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.     

Host Location of a Pupal Parasitoid in a Tritrophic System Compared to a Model Offering Mechanosensory Cues Only

Several species of hymenopteran parasitoids are able to locate concealed pupal hosts by vibrational sounding. However, the specific role of this technique of mechanosensory host location has not yet been investigated in a natural, tritrophic system with multiple cues. Here we compared the host location of the pupal parasitoid Xanthopimpla stemmator in a tritrophic system with corn borer pupae in maize stem to the behavior on a paper model offering mechanosensory cues only. In general, the behavioral pattern and the behavioral states exhibited by host-searching female parasitoid were identical in the model and in the tritrophic system, while quantitative aspects differed. Our results demonstrate that vibrational sounding maintains its significance for host location in an environment with multiple cues, and that additional cues may increase responsiveness of females.     

Host-foraging stable flies,Stomoxys calcitrans,are preferentially attracted to objects with both visual and thermal host-like characteristics

Many haematophagous insects use the heat emitted by warm-blooded animals as a cue for locating suitable hosts. Blood-feeding stable flies, Stomoxys calcitrans (L.) (Diptera: Muscidae), are known to respond to visual and olfactory host cues. However, the effects of thermal host cues on the foraging behaviour of these flies remain largely unknown. Here we tested the hypothesis that host-foraging stable flies preferentially land on objects with host-like temperature, and on objects with both visual and thermal host-like cues. In laboratory bioassays, stable flies were offered a choice between paired temperature-controlled copper discs. Flies preferentially landed on the disc with a host-like temperature (40 °C), discriminating against discs that were cooler (26 or 35 °C) or warmer (50 or 60 °C) than vertebrate hosts. Flies that were well fed and thus not in foraging mode, or host-foraging flies that were offered infrared radiation but not the conductive and convective heat of different temperature discs, failed to discriminate between the stimuli. In greenhouse experiments, when flies were offered a choice between paired barrels as surrogate hosts, flies preferentially landed on barrels that were both thermally and visually appealing (38–39 °C, black), discriminating against barrels that were cold (10 °C), white, or both cold and white. Thermal cues augmented the overall landing responses of flies but their initial (mid-range) attraction to barrels was mediated by visual cues. Overall, the data suggest that thermal host cues affect the host-foraging behaviour of stable flies primarily at close range, prompting landing on a host.     

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.     

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.     

Size,shape and hue modulate attraction and landing responses of the braconid parasitoid <Emphasis Type="Italic">Fopius arisanus</Emphasis> to fruit odour-baited visual targets

Female parasitoids are guided by multisensory information, including chemical and physical cues during host location. In the present study, we investigated the behavioural responses of naïve Fopius arisanus (Sonan) females to visual targets baited with guava odour. In non-choice wind tunnel tests, the attraction and landing responses of parasitoids to spheres painted with different colours, and targets of different shapes and sizes were evaluated. Females were more frequently attracted and landed more often on dark yellow targets than on targets with other colours. There was no correlation between the brightness of each colour and the attraction or landing responses. In contrast, both responses were correlated with relative reflectance (hue) of the coloured targets. A positive correlation was observed between attraction and hue, and a negative correlation between landing and hue. F. arisanus was attracted to and landed more often on spheres than on other shape models. The attraction response of this parasitoid was affected by the size of the targets, with spheres of 10 and 12 cm diameter being more attractive than spheres of 8, 6 and 4 cm diameter. The fact that F. arisanus females were able to discriminate among visual targets that differ in colour, shape and size stresses the importance of vision during host location by this species.     

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.     

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.     

Diving Into The Water: Cues Related to the Decision‐Making by an Egg Parasitoid Attacking Underwater Hosts

Although adult parasitoids spend a majority of their lives above ground, females of several species must search for their host in the water or on the soil. Adult parasitoids above ground can use a variety of sensory cues to detect their hosts from a distance. However, their sensory cues can be impaired from volatile chemicals, and their visual stimuli can be decreased while submerging or burrowing in the water of soil during their search for their hosts. Searching underwater or underground would incur high foraging costs, that is, time and energy consumption and increase risk of drowning. Therefore, to reduce such costs and increase searching efficiency, the decision on where to start submerging or burrowing for attacking hosts is important for parasitoids. Furthermore, there are no studies that have examined the cues of submerging or burrowing parasitoids on their exploit for the decision to attack their hosts. We have examined the cues used by the egg parasitoid Tiphodytes gerriphagus attacking underwater hosts. We compared the searching behaviors of T. gerriphagus among four oviposition site conditions. The four sites investigated were oviposition site with both host adult chemical residues and presence of eggs, with only the presence of eggs, with only the host adult chemical residues, and without any cue. Our results indicated that T. gerriphagus more frequently contacted and submerged at oviposition sites with the adult residues rather than at oviposition sites without them. Nonetheless, the presence of underwater host eggs did not affect the host‐searching behavior. This suggests that T. gerriphagus decided to submerge at the oviposition site in response to the adult residues. Furthermore, our observation also suggested that T. gerriphagus has already detected that the adult residues might be volatile before contacting the oviposition site. Finally, we will discuss the exploitation patterns of host‐searching cue by parasitoids that need to submerge from the context of its reliability and detectability problems.     

Causal inference regulates audiovisual spatial recalibration via its influence on audiovisual perception

To obtain a coherent perception of the world, our senses need to be in alignment. When we encounter misaligned cues from two sensory modalities, the brain must infer which cue is faulty and recalibrate the corresponding sense. We examined whether and how the brain uses cue reliability to identify the miscalibrated sense by measuring the audiovisual ventriloquism aftereffect for stimuli of varying visual reliability. To adjust for modality-specific biases, visual stimulus locations were chosen based on perceived alignment with auditory stimulus locations for each participant. During an audiovisual recalibration phase, participants were presented with bimodal stimuli with a fixed perceptual spatial discrepancy; they localized one modality, cued after stimulus presentation. Unimodal auditory and visual localization was measured before and after the audiovisual recalibration phase. We compared participants’ behavior to the predictions of three models of recalibration: (a) Reliability-based: each modality is recalibrated based on its relative reliability—less reliable cues are recalibrated more; (b) Fixed-ratio: the degree of recalibration for each modality is fixed; (c) Causal-inference: recalibration is directly determined by the discrepancy between a cue and its estimate, which in turn depends on the reliability of both cues, and inference about how likely the two cues derive from a common source. Vision was hardly recalibrated by audition. Auditory recalibration by vision changed idiosyncratically as visual reliability decreased: the extent of auditory recalibration either decreased monotonically, peaked at medium visual reliability, or increased monotonically. The latter two patterns cannot be explained by either the reliability-based or fixed-ratio models. Only the causal-inference model of recalibration captures the idiosyncratic influences of cue reliability on recalibration. We conclude that cue reliability, causal inference, and modality-specific biases guide cross-modal recalibration indirectly by determining the perception of audiovisual stimuli.     

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.     

A Laboratory study on the visual and chemical orientation of the gastropod Nerita Fulgurans Gmelin, 1791

Behavioural responses of the gastropod Nerita fulgurans Gmelin, 1791 to flat black rectangles and intraspecific mucus trails were measured in a circular arena. Snails were tested in water either in the presence or absence of chemicals generated from a predator gastropod, Chicoreus brevifrons (Lamarck, 1822). The test hypothesis was that this snail has different behavioural responses as result of visual and chemical cue integration. Nerita fulgurans has the capacity to orient to solid targets subtending angles larger than 10° and follow its own mucus trails. In water conditioned by the predator C . brevifrons, snails exhibited an avoidance response when 10°, 20° and 45° sectors were presented, demonstrating an integration of chemical and visual information. The simultaneous presentation of two orienting cues (black sectors and mucus trails) was tested to determine the nature of the interaction. When the two cues were oriented in the same direction there was no effect. When the two cues were presented from directions 180° apart a preference for visual cues over mucus trail cues was evident when the visual angle of the visual cue subtended angles greater than 90°. This result demonstrates a hierarchical usage of the orienting references.     

Fitness and life history parameters of <Emphasis Type="Italic">Leptomastix epona</Emphasis> and <Emphasis Type="Italic">Pseudaphycus flavidulus</Emphasis>, two parasitoids of the obscure mealybug <Emphasis Type="Italic">Pseudococcus viburni</Emphasis>

Fitness and life table parameters of two endoparasitoids of the obscure mealybug Pseudococcus viburni (Signoret), the solitary Leptomastix epona (Walker) and the gregarious Pseudaphycus flavidulus (Brèthes), were examined in relation to temperature and host size with a view to determine the efficacy of the parasitoids as biocontrol agents of the pest. Three temperature levels (21°C, 26°C and 31°C) and two host sizes classes (small, which mostly comprised third instar nymphs and large, which consisted of female adults) were studied. The lower developmental threshold and thermal constant of the host and the parasitoids were found similar so the coincidence of pest and parasitoids is likely. The rate of development of the parasitoids increased with a linear trend as the temperature increased from 21°C to 31°C. Temperature had a significant effect on mummification in both parasitoid species and on successful parasitism by P. flavidulus. Host size had a significant effect on the mummification caused by L. epona and on the proportion of the male offspring which emerged as well as on the successful parasitism by P. flavidulus. Life table parameters of the parasitoids were estimated in small and large hosts at 26°C in the laboratory. Both parasitoids achieved a greater intrinsic rate of natural increase and gross reproductive rate in addition to a shorter generation and doubling time in large mealybugs compared with small ones. Consequently, large hosts are expected to have a higher impact on the rise of the parasitoids population and the potential of the parasitoids to control the mealybug population improves with the increase of host size. Handling Editor: Torsen Meiners.     

Bayesian multisensory integration and cross-modal spatial links.

Our perception of the word is the result of combining information between several senses, such as vision, audition and proprioception. These sensory modalities use widely different frames of reference to represent the properties and locations of object. Moreover, multisensory cues come with different degrees of reliability, and the reliability of a given cue can change in different contexts. The Bayesian framework--which we describe in this review--provides an optimal solution to deal with this issue of combining cues that are not equally reliable. However, this approach does not address the issue of frames of references. We show that this problem can be solved by creating cross-modal spatial links in basis function networks. Finally, we show how the basis function approach can be combined with the Bayesian framework to yield networks that can perform optimal multisensory combination. On the basis of this theory, we argue that multisensory integration is a dialogue between sensory modalities rather that the convergence of all sensory information onto a supra-modal area.     

Pattern vision of the honeybee (Apis mellifera). What is an oriented edge?

Pairs of black patterns on a white background, one rewarded the other not, were presented vertically each in one arm of a Y-maze. During training the locations of the black areas were changed every 5 min to prevent the bees using them as cues, but cues from edges were kept consistent. Bees detect orientation even in a gradient that subtends 36° from black to white (normal to the edge). Orientation cues in short lengths of edge are detected and summed on each side of the fixation point, irrespective of the lay-out of the pattern. Edges at right angles reduce the total orientation cue. The polarity of edges in a sawtooth grating is weakly discriminated, but not the orientation of a fault line where two gratings meet. Edge quality can be discriminated, but is not recognised in unfamiliar orientations. When spot location is excluded as a cue, the orientation of a row of spots or squares which individually provide no net orientation cue is not discriminated. In conclusion, when locations of black areas are shuffled, the bees remember the sum of local orientation cues but not the global pattern, and there is no re-assembly of a pattern based on differently oriented edges. A neuronal model consistent with these results is presented. Accepted: 5 March 2000     

Location and Color Learning in Bumblebees in a Two-Phase Conditioning Experiment

Bees use spatial and visual cues that characterize flowers to make dietary choices. If two such cues always appear together nonambiguously, they provide identical information. In such cases, do bees base dietary choices on one cue and ignore the other, or do they consider both cues? We allowed bumblebees to forage on two patches of artificial flowers that differed in location, color, and reward presence in a two-phase experiment. We switched either the display color, the location, or both the color and the location associated with the rewarding patch between phases. We tested for the effects of the switch on the bees' choices. Immediately following a switch in the location or both the location and the color of the rewarding patch, the bees' performance decreased, as they continued to visit the patch that was previously rewarding. This decrease did not occur when only the color of the rewarding patch was changed or in no-change controls. We suggest that the bees' foraging choices were guided mostly by a location cue when both the location and the color conveyed the same information.     

Experimental evidence for juvenile Chinook salmon, Oncorhynchus tschawytscha Walbaum, orientation at night and in sunlight after a 7° change in latitude

A group of eighteen young chinook salmon, Oncorhynchus tschawytscha Walbaum, trained to orientate in the direction 270°, showed a unimodal orientation of 264° and a mean bimodal axis of orientation of 258°/078° (magnetic) within confidence limits of 218°←→285°: 038°←→105° when tested under controlled conditions in Auckland. Two years later 12 of these fish were transferred to a new test arena in Christchurch, south (7° latitude) of the original location, for individual re-testing at night in a light-proof room and also in sunlight; in the absence of ‘local’ Auckland cues/clues. These fish had been kept in artificial light but six fish were exposed to sunlight in Auckland 2 weeks before moving to Christchurch. At night each fish showed consistent non-random orientation and nine out of 10 fish showed a mean bimodal orientation that fell within the confidence limit established in Auckland; the mean of means axis of orientation for 10 fish was 270°/090°. In sunlight each individual fish showed a consistent, non-random mean bimodal orientation that fell outside the confidence limits established in Auckland and, at night, in Christchurch. The mean of means axis of orientation was 001°/181° (magnetic); the map direction from Christchurch to Auckland is 15°. The principal findings in this study were: (a) ‘Local’ Auckland cues were not essential for location of the learnt direction. (b) A non-visual ‘universal’ cue was used as a reference for location of direction at night. (c) Daylight orientation was influenced by anisotropic radiance, even though the sun image was obscured by the test arena cover. (d) The concentration of data at midday and sunset in artificial light and perhaps at midnight, may indicate the presence of a non-visual zeitgeber. (e) A correlation between time and direction, in light and in darkness, which by implication involves a co-ordination process. (f) The fish under test apparently imprinted on some aspect of the sun (in Auckland) within a 2-day period at the age of 2 years. (g) Displacement, by 7° in latitude, may have been detected by both visual and non-visual means. It is proposed that directional information from the geomagnetic field and the anisotropic radiance of sunlight provides a complementary cross reference which would be sufficient for positional orientation, in relation to some fixed landmark, within coastal waters; but would not suffice for spatial orientation in mid-ocean.     

Microhabitat use affects goby (Gobiidae) cue choice in spatial learning task

This study investigated whether spatial learning ability and cue use of gobies (Gobiidae) from two contrasting habitats differed in a spatial task. Gobies were collected from the spatially complex rock pools and dynamic, homogenous sandy shores. Fishes were trained to locate a shelter under the simulated threat of predation and it was determined whether they used local or extra‐maze (global) and geometric cues to do so. It was hypothesized that fishes from rock pools would outperform fishes from sandy shores in their ability to relocate shelter and the two groups would differ in their cue use. It was found that rock‐pool species learnt the location of the correct shelter much faster, made fewer errors and used a combination of all available cues to locate the shelter, while sand species relied significantly more on extra‐maze and geometric cues for orientation. The results reported here support the hypothesis that fishes living in complex habitats have enhanced capacity for spatial learning and are more likely to rely on local landmarks as directional cues than fishes living in mundane habitats where local cues such as visual landmarks are unreliable.     

Integration of Visual and Olfactory Cues in Host Plant Identification by the Asian Longhorned Beetle,Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae)

Some insects use host and mate cues, including odor, color, and shape, to locate and recognize their preferred hosts and mates. Previous research has shown that the Asian longicorn beetle, Anoplophora glabripennis (Motschulsky), uses olfactory cues to locate host plants and differentiate them from non-host plants. However, whether A. glabripennis adults use visual cues or a combination of visual and olfactory cues remains unclear. In this study, we tested the host location and recognition behavior in A. glabripennis, which infests a number of hardwood species and causes considerable economic losses in North America, Europe and Asia. We determined the relative importance of visual and olfactory cues from Acer negundo in host plant location and recognition, as well as in the discrimination of non-host plants (Sabina chinensis and Pinus bungeana), by female and male A. glabripennis. Visual and olfactory cues from the host plants (A. negundo), alone and combined, attracted significantly more females and males than equivalent cues from non-host plants (S. chinensis and P. bungeana). Furthermore, the combination of visual and olfactory cues of host plants attracted more adults than either cue alone, and visual cues alone attracted significantly more adults than olfactory cues alone. This finding suggests that adult A. glabripennis has an innate preference for the visual and/or olfactory cues of its host plants (A. negundo) over those of the non-host plant and visual cues are initially more important than olfactory cues for orientation; furthermore, this finding also suggests that adults integrate visual and olfactory cues to find their host plants. Our results indicate that different modalities of host plant cues should be considered together to understand fully the communication between host plants and Asian longhorned beetles.