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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Visual and olfactory location of biotopes, prey patches, and individual prey by the ladybeetleChilocorus nigritus

Foraging behaviour of the predatorChilocorus nigritus (Fabricius) (Coleoptera: Coccinellidae) at the three spatial levels of biotope, prey patch and individual prey, was studied in the laboratory, and related to behaviour in the field. Vertically oriented parallel lines were more attractive than the same shapes in a horizontal position. A simulated horizon with a tree line was preferred to a simulated flat horizon. They were attracted to a tree image for the first 2 h of exposure, but were less attracted after longer exposure, possibly due to habituation. Leaf shape was recognised, and simple ovate leaves were preferred to compound bipinnate leaves and to squares. These responses were associated with biotope selection for feeding and aggregation at aestivation sites. The location of prey patches by adults involved prey odour but the location of such sites by larvae did not. Adults detected individual prey visually and olfactorily over short distances but physical contact with prey was required for detection by larvae. Location of individual prey and prey patches by adults and larvae was facilitated by alternation between intensive and extensive search. The differences in the ability of larvae and adults to locate prey, stem from the adults being the active locators of biotope and patch, whereas the comparatively immobile larvae depend on their parents’ ability for long-range location of prey. Two hypotheses concerning coccinellid foraging behaviour are proposed. Firstly, the duration of response to a visual cue is related to the distance over which such a cue may be perceived. It follows that habituation to closer range cues occurs more rapidly than to longer range cues. Secondly, visual cues used by adults at the different spatial levels of prey location, and the location of mates and aggregation sites, have the same or similar shape. These results also provide guidelines for orchard management to maximise the biocontrol value of this species.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

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.     

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.     

Predator–prey interactions between crayfish (Orconectes juvenilis) and snails (Physa gyrina) are affected by spatial scale and chemical cues

Abstract. We conducted two experiments to compare the behaviors of predatory crayfish ( Orconectes juvenilis ) and snail prey ( Physa gyrina ), with and without exposure to injured-snail cues, in seven different sizes of arena. Individuals in both O. juvenilis and P. gyrina are known to obtain information about predation events from chemical cues present in the water, but the effect of spatial scale on this information or the ensuing interaction has not been previously investigated. We found that crayfish were generally more active in larger arenas, but their response to injured-snail cues decreased as arena size increased. Snails responded to injured-snail cue by seeking refuge, but responded less strongly in larger arenas. Less time was required for crayfish to capture a snail in the presence of injured-snail cue, and there was an interaction between cue and arena size evident in middle-sized arenas. Consumption time was lower in the presence of injured-snail cue but was unaffected by arena size. Based on these results, we conclude that the effects of injured-snail cue are mediated by spatial scale, and this affects the outcome of this predator–prey interaction. Spatial scale should be considered in the design and interpretation of other predator–prey studies, particularly when sensory or motility differences exist between predators and prey that affect how each gathers information about the environment.     

Visual cues override olfactory cues in the host-finding process of the monophagous leaf beetle Altica engstroemi

It is generally assumed that specialist insect herbivores utilize plant odours to find their particular host plants and that visual cues are of minor importance in the host‐finding process. We performed Y‐tube olfactometer bioassays and small‐scale field experiments to determine whether, under laboratory and field conditions, the monophagous herbivore Altica engstroemi J. Sahlberg (Coleoptera: Chrysomelidae: Alticinae) is guided to its host plant Filipendula ulmaria (L.) Maxim. (Rosaceae) by visual or olfactory cues. The olfactometer tests showed that A. engstroemi was never attracted to odours, either from undamaged or from damaged plants. Even starvation for 24 h did not change this behaviour. However, the field experiment showed that visual cues alone were sufficient to attract a significant number of starved beetles when offered a choice between bagged host plants and bagged green plastic control ‘plants’. Our findings contrast with the general view that plant odours constitute the major cue in the host‐finding process among specialized phytophagous insects. A review of the literature for the period 1986–2006 inclusive, relating to host‐plant finding in Chrysomelidae, identified studies of 19 chrysomelid species, all of which were guided by olfactory cues. No species were guided to their host by visual cues. Although some studies demonstrated that chrysomelids may exhibit orientation responses to colour or contrast, our study on A. engstroemi is the only one demonstrating that visual cues affect host‐plant selection in a chrysomelid species. We suggest that the use of visual cues in host‐finding may evolve among chrysomelids with limited dispersal ability in persistent habitats and may be found among species monophagous on abundant host plants that dominate the structure of the plant community, that is, where the host plant's presence is predictable in time and space.     

Effects of patch scale on density-dependence and species-dependence in two host-parasitoid systems

Summary Data from two host-parasitoid communities were analyzed to ascertain whether patch scale affected the kinds of correlations existing between 1) spatial differences in host density and the intensity of parasitism (density-dependence) and 2) number of species of parasitoids and the intensity of parasitism (species-dependence). We concluded that parasitization rates are usually independent of both host density and number of parasitoid species present regardless of patch scale. Therefore, the responses of parasitoids to host density and the addition of parasitoid species to a community are equally unpredictable in outcome.     

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.     

Cues Used for Localizing Food by the Gray Squirrel (Sciurus carolinensis)

We compared the use of olfactory, visual, and spatial cues for learning the location of stored food by gray squirrels (Sciurus carolinensis). All experimental cues were extrinsic, that is, they originated from the environment around the food rather than from the food itself. In training trials, artificial caches with one of two odors, one of two colors, and six of 12 spatial locations contained sunflower seeds. In experimental trials, the odors, colors, and sets of spatial locations associated with food were reversed one at a time, so that only two of the three training cues gave evidence of the food rewards. Consequent declines in food localization by the squirrels revealed differential use of particular cue modalities. The data show that squirrels used visual cues the most and olfactory cues the least with this design. These results, along with other evidence, suggest that gray squirrels use spatial memory in food recovery.     

The use of general foraging kairomones in a generalist parasitoid

Almost no comparative studies are available on the use of general and specific infochemical cues by generalist parasitoids with hosts from different families feeding on host plants also from different families. Based on literature, two hypotheses were developed and tested with host recognition cues used by the larval parasitoid Lariophagus distinguendus . This generalist parasitizes beetle species from different families developing in seeds of plant species from the Poaceae and Fabaceae. The first hypothesis predicts that for initial encounters with host species, natural enemies should innately use general cues, which are common to all hosts and their food plants. The second hypothesis predicts that natural enemies should learn specific cues from host plant and host after experience with a host species. The first hypothesis was partly confirmed. L. distinguendus innately reacted to faecal cues from several host species and chemical analyses of faeces from these hosts revealed the common occurrence of chemicals that are used for host recognition by L. distinguendus . In disagreement with the first hypothesis, parasitoids did not innately respond to cues from plant seeds. Preference experiments on the influence of experience demonstrated an increased host recognition response towards a host after experience with it. In support of the second hypothesis, L. distinguendus females learned specific cues from herbivore-damaged wheat, rice and cowpea seeds and from the faeces of the bean weevil Callosobruchus maculatus .