Interaction of vibrational and visual cues in parasitoid host location

Female parasitoids are guided by multisensory information during host finding. Individual cues are used in an interactive or a hierarchical manner according to the relative importance on the spatial scale of their effect. Unlike most studies that concentrate on single cues, the present paper investigates the interaction of two physical cues. The interaction of mechanosensory and visual cues was studied in the pupal parasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae). This species uses, amongst other senses, vibrational sounding (echolocation in a solid substrate) to find its mainly endophytic hosts. Location and frequency of ovipositor insertions were scored on cylindrical plant stem models with single or combined cues. Single-cue experiments show that parasitoids use both visual and mechanosensory cues and achieve a similar precision of host location with either cue. The combination of vision and vibrational sounding increased the precision of host location by a factor of approximately two to three. We conclude that the two senses interact, resulting in an additive accuracy. Neither the visual nor the mechanosensory cue was favored when offered adjacent to each other on the same stem model. On the investigated spatial scale, both physical cues are used and seem to be equally important for host location in this species.     

Ambient temperature affects mechanosensory host location in a parasitic wasp

Certain parasitic wasps (Ichneumonidae, Pimplinae) use self-produced vibrations transmitted on plant substrate to locate their immobile concealed hosts (i.e. lepidopteran pupae). This mechanosensory mechanism, called the vibrational sounding, depends both on physical cues of the environment and physical activity of the parasitoid and is postulated to depend on ambient temperature. We analysed the influences of temperature on vibrational sounding by choice experiments using plant-stem models with hidden host mimics in the temperate species Pimpla turionellae. The results show a significant effect of temperature on host-location activity and on the success of this process. Outside an optimum range, the performance of the wasps decreased both at low and high temperatures. Below 10°C and beyond 24°C, the wasps displayed (1) substantial reduction in responsiveness, i.e. proportion of females showing ovipositor insertions, (2) reduction of quantitative activity with ovipositor insertions in the individuals, and (3) reduced precision of mechanosensory host location. Nevertheless, female wasps were able to locate their host over a surprisingly broad range of ambient temperatures which indicates that the wasps are able to compensate for temperature effects on vibrational sounding.     

Efficiency of vibrational sounding in parasitoid host location depends on substrate density

Parasitoids of concealed hosts have to drill through a substrate with their ovipositor for successful parasitization. Hymenopteran species in this drill-and-sting guild locate immobile pupal hosts by vibrational sounding, i.e., echolocation on solid substrate. Although this host location strategy is assumed to be common among the Orussidae and Ichneumonidae there is no information yet whether it is adapted to characteristics of the host microhabitat. This study examined the effect of substrate density on responsiveness and host location efficiency in two pupal parasitoids, Pimpla turionellae and Xanthopimpla stemmator (Hymenoptera: Ichneumonidae), with different host-niche specialization and corresponding ovipositor morphology. Location and frequency of ovipositor insertions were scored on cylindrical plant stem models of various densities. Substrate density had a significant negative effect on responsiveness, number of ovipositor insertions, and host location precision in both species. The more niche-specific species X. stemmator showed a higher host location precision and insertion activity. We could show that vibrational sounding is obviously adapted to the host microhabitat of the parasitoid species using this host location strategy. We suggest the attenuation of pulses during vibrational sounding as the energetically costly limiting factor for this adaptation.     

Temperature affects interaction of visual and vibrational cues in parasitoid host location

Parasitoid host location in nature is facilitated by simultaneously using different information sources. How multisensory orientation on the same spatial scale is influenced by environmental conditions is however poorly understood. Here we test whether changes in reliability of cues can cause parasitoids to alter multisensory orientation and to switch to cues that are more reliable under extreme temperatures. In the ichneumonid wasp Pimpla turionellae, multisensory use of thermally insensitive vision and thermally sensitive mechanosensory host location by vibrational sounding (echolocation on solid substrate) was investigated with choice experiments on plant-stem models under optimum temperature (18°C), at high- (28°C) and low-temperature limits (8°C) of vibrational sounding. Temperature affected relative importance of vibrational sounding whereas visual orientation did not vary. At 18°C, parasitoids used visual and vibrational cues with comparable relative importance. At 8 and 28°C, the role of vibrational sounding in multisensory orientation was significantly reduced in line with decreased reliability. Wasps nearly exclusively chose visual cues at 8°C. The parasitoids switch between cues and sensory systems depending on temperature. As overall precision of ovipositor insertions was not affected by temperature, the parasitoids fully compensate the loss of one cue provided another reliable cue is available on the same spatial scale.     

Effect of ambient temperature on mechanosensory host location in two parasitic wasps of different climatic origin

Abstract.  Several parasitic wasps of the Pimplinae (Ichneumonidae) use self-produced vibrations transmitted through plant substrate to locate their concealed immobile hosts (lepidopteran pupae) by reflected signals. This mechanosensory mechanism of host location, called vibrational sounding, depends on the physical characteristics of the plant substrate and the wasp's body and is postulated to depend on ambient temperature. Adaptations of two parasitoid species to thermal conditions of their habitats and the influence of temperature on the trophic interaction during host location are investigated in the tropical Xanthopimpla stemmator (Thunberg) and compared with the temperate Pimpla turionellae (L.). Plant-stem models with hidden host mimics are offered to individual wasps under defined temperature treatments and scored for the number and location of ovipositor insertions. Significant effects of temperature are found on host-location activity and its success. The tropical species possesses an optimum temperature range for vibrational sounding between 26 and 32 °C, whereas the performance decreases both at low and high temperatures. The temperate species reveals substantial differences with respect to performance at the same thermal conditions. With increasing temperature, P. turionellae shows a reduced response to the host mimic, reduced numbers of ovipositor insertions, and decreased precision of mechanosensory host location. In the tropical X. stemmator , the female wasps are able to locate their host with high precision over a broad range of ambient temperatures, which suggests endothermic thermoregulation during vibrational sounding. Environmental physiology may therefore play a key role in adaptation of the host location mechanism to climatic conditions of the species' origin.     

The adaptive significance of host location by vibrational sounding in parasitoid wasps

Vibrational sounding, which is a form of echolocation, is a means of host location by some parasitoid wasps. The wasp taps the substrate (wood, stem or soil) and detects the position of a potential host through the returning 'echoes'. The deployment of vibrational sounding is inferred through the form of the subgenual organ in the female tibia in combination with the presence of modifications to the female antenna used for tapping the substrate. Vibrational sounding and its associated modifications were found in two families. The use of vibrational sounding by parasitoid wasps was positively correlated with the depth of the host in the substrate relative to the size of the parasitoid. There were also significant correlations between the use of vibrational sounding and parasitism of immobile and concealed hosts and between vibrational sounding and idiobiosis. The data suggested that vibrational sounding evolved under a variety of ecological conditions, being employed in the location of wood-boring, stem-boring, soil-dwelling and cocooned hosts and stem-nesting aculeates, often in situations in which the host does not produce vibrations itself.     

Body temperature of the parasitic wasp Pimpla turionellae (Hymenoptera) during host location by vibrational sounding

Abstract.  The pupal parasitoid Pimpla turionellae (L.) uses self-produced vibrations transmitted on the plant substrate, so-called vibrational sounding, to locate immobile concealed pupal hosts. The wasps are able to use vibrational sounding reliably over a broad range of ambient temperatures and even show an increased signal frequency and intensity at low temperatures. The present study investigates how control of body temperature in the wasps by endothermic mechanisms may facilitate host location under changing thermal environments. Insect body temperature is measured with real-time IR thermography on plant-stem models at temperature treatments of 10, 18, 26 and 30 °C, whereas behaviour is recorded with respect to vibrational host location. The results reveal a low-level endothermy that likely interferes with vibrational sound production because it occurs only in nonsearching females. At the lowest temperature of 10 °C, the thoracic temperature is 1.15 °C warmer than the ambient surface temperature whereas, at the high temperatures of 26 and 30 ° C, the wasps cool down their thorax by 0.29 and 0.47 °C, respectively, and their head by 0.45 and 0.61 °C below ambient surface temperature. By contrast, regardless of ambient temperature, searching females always have a slightly elevated body temperature of at most 0.30 °C above the ambient surface temperature. Behavioural observations indicate that searching females interrupt host location more frequently at suboptimal temperatures, presumably due to the requirements of thermoregulation. It is assumed that both mechanisms, producing vibrations for host location and low-level endothermy, are located in the thorax. Endothermy by thoracic muscle work probably disturbs signal structure of vibrational sounding, so the processes cannot be used at the same time.     

Learning used as a strategy for host stage location in an endophytic host-parasitoid system

The relationship between host stage selection and foraging behaviour of Pholetesor bicolor Nees (Hymenoptera: Braconidae), a larval parasitoid of Phyllonorycter spp. (Lepidoptera: Gracillariidae), was investigated under laboratory conditions. The endophytic host develops through two larval stages with different feeding habits, accordingly named sap- and tissue-feeders. The parasitoid was able to find and parasitise both larval stages, even though it is most successful in parasitising the sap-feeder stage. The influence of experience in the parasitoid's searching behaviour was observed in a choice bioassay. Searching activity increased when either contact experience with the sap- or the tissue-feeder host was given. Furthermore, the ability of the parasitoid to locate a sap- or a tissue-feeder infested plant was influenced by the type of experience given prior to the bioassay. Naive females were less active, and were observed with equal frequency on sap-feeder, tissue-feeder and non-infested plants. In contrast, females that were given previous contact experience with sap-feeders (i.e., the host stage which provided the most successful parasitism) were observed foraging more often on plants infested by the sap-feeders, than on those infested by tissue-feeders or on non-infested plants. Experience with a tissue-feeder host had no detectable effect on host stage location and only enhanced P. bicolor's foraging activity. The advantages of learning in this tritrophic system are discussed.     

Parasitoid load affects plant fitness in a tritrophic system

Plants attacked by herbivorous insects emit volatile compounds that attract predators or parasitoids of the herbivores. Plant fitness increases when these herbivorous insects are parasitized by solitary parasitoids, but whether gregarious koinobiont parasitoids also confer a benefit to plant fitness has been disputed. We investigated the relationship between parasitoid load of the gregarious Cotesia glomerata (L.) (Hymenoptera: Braconidae), food consumption by larvae of their host Pieris brassicae L. (Lepidoptera: Pieridae), and seed production in a host plant, Brassica nigra L. (Brassicaceae), in a greenhouse experiment. Plants damaged by caterpillars containing single parasitoid broods produced a similar amount of seeds as undamaged control plants and produced significantly more seeds than plants with unparasitized caterpillars feeding on them. Increasing the parasitoid load to levels likely resulting from superparasitization, feeding by parasitized caterpillars was significantly negatively correlated with plant seed production. Higher parasitoid brood sizes were negatively correlated with pupal weight of Cotesia glomerata , revealing scramble competition leading to a fitness trade-off for the parasitoid. Our results suggest that in this tritrophic system plant fitness is higher when the gregarious parasitoid deposits a single brood into its herbivorous host. A prediction following from these results is that plants benefit from recruiting parasitoids when superparasitization is prevented. This is supported by our previous results on down-regulation of synomone production when Brassica oleracea was fed on by parasitized caterpillars of P. brassicae . We conclude that variable parasitoid loads in gregarious koinobiont parasitoids largely explain existing controversies about the putative benefit of recruiting these parasitoids for plant reproduction.     

Interactions between host plant,Aphis fabae,and its natural enemies,Orius albidipennis and Lysiphlebus fabarum in a tritrophic system

The interactions between two natural enemies (NEs) were studied in a tritrophic system to evaluate the efficacy of simultaneous releases of a parasitoid, Lysiphlebus fabarum Marshal (Hymenoptera: Braconidae) and a predator, Orius albidipennis Reuter (Heteroptera: Anthocoridae) against Aphis fabae Scopoli (Homoptera: Aphididae). Three experiments were performed to evaluate the prey preference of a predator to parasitized versus unparasitized aphid hosts; to investigate the emission of volatile synomones by the host plant, Vicia fabae, and to determine its behavioral effect on the NEs; and to determine behavioral effect of volatile infochemicals between NEs. Results showed that the female predatory bug did not show significant preference between parasitized and unparasitized aphids, but the male bug had significant preference for parasitized mummies. Olfactometry trials documented that both NEs were significantly attracted to volatile cues released by the host plant infested with the aphid. Each of the NEs avoided odors which indicated the presence of another intraguild competitor. Therefore, simultaneously releases of the NEs are not recommended.     

Functional Synchronization of Biological Rhythms in a Tritrophic System

In a tritrophic system formed by a plant, an herbivore and a natural enemy, each component has its own biological rhythm. However, the rhythm correlations among the three levels and the underlying mechanisms in any tritrophic system are largely unknown. Here, we report that the rhythms exhibited bidirectional correlations in a model tritrophic system involving a lima bean, a pea leafminer and a parasitoid. From the bottom-up perspective, the rhythm was initiated from herbivore feeding, which triggered the rhythms of volatile emissions; then the rhythmic pattern of parasitoid activities was affected, and these rhythms were synchronized by a light switch signal. Increased volatile concentration can enhance the intensity of parasitoid locomotion and oviposition only under light. From the top-down perspective, naive and oviposition-experienced parasitoids were able to utilize the different volatile rhythm information from the damaged plant to locate host leafminers respectively. Our results indicated that the three interacting organisms in this system can achieve rhythmic functional synchronization under a natural light-dark photoperiod, but not under constant light or darkness. These findings provide new insight into the rhythm synchronization of three key players that contribute to the utilization of light and chemical signals, and our results may be used as potential approaches for manipulating natural enemies.     

Host location and selection cues in a generalist tachinid parasitoid

Tachinid flies are diverse and ecologically important insect parasitoids. However, the means by which tachinid species locate and select hosts are poorly known. Many tachinids exhibit unusually wide host ranges and they also possess well-developed visual systems. These characteristics suggest that tachinids differ from parasitic wasps in their reliance on various sensory modes and types of cues. A series of behavioral assays using the generalist tachinid Exorista mella Walker (Diptera: Tachinidae) were conducted to examine what types of cues this parasitoid uses to locate and accept hosts, and how the cues used may reflect its ecological relationships with hosts. Female E. mella responded strongly to host motion in assays using both live hosts and host corpses, and this cue is shown to be an important elicitor of attack behavior. Females also responded to volatile chemicals associated with damaged food plants of their host in an olfactometer. Flies responded only weakly to direct visual contact with stationary hosts and odors directly associated with hosts. The behavior of female E. mella changed with experience such that more experienced flies recognized and attacked hosts more readily than did inexperienced flies. The use of general olfactory and visual cues by E. mella may be an effective strategy by this polyphagous parasitoid to locate a broad range of potential hosts.     

Visual and Chemical Cues Used in Host Location and Acceptance by a Dipteran Parasitoid

Locating potential hosts for egg laying is a critical challenge in the life history of many insects. Female insects in several orders have evolved mechanisms to find hosts by using olfactory and visual signals derived from their hosts. We describe visual and chemical cues used by the dipteran parasitoid Apocephalus paraponerae (Diptera: Phoridae) in the location and acceptance of its host ant Paraponera clavata (Hymenoptera: Formicidae: Ponerinae). Our results show that A. paraponerae uses the visual cue of ant body size when locating hosts at short range and that these flies lay more eggs in ants that retain their surface chemicals than in ants with these chemicals removed. We compare the cues used by A. paraponerae with cues used by tephritid fruit flies in location and acceptance of their hosts, and we suggest further avenues for the study of host location, acceptance, and host discrimination of A. paraponerae and other parasitoids of ants.     

Foraging Behavior and Patch Time Allocation by Fopius arisanus (Hymenoptera: Braconidae), an Egg-Larval Parasitoid of Tephritid Fruit Flies

This study quantitatively describes the host-searching behavior of Fopius arisanus (Sonan) (Hymenoptera: Braconidae), an important egg-larval parasitoid of tephritid fruit fly pests, on coffee berries infested with host eggs of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). We also investigate the parasitoid's response to local variation in host patch quality. The temporal pattern of behavioral organisation was examined by constructing an ethogram. The parasitoid spent over 90% of its foraging time in detecting and locating hosts after arriving on a host-infested fruit, and displayed a relatively fixed behavioral pattern leading to oviposition. Patch residence time increased in the presence of host-associated cues, following successful ovipositions, and with increasing size of host clutches per fruit, but decreased with each successive visit to the same host patch and with increasing availability of alternative host patches. The parasitoid females discriminated against previously parasitized hosts and spent significantly less time and searching effort on patches previously exploited by herself or by conspecific females. The effective host-searching behavior, perfect host discrimination ability, and success-motivated searching strategy shown by F. arisanus ensured a thorough exploitation of host resources by this parasitoid.     

Host–parasitoid development and survival strategies in a non-pollinating fig wasp community

In a tritrophic system, parasitoid development and galler host survival strategies have rarely been investigated simultaneously, an approach crucial for a complete understanding of the complexity of host–parasitoid interactions. Strategies in parasitoids to maximize host exploitation and in gallers to reduce predation risk can greatly affect the structure of tritrophic communities. In this study, the developmental strategies of galler hosts and their associated parasitoids in the tritrophic fig–fig wasp system are experimentally investigated for the first time. In this highly co-evolved system, wasp development is intrinsically tied with the phenology of the wasp brood sites that are restricted to the enclosed urn-shaped fig inflorescence called the syconium which can be regarded as a microcosm. Wasp exclusion experiments to determine host specificity, gall dissections and developmental assays were conducted with non-pollinating fig wasps in Ficus racemosa. Our results provide evidence for exceptions to the widely accepted koinobiont–idiobiont parasitoid dichotomy. This is also the first time fig wasps were raised ex situ from non-feeding stages onwards, a technique that enabled us to monitor their development from their pre-pupal to adult stages and record their development time more accurately. Based on variation in development time and host specificity, the possibility of a cryptic parasitoid species is raised. The frequency of different wasp species eclosing from the microcosms of individual syconia is explained using host–parasitoid associations and interactions under the modulating effect of host plant phenology.     

Host Location by Ichneumonid Parasitoids is Associated with Nest Dimensions of the Host Bee Species

Parasitoid fitness depends on the ability of females to locate a host. In some species of Ichneumonoidea, female parasitoids detect potential hosts through vibratory cues emanating from them or through vibrational sounding produced by antennal tapping on the substrate. In this study, we (1) describe host location behaviors in Grotea gayi Spinola (Hymenoptera: Ichneumonidae) and Labena sp. on nests of Manuelia postica Spinola (Hymenoptera: Apidae), (2) compare nest dimensions between parasitized and unparasitized nests, (3) correlate the length of M. postica nests with the number of immature individuals developing, and (4) establish the relative proportion of parasitized nests along the breeding period of M. postica. Based on our results, we propose that these parasitoids use vibrational sounding as a host location mechanism and that they are able to assess host nest dimensions and choose those which may provide them with a higher fitness. Finally, we discuss an ancestral host?Cparasitoid relationship between Manuelia and ichneumonid species.     

Host selection and reproductive success of French and Moroccan populations of the parasitoid, Microctonus aethiopoides (Hymenoptera: Braconidae)

French and Moroccan populations of the parasitoid Microctonus aethiopoides Loan were studied in the laboratory for their host selection, mating behavior, and reproductive success. The French strain, collected on Hypera postica (Gyllenhal), although capable of parasitizing and producing viable offspring on Sitona weevils, preferred Hypera weevils, its known target host. The Moroccan strain, collected on Sitona discoideus Gyllenhal, exhibited host specificity for Sitona. A partial reproductive isolation was observed between the two strains. Moroccan females mated more frequently with French males than did French females with Moroccan males. The pre-copulation time for mating pairs of opposite strains was significantly longer than that for mating pairs of the same strain. There was no significant difference in copulation time nor in larval and pupal duration between French and Moroccan strains. In summary, the French and Moroccan strains of M. aethiopoides are clearly separable by biological, behavioral, and morphometric traits and the preferred host for Hypera is the French strain and Sitona for the Moroccan strain. Consequently, geographic location and host source become important when considering this parasitoid as a potential biological control agent.     

Optimized timing of parasitoid release: a mathematical model for biological control of <Emphasis Type="Italic">Drosophila suzukii</Emphasis>

We present a model for the population dynamics of the invasive fruit fly Drosophila suzukii and its pupal parasitoid Trichopria drosophilae. Seasonality of the environment is captured through a system of delay differential equations with variable delays. The model is used to explore optimal timing for releasing parasitoids in biological control programs. According to the results, releasing parasitoids is most effective between late spring and early summer when the host population begins to increase. A single parasitoid release event can be more efficient than multiple releases over a prolonged period, but multiple releases are more robust to suboptimal timing choices. The findings can be useful for optimizing parasitoid release and should be transferable for similar systems. More generally, the model is an example for stage-structured resource-consumer dynamics in a varying environment.     

Infochemical use and dietary specialization in parasitoids: a meta‐analysis

Many parasitoid species use olfactory cues to locate their hosts. In tritrophic systems, parasitoids of herbivores can exploit the chemical blends emitted by plants in reaction to herbivore‐induced damage, known as herbivore‐induced plant volatiles (HIPVs). In this study, we explored the specificity and innateness of parasitoid responses to HIPVs using a meta‐analysis of data from the literature. Based on the concept of dietary specialization and infochemical use, we hypothesized that (i) specialist parasitoids (i.e., with narrow host ranges) should be attracted to specific HIPV signals, whereas generalist parasitoids (i.e., with broad host ranges) should be attracted to more generic HIPV signals and (ii) specialist parasitoids should innately respond to HIPVs, whereas generalist parasitoids should have to learn to associate HIPVs with host presence. We characterized the responses of 66 parasitoid species based on published studies of parasitoid behavior. Our meta‐analysis showed that (i) as predicted, specialist parasitoids were attracted to more specific signals than were generalist parasitoids but, (ii) contrary to expectations, response innateness depended on a parasitoid's target host life stage rather than on its degree of host specialization: parasitoids of larvae were more likely to show an innate response to HIPVs than were parasitoids of adults. This result changes our understanding of dietary specialization and highlights the need for further theoretical research that will help clarify infochemical use by parasitoids.     

Fitness-related traits in a parasitoid fly are mediated by effects of plants on its host

Plants can affect parasitoids directly, by reducing or enhancing their ability to locate hosts, or indirectly by affecting the fitness of herbivores and thus of parasitoids. Tritrophic interactions between three host plants (cucumber, tomato, sweet pepper), a polyphagous herbivore Trichoplusia ni and a generalist parasitoid Compsilura concinnata were assessed. Plants had a strong effect on T. ni larval survival, as well as on C. concinnata fitness-related traits: cucumber-fed hosts yielded parasitoids with shorter larval development time and females had heavier pupal weights than parasitoids from host larvae that were fed tomato. Furthermore, C. concinnata was more efficient at finding cucumber-fed than tomato-fed T. ni . These results suggest that C. concinnata has different efficiency and potential as a biocontrol agent on the different crops. This highlights the importance of assessing tritrophic interactions in systems where an inundative biological control agent may be released against generalist targets on more than one crop plant.