Response of the parasitoidEupelmus vuilleti to the odours of the phytophagous host and its host plant in an olfactometer

Eupelmus vuilleti (CRW) is a solitary ectoparasitoid which, under our experimental conditions, developed at the expense of the larvae and pupae ofBruchidius atrolineatus (Pic) (Coleoptera, Bruchidae). The larvae of this beetle are found inside the seeds of cowpea,Vigna unguiculata (Walp). Using a tubular olfactometer, we determined the olfactory stimuli involved in the orientation of females of the hymenopterous speciesE. vuilleti towards one of its hosts;B. atrolineatus. Several odours were tested including those from host plants ofB. atrolineatus, from non-host plants, from the host itself and from the waste products of the host. The odours of pods or dry seeds ofV. unguiculata (host plant of the phytophagous insect) affected the locomotor behaviour of females ofE. vuilleti. The odours from the plant in the vegetative stage had no effect. Kairomones from larvae, pupae or faeces ofB. atrolineatus were attractive to the parasitoid females. Odours from adult male or femaleB. atrolineatus, as well as the sex pheromone emitted by females were not attractive toE. vuilleti females. This sex pheromone did however stimulate the locomotor activity of the parasitoid. The adaptive significance of these olfactory stimuli is discussed.

---

Résumé Eupelmus vuilleti (CRW) est un ectoparasito?de solitaire qui se développe dans nos conditions expérimentales aux dépens des larves et des nymphes deBruchidius atrolineatus (Pic) (Coléoptère:Bruchidae). Les larves de ce Coléoptère se trouvent à l'intérieur des graines d'une LégumineuseVigna unguiculata (Walp). Grace à un olfactomètre tubulaire, nous avons déterminé les différents stimuli olfactifs intervenant dans l'orientation des femelles de cet hyménoptère, vers l;un de ses h?tes;Bruchidius atrolineatus. Plusieurs odeurs émanant soit de plantes-h?tes ou nonh?tes deB. atrolineatus, soit de l'h?te lui-même ou résultant de son métabolisme ont été testées. Les odeurs de gousses ou de graines sèches deVigna unguiculata Walp (plante-h?te du phytophage) influencent le comportement locomoteur des femelles. Par contre, les odeurs de plantes au stade végétatif n'ont pas d'effet. Les kairomones émanant de larves, nymphes ou fèces de larves deB. atrolineatus exercent un effect attractif sur les femelles parasito?des. Les odeurs émanant d'adultes males ou femelles deB. atrolineatus ainsi que la phéromone sexuelle émise par les femelles ne sont pas attractives pour les femelles deE. vuilleti. Cette phéromone sexuelle, par contre, stimule l'activité locomotrice des parasito?des. La signification adaptative de ces différents stimuli olfactifs est discutée.

     

Influence of pre-emergence experience on response to host and host plant odours in the larval parasitoidEupelmus vuilleti

The response to different host and plant species odours was investigated inEupelmus vuilleti (Crw). This hymenopteran is a solitary ectoparasitoid of several species of bruchids developing inside Leguminosae seeds. The locomotor behaviour of females reared onBruchidius atrolineatus (Pic) larvae developing inVigna unguiculata (Walp) seeds was analysed using a tubular olfactometer. Females showed a specific sensitivity to the semiochemicals emanating from the host and the seed species on which they had developed. Odours fromV. unguiculata seeds were attractive to the parasitoid and stimulated their locomotor activity. Odours fromVigna radiata (Wil) seeds had no effect on the locomotor behaviour. Odours fromB. atrolineatus larvae were attractive to the females whereas odours fromCallosobruchus maculatus (Fab), another bruchid species, had no effect. By isolating the females from the seed and the host at different developmental stages, we found that the specific sensitivity observed resulted from an early adult learning. This learning which occurs before the emergence from the seed while the imago is in the larval chamber of its host is dependent on contact with the seed and the host larval remains.     

Interspecific Relations Between Two Sympatric Species of Hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Crw), Ectoparasitoids of the Bruchid Callosobruchus maculatus (F)

Dinarmus basalis (Rond) and Epelmus vuilleti (Crw) are two Hymenopteran species, which are solitary ectoparasitoids of bruchid larvae. In the presence of seeds of Vigna unguiculata (Walp) containing hosts parasitized by E. vuilleti, a high percentage of D. basalis females avoided multiparasitism whatever the age of the eggs or the larvae present on the host. The least avoidance was observed when the hosts were parasitized by E. vuilleti 30 min beforehand. This avoidance behavior is adaptive and is related to the low survival chances of the D. basalis larvae when they are in interspecific competition with E. vuilleti larvae. The analysis of the behavior of D. basalis demonstrated that the avoidance of multiparasitism could be due to the perception of two signals; an external signal deposited on the surface of the seeds during the E. vuilleti oviposition phase and an internal signal due to the presence of the eggs and larvae at the surface of the hosts. E. vuilleti females did not avoid multiparasitism and multiparasitized the hosts bearing D. basalis eggs or larvae. The behavior of E. vuilleti females was not disturbed by the presence of its competitor. Under these conditions of interspecific competition, the survival chances of E. vuilleti larvae were very high whatever the age of its competitor D. basalis. The two species of parasitoids could move in a column containing healthy seeds of V. unguiculata and patches with seeds containing parasitized or unparasitized larvae. The distribution of D. basalis females introduced into these columns depended on the host quality. They avoided the patches containing the hosts parasitized E. vuilleti and were found in the patches with healthy hosts. The behavior of E. vuilleti females was very different; the distribution of the females and the parasitism and multiparasitism rates were not affected by the quality of the hosts present in the patches. The adaptive significance of the behaviors of these two species was analyzed in relation to the survival chances of their offspring.     

Competition for hosts between two hyperparasitoids of aphids,Dendrocerus laticeps andDendrocerus carpenteri (Hymenoptera: Megaspilidae): The benefit of interspecific host discrimination

The two hyperparasitoids of aphids, Dendrocerus carpenteri(Curtis) and Dendrocerus laticeps(Hedicke), differ in their interspecific host discrimination behavior: D. carpenterireadily accepts hosts for oviposition previously parasitized by D. laticeps,whereas D. laticepsoften refrains from ovipositing on hosts previously parasitized by D. carpenteri.The two species also differ in their competitive abilities: D. carpenteriis competitively superior to D. laticepswhen the time between ovipositions is 1 h. D. carpenteri's superiority probably arises from (a) the action of the venom produced by the female to paralyze the host, as evidenced by the comparison of emergence patterns from naturally vs artificially parasitized hosts, and (b) its more rapid egg development. Because of its competitive abilities, D. carpenterigains only limited benefit from discriminating interspecifically, at least when encountering a host parasitized by a competitively inferior species, such as D. laticeps.In contrast, D. laticepsgains considerable benefit from recognizing hosts previously parasitized by D. carpenteri,as the probability to produce offspring from such hosts is greatly reduced.     

Influence of adult experience on host microhabitat location by the generalist parasitoid,Campoletis sonorensis (Hymenoptera: Ichneumonidae)

The effect of adult experience on microhabitat location behavior of the generalist parasitoid Campoletis sonorensis (Cameron)was examined in a wind tunnel bioassay. Responses were tested to the odors of two host plants (cotton and sesame) of Heliothis virescens (F.) or a nonhost plant (potato), either damaged and infested with host larvae and host products (host/plant complex) or intact, clean and uninfested. Parasitoid females remained naive or were allowed one oviposition experience on either of the plants, 1 min, 2 h, or 24 h prior their introduction into the wind tunnel. In a no-choice test, parasitoids experienced 1 min prior to bioassay completed significantly more flights to sesame and potato host/plant complexes than did naive parasitoids. However, 24 h after experience, only females experienced on potato completed more flights to the host/ plant complex than did naive females. Parasitoids experienced 1 min prior to flight to undamaged plants showed a slight increase in flight response (significant only for potato) but, after 24 h, completed only as many flights as naive parasitoids. In a dual-choice situation, parasitoids did not show a preference for either of the two host plants but did prefer a host to a nonhost plant. This innate plant preference was not changed by a single oviposition experience. The potential significance of these results to the microhabitat location behavior of C. sonorensisin the field is discussed.     

Postemergence learning in the insect parasitoid,Cotesia congregata (Say) (Hymenoptera: Braconidae)

Exposing newly emerged females of Cotesia congregata(Say) to wild cherry, an inherently unattractive plant, and their host larvae at 0–4 h after adult emergence induced a positive searching response to wild cherry and an inhibited response to cabbage, an attractive plant. Inherent responses were not affected when females were exposed to their hosts at 0–12 h and to cherry at 8–12 h after emergence. The induced response to cherry was constant until its disappearance at 6–7 days;inhibition of the response to cabbage was released at 4–5 days after emergence. Postemergence exposure to cherry and parasitoid cocoons induced similar but weaker searching responses. Induced searching responses exhibit features of associative learning and receptor modification. In addition to its presumed role in foraging, postemergence experience with plants may encourage assortative mating of C. congregatawithin suitable host habitats and, thus, facilitate local adaptations to specific plants.     

Olfactory host location and learning in the granary weevil parasitoidLariophagus distinguendus (Hymenoptera: Pteromalidae)

The sources of volatiles that attract the parasitoid Lariophagus distinguendus(Först.) to its hosts, the larvae of the granary weevil Sitophilus granarius(L.) infesting grains of Triticum aestivumL., were investigated in bioassays. The influence of oviposition experience on the responsiveness of the parasitoids to the sources of volatiles was considered. The potential sources of attractants are the host larvae, their feces, and the grain infested by the host. Weevil larvae were not attractive. Feces were attractive to females without and females with oviposition experience. Infested grains from which the larvae and feces were removed were slightly attractive to inexperienced, but very attractive to experienced females. Healthy and artificially damaged grains were attractive to experienced parasitoids only. Refering to the “variable response model,” we discuss the effect of experience on the response of the parasitoids to the several stimuli. Stimuli from different trophic levels are used by the foraging parasitoids: feces of the host larvae is an important source of attractants, but also the grains, particularly after experience.     

Adult experience modifies attraction of the leafminer parasitoidOpius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals

Oviposition-experienced females of Opius dissitus Muesebeck, a braconid parasitoid of Liriomyza sativaeBlanchard, preferentially landed on leafminer-infested rather than uninfested lima bean (Phaseolus lunatus L.) plants in a flight tunnel assay. Both naive and oviposition-experiencedparasitoids responded strongly to odors of infested lima bean plants in a four-arm olfactometer in comparison with odors of uninfested plants, suggesting that volatile semiochemicals are used in host location. Parasitoids with an oviposition experience on lima bean (lima-experienced) spent significantly more time in the infested odor than naive individuals, however, eggplant-experienced wasps did not spend significantly more time in the infested odor field than naive wasps. When parasitoids reared on leafminers in lima bean were provided a choice between the odor of infested lima bean and the odor of infested eggplant or cotton, naive and lima-experienced wasps preferred infested lima odor. An oviposition experience on the other plant species resulted in a dramatic shift in preference. It was concluded that the experience effect was due, at least in part, to associative learning, as has been reported for other parasitoids. The parasitoids may perceive unconditioned stimuli during host contact and oviposition on an infested leaf and may associate those stimuli with volatile semiochemicals emanating from the leaf or host. Subsequently, the volatiles associated with the presence of hosts are used in directing the search for hosts.     

Influence of physiological state and experience on the responsiveness ofLysiphlebus testaceipes (Cresson) (hymenoptera: aphidiidae) to aphid honeydew and to host plants

The effect of physiological state (hunger) and experience on the responsiveness of the aphid parasitoid, Lysiphlebus testaceipes(Cresson), to clean and honeydew-contaminated host plants was investigated in laboratory bioassays. Both fed and unfed parasitoids spent significantly longer examining honeydew-contaminated plants compared to uncontaminated controls, but the presence of honeydew did not influence attack latency (i.e., the speed with which naive parasitoids found and attacked hosts). Hunger, however, had a significant negative effect on attack latency, presumably as a result of a physiologically based shift from host- to food-location behavior in starved parasitoids. The parasitoid 's response to clean plants was significantly increased as a result of classical conditioning procedures, whereas the response to honeydew-contaminated plants was not.     

Analysis of multiparasitism by Eupelmus vuilleti (Craw) (Eupelmidae) and Dinarmus basalis (Rond) (Pteromalidae) in the presence of one of their common hosts,Bruchidius atrolineatus (Pic) (Coleoptera Bruchidae)

Bruchidius atrolineatus (Pic) is a tropical beetle (Coleoptera Bruchidae) that develops during the larval and pupal stages in the seeds of a legume Vigna unguiculata (Walp). Two species of Hymenoptera, Dinarmus basalis (Rond) and Eupelmus vuilleti (Craw), solitary ectoparasitoids of the larvae and pupae of B. atrolineatus, were introduced successively in the presence of their hosts, varying the interval between the two introductions. When D. basalis females were introduced 24 h, 3 days or 7 days after E. vuilleti, multiparasitism was low. The females had low fecundity, and their eggs were not distributed randomly over the different available hosts. When E. vuilleti females were introduced second, they oviposited on the different hosts availabe and did not avoid multiparasitism. The presence of hosts already parasitised by D. basalis increased the reproduction of E. vuilleti, and the fecundity of the females was higher than in control batches with E. vuilleti alone. E. vuilleti seems capable of detecting the ovipositor shafts drilled by the D. basalis females, and by introducing its own ovipositors killing the D. basalis eggs or larvae. When interspecific competition was occurring the number of E. vuilleti adults emerging from the seeds was no different from that observed in control batches with E. vuilleti alone, and there were always fewer D. basalis adults than in control batches (D. basalis alone). This interspecific competition reduces the influence of the two parasitoids in the biological control of bruchid populations.     

Influence of Liriomyza species (Diptera: Agromyzidae) and their host plants, on oviposition by Opius dissitus females (Hymenoptera: Braconidae)

Two factors, among others, influence the oviposition of Opius dissitus Muesebeck. The first was the host species, the second the plant upon which the pest host larvae develop. O. dissitus females prefer Liriomyza trifolii (Burgess) larvae over those of L. huidobrensis (Blanchard). O. dissitus females were more attracted to the larvae of L. trifolii or L. huidobrensis when these were present on courgette rather than tomato or lettuce.     

Effect of experience on host preference inCallosobruchus maculatus (Coleoptera: Bruchidae): Variability among populations

Experiments using naive females established differences in host specificity among geographic strains of the seed beetleCallosobruchus maculatus; some females strongly preferred azuki bean over mung bean, and others failed to discriminate between the two hosts. We examined whether such congenital differences affect the degree to which host preference can be modified by experience. In choice tests, previous exposure to azuki bean increased the proportion of eggs laid on that host, but only in strains with a relatively low host specificity. Under more realistic, no-choice conditions, egg-laying experience affected oviposition rates mostly in strains with a high host specificity, but these experiments could not distinguish between the effects of a female's experience per se and her physiological state (i.e., egg load). Our results indicate that the likelihood of detecting an effect of experience on host choice depends on both the experimental protocol and the source of the test population. In natural populations ofC. maculatus, recent egg-laying experience probably plays little or no role in discrimination between host species but may influence discrimination between conspecific seeds that differ in quality.     

The role of learning in adult food location by the larval parasitoid,Microplitis croceipes (Hymenoptera: Braconidae)

Wind tunnel experiments were conducted to determine roles of odor learning in food foraging of the larval parasitoid,Microplitis croceipes (Hymenoptera: Braconidae). Females that had neither fed on sucrose water nor experienced any odor and females that had experienced an odor without feeding failed to respond to any odors in a wind tunnel. Most of the females that had fed without an odor also did not respond to odors. However, most of the females that had experienced an odor during feeding on sucrose water flew to the odor. These results indicate that when females experience an odor during feeding, they learn to associate the odor with food and subsequently respond to the odor. As age of females increased, their response to an experienced odor increased, peaked 2 to 5 days after emergence, and then decreased. With an increasing number of odor experiences while feeding, accuracy of females choosing the experienced odor increased. Females that experienced an odor while feeding three to five times chose the experienced odor 90% of the time. When females experienced an odor while feeding five times, the memory of food associated odor lasted at least 2 days. When they experienced food with two odors successively, they could memorize both odors, and multiple experiences did not cause memory interference. Even when females had learned a food-associated odor, their response to the learned odor ceased after several visits on patches containing the odor but no food. Such negative experience may cause switching of food searching to new odors by females.     

Chemically mediated associative learning in the host foraging behavior of the aphid parasitoidAphidius ervi (Hymenoptera: Braconidae)

The effect of experience on the responsiveness of the braconid parasitoidAphidius ervi to host(Acyrthosiphon pisum)-associated cues was investigated on bean plants(Vicia faba) using a wind tunnel bioassay. Oviposition experience on the plant-host complex significantly increased the oriented flight and landing responses ofA. ervi females to an undamaged plant and to a plant-host(A. pisum) complex. However, oviposition experience onA. pisum aphids when isolated from the plant did not change their responses to the intact plant and the complex. Searching on an unwashed plant which had been previously damaged byA. pisum also increased their response to an undamaged plant and a host-damaged plant, whereas the experience of searching on an undamaged plant did not significantly change their responses to undamaged plants. However, when parasitoids were allowed to search on an undamaged plant which had been sprayed withA. pisum honeydew, this significantly increased their response to an undamaged plant. Oviposition experience on the plant-host complex and foraging experience on a host-damaged plant or an undamaged plant sprayed with honeydew also significantly reduced the mean time taken by the parasitoids to respond in the wind tunnel. The behavioral changes associated with such experience were acquired within 30 min and persisted for at least 3 days. The results demonstrate the capacity ofA. ervi to learn associatively olfactory cues from plants, host-damaged plants, and plant-host complexes and confirm the role of aphid honeydew as a host recognition kairomone forA. ervi.     

Effect of temperature on reproduction and parasitism of the egg parasitoid,Anastatus orientalis (Hymenoptera: Eupelmidae)

Anastatus orientalis is a solitary endoparasitoid of Lycorma delicatula (Hemiptera: Fulgoridae) eggs. We investigated the development, longevity, fecundity, and sex ratio of A. orientalis on different temperatures to establish the optimal temperature condition for laboratory mass rearing. There were significant differences in its development and longevity between 15 °C and the rest of temperature conditions (20, 25, and 30 °C), among which were no significant differences. The average number of eggs laid by A. orientalis was higher at 20 and 25 °C, but there was no statistically significant difference in its fecundity between the two temperatures. More females emerged at 15 and 20 °C than higher temperatures.Parasitisms of A. orientalis varied with host egg ages and densities. Even in 14 day old eggs of L. delicatula, parasitoids successfully emerged from 92.3% of the parasitized eggs. On the other hand, parasitism was lowest (13.8%) on just before hatching eggs. Parasitism was negatively dependent on host density.Oviposition behavior for A. orientalis primarily occurred at 1400–1600 h, not at 2400–0800 h. The majority of this parasitoid's emergence occurred at 0800–1000 h, largely before noon. These results may be useful for controlling the adequate time for supplying host eggs and release density of this parasitoid as well as for potentially predicting the accurate time for securing parasitoid adults in laboratory mass rearing of A. orientalis.     

Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) response to relative humidity with and without host cues

Trichogramma ostriniae is a parasitoid wasp species that is used as a biological control for several lepidopteran agricultural pests. Our study examined the effects of relative humidity (RH) on the behaviour of female T. ostriniae. In Y-tube RH choice assays, wasps generally chose higher RH over lower RH but the latency time taken to make a choice displayed no clear patterns that could be ascribed to the magnitude of the RH difference between arms of the Y-tube. In trials conducted in glass arenas with fixed humidities, the conditional probabilities of transition from searching to interacting with the leaf disk, and from interacting with leaf disks to antennal egg drumming and oviposition, were not significantly different among the RH levels, nor were there differences in latency times. These findings suggest that the level of RH may influence habitat choice but have little effect on search efficacy.     

Influence of host behavior and host size on the success of oviposition ofCotesia urabae andDolichogenidea eucalypti (Hymenoptera: Braconidae)

Behavioral interactions among Cotesia urabaeAustin and Allen, Dolichogenidea eucalyptiAustin and Allen (Hymenoptera: Braconidae), and their host Uraba lugensWalker, the gum leaf skeletonizer (Lepidoptera: Noctuidae), were observed at three host sizes over a 20-min period. These sizes were first instar (small, gregarious), fourth-fifth instar (mid, gregarious), sixth-seventh instar (large, solitary) larvae. Unlike C. urabae, D. eucalyptiused its legs to hold small larvae before ovipositor insertion. D. eucalyptialso visited patches of small larvae more frequently, proceeded less often through patches of mid larvae, and made significantly fewer ovipositions in mid and large larvae. Small larvae responded to both parasitoids by dispersing outward, while mid larvae responded to parasitoids by moving inward to form a denser group. Larvae reared or thrashed after each parasitoid visit, especially mid larvae, and some continued to do so for up to 2h after parasitoid departure. Mid and large larvae occasionally injured parasitoids by biting their appendages. By rearing or thrashing immediately prior to an encounter with a parasitoid, mid and large larvae decreased the likelihood of being parasitized by up to 50%.     

Ovipositional response ofVenturia canescens (Grav.) (Hymenoptera: Ichneumonidae) to various host and parasite densities

Summary Ovipositional response inVenturia canescens (Grav.) parasitizingAnagasta kühniella (Zeller) is analyzed for all combinations of five parasite densities (2, 5, 10, 25, and 50), four host densities (25, 50, 100, and 200), and three floor area universe sizes (76 cm², 160 cm², and 345 cm²). Over this range, no mutual interference (as measured by decreasing parasite fecundity) was observed, althoughNicholson’s area of discovery decreased significantly with parasite density increase as a result of a non-Poisson distribution of parasite eggs; use of this parameter is therefore not a suitable means of determining if mutual interference is present. Other parameters studied, and for which significant correlations were obtained, include mean parasite eggs per host, percentage parasitization, percentage of parasite eggs wasted, and negative binomialk approximations. This study was conducted as part of a broad investigation into the processes operating in the dynamics of arthropod populations under a grant toC. B. Huffaker by the U.S. Public Health Service, National Institutes of Health.     

Segregation of temporal and spatial distribution between kleptoparasites and parasitoids of the eusocial sweat bee, Lasioglossum malachurum (Hymenoptera: Halictidae, Mutillidae)

Cuckoo bees and velvet ants use different resources of their shared host bees, the former laying eggs on the host pollen stores and the latter on immature stages. We studied the activity patterns of the cuckoo bee Sphecodes monilicornis and the velvet ant Myrmilla capitata at two nesting sites of their host, the social digger bee Lasioglossum malachurum , over a 3 year period. Due to the difference in host exploitation, we expected different temporal patterns of the two natural enemies as well as a positive spatial association with host nest density for both species. At a daily level, S. monilicornis was more abundant between 10.00 and 15.00 h, while M. capitata was most active in the early morning and late afternoon; both species activities were independent from host provisioning activity. The activity of cuckoo bees was in general positively correlated with the density of open host nests (but not with the total number of nests), while that of velvet ants was rarely correlated with this factor. Sphecodes monilicornis was seen both attacking the guard bees and directly entering into the host nests or digging close to nest entrances, while M. capitata only gained access to host nests through digging. We conclude that the temporal and spatial segregation between the two species may be, at least partially, explained both by the different resources exploited and by the different dynamics of host interactions.