosts. Secondly, individuals may differ because they have experienced different environments (i.e. learning).Local variation in parasitoid behavior and physiologyThe existence of plant specific strains in C.flavipes has been postulated by Mohyuddin and coworkers (e.g. Mohyuddin et al., 1981; Mohyuddin, 1990). However, the genetic and/or phenotypic basis for this reported specificity has never been addressed thoroughly. For instance, early adult conditioning can mimic genetic differences between parasitoid strains. However, in chapter 5 we demonstrated that there is no early adult conditioning for the development and emergence environment in C.flavipes , indicating innate (genetic) differences among strains. Therefore, the between population variation in behavior and physiology of C.flavipes populations was investigated in more detail in chapter 6 . The host selection behavior and physiological compatibility with different stemborers (i.e. parasitoid virulence) was compared for six different geographic strains of C.flavipes that differed in the plant-host-complex they were obtained from. The results of these host selection experiments indicated that there is no interspecific variation in host selection behavior among C.flavipes strains, which contradicts the finding of the Mohyuddin research group. However, the comparative experiments did show variation in reproductive success among strains. The most significant result was that the strain with the longest co- existence time with the new host D. saccharalis , had the highest reproductive success on this host species. It is argued that the earlier reported existence of C.flavipes strains is not based on a differential host selection behavior, but on differences in physiological compatibility between local parasitoid and host population. C.flavipes has beenused on a worldwide scale in biological control against stemborers with varying degree of success (Polaszek and Walker, 1991). The failure of biological control with C flavipes may be due to the introduction of an inappropriate strain. The present study has demonstrated that there is no differential plant preference among strains, but that there are differences in parasitoid virulence among strains. For a reliable biological control with C flavipes it is thus important to select a strain that is physiologically adapted to the target host population.
... Esse processo de resposta imunológica torna-se mais eficiente à medida que a lagarta vai se desenvolvendo, sendo que lagartas hospedeiras dos últimos ínstares apresentam maior capacidade de encapsulação (Hu et al., 1986;Vet, 1995). A baixa capacidade de encapsulação dos hospedeiros nas fases iniciais e, consequentemente, a maior adequabilidade de lagartas de 2 o e 3 o ínstares, como a observada neste trabalho (Tabela 2), assemelham-se aos resultados observados por Geervliet et al. (1993) e por Mattiacci;Dicke (1995) com essa espécie de parasitoide utilizando como hospedeiro lagartas de P. brassicae, P. rapae e P. rapi, havendo preferência do parasitoide por hospedeiros nos ínstares iniciais. Em lagartas de A. monuste orseis, Cunha (1983) também observaram preferência para o parasitismo de A. yerzia nos 3 primeiros ínstares; contudo, esses autores obtiveram uma maior porcentagem de parasitismo (50%), quando comparada com os resultados do parasitismo médio deste trabalho (26,8%). ...
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The study aimed to adapt the instar of host Ascia monuste orseis to the parasitism of Cotesia glomerata and evaluate the parasitoid performance. Females of C. glomerata were exposed to 2nd, 3rd, 4th and 5th instars larvae of A. monuste orseis , allowing parasitism for two hours. Subsequently, the development of caterpillars that were fed with leaf sections of kale was monitored. The duration of each caterpillar instar, the weight of four days-old pupae, the percentage of parasitized caterpillars and mortality were assessed. Despite parasitoids, the following parameters were assessed: percentage of parasitism; number of parasitoids per host; percentage of emergence, sex ratio; average weight of the pupae, number of parasitoids per caterpillar; period egg-pupae; pupal period; and period egg-adult. The results indicated that the second instar of host A. monuste oreseis is the most suitable for the parasitism of C. glomerata for providing highest percentage of parasitism and a larger number of offspring per host.
... cies showing different spatial distribution patterns. However, a description of interspecific variation, based on an accurate phylogenetic approach, has never been conducted. Only a few studies have been undertaken to compare the foraging behaviour of related parasitoid species (Vet & Bakker 1985; Vet & van Alphen 1985; Poolman Simons et al . 1992; Geervliet et al . 1993; Vet et al . 1993 ). However, as far as patch time allocation is concerned , only Vos, Hemerik & Vet (1998) compared two Cotesia species (Hymenoptera: Braconidae), one specialist and one generalist, and a difference in the patchleaving decision rules adopted by these two species was discovered. The phylogenetic history of a species is ne ...
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Summary • The proximate behavioural rules adopted by parasitoid females to manage their foraging time on patches of hosts were studied, under standardized laboratory conditions, in different species (and populations) of the Trichogrammatidae (Hymenoptera) family. • Seventeen species/populations were compared and the behavioural mechanisms adopted by the females were identified by means of a Cox's proportional hazards model. • On average, females increased their patch-leaving tendency each time a healthy host was attacked and each time a parasitized host was rejected. • Strong variation was observed in these patch-leaving mechanisms among the different species. • Moreover, the interspecific variation in these two behavioural mechanisms showed a significant positive correlation, and this correlation remained significant when the phylogenetic relationship between the strains was controlled with the use of phylogenetic comparative methods. • The adaptive and evolutionary meanings of these results are probably related to the ecological features and distribution patterns of the hosts attacked by the species/populations compared.
... Papaj 1986) or compare the learning abilities of different species (macro-evolutionary approach). The macro-evolutionary approach has been used for instance to compare the learning abilities of specialist and generalist parasitoids (Poolman Simons et al. 1992;Geervliet et al. 1993;Vet et al. 1995). A species comparative approach can also be used for parasitoids attacking stemborer larvae. ...
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Parasitic wasps are commonly found to learn olfactory and visual cues that are associated with successful host location. For many parasitoids the cues that are associated with hosts vary in space and time, and are therefore unpredictable. An ability to learn allows the wasp to concentrate on those cues that will lead it to new hosts most effectively in a particular area. In contrast, parasitoids that forage in a predictable homogeneous environment and/or make only a few foraging decisions do not need to learn and should rely on innate responses to specific cues. The role of learning in host foraging was studied in Cotesia flavipes (Hymenoptera: Braconidae), a parasitoid of stemborer larvae with an ecology where learning is expected to be of low adaptive value. There was no evidence that C. flavipes uses odour learning in host-micro-habitat location. There was no significant effect of the development and emergence environment on the response level or preference towards the odour of infested plants. Neither was there evidence that experience with a particular plant-host complex during foraging influences subsequent foraging decisions in C. flavipes females. The absence of learning in C. flavipeswhich seems an exception among the parasitoids studied, is discussed in relation to its ecology.
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Some parasitoids are restricted with respect to the host stage that they attack and even to a certain age within a stage. In this paper we investigate whether the parasitoid Cotesia glomerata can discriminate between old and young caterpillar instars of its host, Pieris brassicae, before contacting these hosts, since contacts with older instars are very risky with a chance of being killed, due to the aggressive defensive behaviour of the caterpillars. Flight chamber dual choice tests showed that volatile chemicals emitted by Brussels sprouts plants (Brassica oleracea var. gemmifera) after feeding damage by 1st and 5th larval instars are equally attractive to the wasps. Simulated herbivore damage by 2nd and 5th larval instars, obtained by treating mechanically damaged leaves with carterpillar regurgitant, was also equally attractive, even when the wasps were exposed to repeated experience on different larval instars to increase their discriminatory ability. In contrast, single choice contact bioassays showed that the time spent searching on a leaf with feeding damage of 1st instar larvae was significantly longer than the time spent on 5th instar feeding damage or on mechanically damaged leaves. Both flight and contact bioassays did not show any effect of egg-related infochemicals. The results demonstrate that C. glomerata can discriminate between young and old larval instars of P. brassicae, without contacting the caterpillars. This is not done through volatile herbivore-induced synomones but through cues that are contacted after arrival at a caterpillar-infested leaf.
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The role of volatile infochemicals emitted by feces of larvae in the host-searching behavior of the parasitoidCotesia rubecula was evaluated during single- and dual-choice tests inside a wind tunnel. The following treatments were tested: feces produced by second and fourth instars ofPieris rapae (preferred host), second instars ofP. brassicae (inferior host), second instars ofP. napi (nonhost), and wet feces of second instars ofP. rapae. During a single-choice situation females ofC. rubecula oriented to all types of feces tested. When a preference was to be made,C. rubecula preferred feces of second instars ofP. rapae over that of fourth, feces ofP. rapae over that ofP. brassicae, feces ofP. napi over that ofP. brassicae, and wet over normal host feces. No preference was exhibited between feces of second instars ofP. napi and that of second instars ofP. rapae. The relative importance of infochemicals from host feces versus plant damage caused by host larvae to the searching behavior ofC. rubecula was also evaluated. Plant damage was more important to the searching females than host feces when feces were present in specific concentrations in relation to damage. The volatiles released by normal and wet feces of second instars ofP. rapae, wet feces of fourth instars ofP. rapae, and normal and wet feces ofP. brassicae were collected and identified. Overall, 85 chemical compounds were recorded belonging to the following chemical groups: alcohols, ketones, aldehydes, esters, isothiocyanates, sulfides, nitriles, furanoids, terpenoids and pyridines. The blend of chemicals emitted by feces of different instars ofP. rapae and different species ofPieris exhibited an instar and species specificity in both quantity and quality. Wetting of normal feces increased the amount of volatile chemicals released, and it was also responsible for the appearance of new compounds. The role of feces of larvae in the host-seeking behavior ofC. rubecula is discussed.
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In the present study we apply a comparative approach, in combination with experimentation, to study behavior of two parasitoid species that attack caterpillar hosts with different feeding strategies (gregarious or solitary). In a semifield setup, consisting of clean cabbage plants and plants infested with one of two host species, the foraging behavior of the specialistCotesia rubecula, on obligate parasitoid of solitarily feedingPieris rapae larvae, was compared to that of the generalistCotesia glomerata, a polyphagous parasitoid of several Pieridae species (mainly the gregariously feedingPieris brassicae).Cotesia glomerata displayed equal propensity to search for and parasitize larvae of both host species. AlthoughC. glomerata exhibited a relatively plastic foraging behavior in that it searched differently under different host distribution conditions, its behavior seems more adapted to search for gregariously feeding hosts. Females exhibited a clear area-restricted search pattern and were more successful in finding the gregariously feeding caterpillars.Cotesia rubecula showed a higher propensity to search forP. rapae than forP. brassicae, i.e., females left the foraging setup significantly earlier when their natural hostP. rapae was not present.C. rubecula showed a more fixed foraging behavior, which seems adapted to foraging for solitarily feeding host larvae. In a setup with onlyP. rapae larvae, the foraging strategies of the two parasitoid species were quite similar. In a choice situationC. glomerata did not show a preference for one of the host species, whileCotesia rubecula showed a clear preference for its natural host species. The latter was shown by several behavioral parameters such as the number of first landings, allocation of search time, and percentage parasitization.
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