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.     

The parasitoid fly Exorista japonica uses visual and olfactory cues to locate herbivore‐infested plants

Some parasitoid flies exploit odors derived from plants as olfactory cues for locating the food plants of host insects, but the role of visual cues associated with plants remains largely unknown. The generalist tachinid Exorista japonica Townsend (Diptera: Tachinidae) is attracted to odors derived from maize plants [Zea mays L. (Poaceae)] infested by the larvae of Mythimna separata (Walker) (Lepidoptera: Noctuidae). In this study, we examined the effects of visual parameters on the olfactory attraction of female flies to host‐infested plants. A paper plant model of one of four colors (blue, green, yellow, or red) was placed in front of a host‐infested plant, which was hidden behind a mesh screen in a wind tunnel. The landing rate of females was significantly higher on the green plant model than on the other three models. When an achromatic plant model of one of four gray scales (white, light gray, dark gray, or black) was tested, the response rate of females was significantly higher towards the white model and decreased as the brightness of models decreased. Few female flies responded to the green plant model without odors of the host‐infested plants. When the four color plant models were placed together in a cage filled with odors of host‐infested plants, females remained significantly longer on the green model than on the other three models. These results showed that E. japonica females preferred the color green when odors of the host‐infested plants were present and suggest that E. japonica uses visual as well as olfactory cues to locate the host habitat.     

The influence of aphids on the behaviour of adults of the ladybird beetle,Harmonia axyridis (Col.: Coccinellidae)

The mechanism of prey finding by adultHarmonia axyridis (Pallas) (Coleoptera, Coccinellidae) was investigated in the laboratory by offering beetles small gauze or polyethylene bags containing either aphid-infested leaves or uninfested leaves along with empty control bags. The beetles were attracted to bags containing aphid-infested leaves. It is suggested that adults ofH. axyridis use olfactory and visual cues to detect prey. Mate-searching by males and the mating receptivity of females were enhanced in the presence of an abundance of aphids. The presence of aphids, perceived by the sensory organs of the beetles, possibly influence behaviour other than prey-searching.     

The impacts of Harmonia axyridis cues on foraging behavior of Aphidius gifuensis to Myzus persicae

This study investigated the effect of adult associated cues of the multicolored Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on the foraging behavior of the aphid parasitoid, Aphidius gifuensis Ashmead (Hymenoptera: Aphididae) with three assays: 1) whole aphid leaf-disc with H. axyridis tracks; 2) aphid leaf-disc with only half contaminated with H. axyridis tracks; 3) aphid leaf-discs without H. axyridis tracks. Foraging behavior of A. gifuensis was recorded using the Observer® XT 11 and EthoVsion® XT 12. In addition, functional responses of A. gifuensis in patches with or without H. axyridis cues were also tested. Aphidius gifuensis females preferred oviposition in arenas where no adult tracks of H. axyridis were present. However, no significant difference between functional responses of A. gifuensis foraging in plants with and without H. axyridis cues was detected. Our study suggests that H. axyridis associated cues could influence the foraging behavior and activity of A. gifuensis under laboratory conditions. On the other hand, the foraging efficiency of A. gifuensis was not significantly affected by H. axyridis walking tracks in a single plant system. Aphidius gifuensis might exhibit flexible behavioral responses to predator associated cues. The risk of intraguild interactions and the possibility of mitigating such risks for parasitoids are important components for ultimately determining the compatibility of biological control agents.     

Both olfactory and visual cues promote the hornet Vespa velutina to locate its honeybee prey Apis cerana

Predators use olfactory, visual and sometimes acoustic cues from the preys to assess food information. However, it is not known if the aggressive hornets (Vespa spp.) use olfactory, visual, or both types of information to find and recognize prey. In the present study, we trained hornet workers (Vespa velutina) to a feeding area. Once the hornets began consistently foraging at this feeding area, we determined whether they located prey (bees, Apis cerana) via olfactory or visual cues. We did this by testing whether hornets were attracted to a dummy bait (bee dummy bait or non-bee dummy bait) treated with extracts of honeybee cuticular hydrocarbons. We then tested whether hornets could distinguish between bee dummy bait and cotton ball dummy bait, both treated with bee odors. Hornets preferred the dummy treated with bee odors, and bee dummies (with bee images) were more attractive to the hornet than the cotton ball dummies with only bee odors. These results clearly indicate that a combination of olfactory and visual cues helps the hornet to locate its prey.     

Visual and Olfactory Floral Cues of Campanula (Campanulaceae) and Their Significance for Host Recognition by an Oligolectic Bee Pollinator

Oligolectic bees collect pollen from a few plants within a genus or family to rear their offspring, and are known to rely on visual and olfactory floral cues to recognize host plants. However, studies investigating whether oligolectic bees recognize distinct host plants by using shared floral cues are scarce. In the present study, we investigated in a comparative approach the visual and olfactory floral cues of six Campanula species, of which only Campanula lactiflora has never been reported as a pollen source of the oligolectic bee Ch. rapunculi. We hypothesized that the flowers of Campanula species visited by Ch. rapunculi share visual (i.e. color) and/or olfactory cues (scents) that give them a host-specific signature. To test this hypothesis, floral color and scent were studied by spectrophotometric and chemical analyses, respectively. Additionally, we performed bioassays within a flight cage to test the innate color preference of Ch. rapunculi. Our results show that Campanula flowers reflect the light predominantly in the UV-blue/blue bee-color space and that Ch. rapunculi displays a strong innate preference for these two colors. Furthermore, we recorded spiroacetals in the floral scent of all Campanula species, but Ca. lactiflora. Spiroacetals, rarely found as floral scent constituents but quite common among Campanula species, were recently shown to play a key function for host-flower recognition by Ch. rapunculi. We conclude that Campanula species share some visual and olfactory floral cues, and that neurological adaptations (i.e. vision and olfaction) of Ch. rapunculi innately drive their foraging flights toward host flowers. The significance of our findings for the evolution of pollen diet breadth in bees is discussed.     

Color Preference and Associative Color Learning in a Parasitoid Wasp, <Emphasis Type="Italic">Ascogaster reticulata</Emphasis> (Hymenoptera: Braconidae)

Natural enemies of agricultural pests, such as parasitoids and predators, often use chemical and visual cues in search of their hosts and prey, and they can learn the association between the cues and the host and prey presence. The braconid, egg-larval endoparasitoid wasp Ascogaster reticulata is a promising biological control agent for tortricid pests, such as Adoxophyes honmai, in tea plantations. Although previous studies revealed that A. reticulata uses contact chemicals released by tea plants in response to tortricid egg oviposition and that it can learn the associated cues, the diurnal wasp is also expected to use visual cues, especially color. Therefore, in this study, we investigated the innate color preference and associative color learning ability of A. reticulata. When a green paper and a paper of a different color (black, blue, red or yellow) was offered together to naive females of the wasp, the females spent less time on a black and blue papers. However, wasps trained to associate black or blue with the presence of a host egg-mass showed increased preference for these colors, whereas red- and yellow-trained wasps did not show changes in preference. Our findings indicate that A. reticulata uses colors, in addition to chemical cues, in host searching behavior and has the ability to learn colors associated with host presence.     

Plant scents modify innate colour preference in foraging swallowtail butterflies

Flower-visiting insects exhibit innate preferences for particular colours. A previous study demonstrated that naive Papilio xuthus females prefer yellow and red, whereas males are more attracted to blue. Here, we demonstrate that the innate colour preference can be modified by olfactory stimuli in a sexually dimorphic manner. Naive P. xuthus were presented with four coloured discs: blue, green, yellow and red. The innate colour preference (i.e. the colour first landed on) of the majority of individuals was blue. When scent from essential oils of either orange flower or lily was introduced to the room, females’ tendency to select the red disc increased. Scents of lavender and flowering potted Hibiscus rosa-sinensis, however, were less effective. Interestingly, the odour of the non-flowering larval host plant, Citrus unshiu, shifted the preference to green in females. In males, however, all plant scents were less effective than in females, such that blue was always the most favoured colour. These observations indicate that interactions between visual and olfactory cues play a more prominent role in females.     

The Influence of Prior Learning Experience on Pollinator Choice: An Experiment Using Bumblebees on Two Wild Floral Types of Antirrhinum majus

Understanding how pollinator behavior may influence pollen transmission across floral types is a major challenge, as pollinator decision depends on a complex range of environmental cues and prior experience. Here we report an experiment using the plant Antirrhinum majus and the bumblebee Bombus terrestris to investigate how prior learning experience may affect pollinator preferences between floral types when these are presented together. We trained naive bumblebees to forage freely on flowering individuals of either A. majus pseudomajus (magenta flowers) or A. majus striatum (yellow flowers) in a flight cage. We then used a Y-maze device to expose trained bumblebees to a dual choice between the floral types. We tested the influence of training on their choice, depending on the type of plant signals available (visual signals, olfactory signals, or both). Bumblebees had no innate preference for either subspecies. Bumblebees trained on the yellow-flowered subspecies later preferred the yellow type, even when only visual or only olfactory signals were available, and their preference was not reinforced when both signal types were available. In contrast, bumblebees trained on the magenta-flowered subspecies showed no further preference between floral types and took slightly more time to make their choice. Since pollinator constancy has been observed in wild populations of A. majus with mixed floral types, we suggest that such constancy likely relies on short-term memory rather than acquired preference through long-term memory induced by prior learning.     

Response of Trichogramma egg parasitoids to colored sticky traps

The response of Trichogramma spp. egg parasitoids to colored sticky traps was evaluated in the field during two seasons (1995/1996, 1996/1997). Traps consisted of a glass tube coated with Bird-Tanglefoot® into which colored paper was inserted or clear traps without paper. Colors tested were white, green, blue, yellow and red in the first season and white, green, yellow and black in the second season. The proportion of both female and male parasitoids caught on the sticky traps was significantly different among colors, indicating that the parasitoids actively move between plants and are not solely carried along passively by wind. White was the color most preferred by female parasitoids, followed by clear and green traps. Yellow was preferred over black but was less attractive than green. Visual cues may be used by Trichogramma spp. during the habitat location process. The color preference of male Trichogramma spp. differed significantly from females with yellow and green being more attractive than white. For all colors, more female Trichogramma spp. were caught on the sticky traps (>85% of all wasps caught), indicating a lower activity level and/or shorter lifespan for males. The use of white cylindrical sticky traps for monitoring Trichogramma spp. populations in the field is recommended.     

Variation in female guppy preference for male olfactory and visual traits

Animals often use different sensory systems to assess different sexually selected signals from potential mates. However, the relative importance of different signals on mate choice is not well understood in many animal species. In this study, we examined the relative importance of male olfactory and visual cues on female preference in the guppy Poecilia reticulata. We used digitally modified male images to standardize visual stimuli. We found that, regardless of whether females were presented without male visual stimuli or with identical male visual stimuli, they preferred stimuli with the odor of males to those without. However, when females were allowed to choose between dull male visual stimuli with male odor, and brightly colored male visual stimuli without male odor, there was no clear preference for either. Some females preferred the dull male visual stimuli with male odor, whereas some other females preferred the brightly colored male visual stimuli without male odor. These results indicate that the relative importance of olfactory and visual cues in female mate preference varied between individuals.     

Role of olfaction in host plant selection and local adaptation of a polyphagous herbivore,Eucolaspis Sharp

Host plant cues are known to shape insect–host plant association in many insect groups. More pronounced associations are generally manifested in specialist herbivores, but little is known in generalist herbivores. We used a polyphagous native beetle from New Zealand, bronze beetle, Eucolaspis sp. ‘Hawkes Bay’ (Chrysomelidae: Eumolpinae) to explore the role of olfaction in locating host plants and local adaptation. We also tested the role of other cues in the degree of acceptance or rejection of hosts. Adult Eucolaspis beetles were attracted to fresh leaf volatiles from apple and blackberry (Rosaceae). Male and female beetles responded similarly to olfactory cues of host plants. An indication of evolutionary affiliation was observed in olfactory preferences of geographically isolated conspecific populations. We found that geographically isolated populations of the beetles differ in their olfactory responses and exhibit some degree of local adaptation. However, irrespective of geographical and ecological associations, blackberry was preferred over apple as a feeding plant, and another novel plant, bush lawyer (Rubus australis), was readily accepted by 53.25% of the tested beetles. We show that plant volatiles play an important role in host location by Eucolaspis, but the acceptance or rejection of a particular host could also involve visual and contact cues.     

Oviposition preferences in Grapholita molesta: the relative importance of visual and olfactory cues

The oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), is a major pest of fruit trees worldwide. Females oviposit on the young leaves of peach [Prunus persica (L.) Batsch (Rosaceae)] shoots at twilight, when light intensity changes markedly. Previous researches have shown that the oviposition response of this moth is guided particularly by visual and olfactory cues from host plants. However, the relative importance of visual and olfactory cues in their oviposition preference is largely unknown. As a crepuscular moth, how do choices change as light intensity drops rapidly from day to night? In the present study, through two‐choice behavioural experiments, the oviposition responses of G. molesta to visual and olfactory cues (alone or in combination) from peach shoots were tested at four light intensities ranging from daylight to starlight. Grapholita molesta showed similar oviposition responses to plant cues under 1 000, 100, 1 and 0.01 mW m^?2 illumination. Olfactory cues from peach shoots attracted significantly more oviposition than the negative control, whereas visual cues alone did not. Furthermore, olfactory cues were more attractive than visual cues, and no significant interaction was observed between the responses to the two cues. Our findings indicate that G. molesta females mainly rely on olfactory cues to recognize oviposition sites, regardless of differences in light intensity. These results do not provide evidence for attraction to visual cues, but the possibility that the brightness of leaves might be used to guide oviposition is discussed.     

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.     

Mechanisms of prey finding in the aphidophagous ladybird beetle,Harmonia axyridis [Coleoptera: Coccinellidae]

The mechanism of prey finding in adultHarmonia axyridis was investigated by presenting beetles with small gauze or polyethylene bags containing either aphidinfested leaves or healthy leaves alone together with empty control bags. Beetles were attracted to bags by olfactory and visual cues suggesting the presence of aphids, including the odor of aphid-infested leaves, the odor of aphids, the odor of healthy leaves, and the sight of leaves. Particularly effective in prolonging beetles's stay on bags visited was the odor of aphid-infested leaves. It is suggested that adults ofH. axyridis use olfactory and visual cues to detect prey before actual contact occurs. Use of such cues seems more advantageous than random searching, as has been reported in many previous studies of coccinellid foraging.

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Résumé Le mécanisme de découverte de la proie chez l'adulte d'Harmonia axyridis est étudié en donnant aux Coccinelles de petits sacs en gaze ou en polyéthylène contenant soit des feuilles infestées de pucerons, soit des feuilles saines seules, avec des sacs vides comme témoins. Les coccinelles sont attirées vers les sacs par des indicateurs olfactifs ou visuels suggérant la présence de pucerons, incluant l'odeur des feuilles infestées de pucerons, l'odeur des pucerons, l'odeur des feuilles saines et la vue des feuilles. L'odeur des feuilles infestées de pucerons est particulièrement efficace en prolongeant le séjour des Coccinelles sur le sac visité. Il est suggéré que les adultes d'H. axyridis utilisent des indicateurs olfactifs et visuels pour détecter leur proie avant que s'établisse le véritable contact. L'emploi de tels indicateurs semble plus avantageux que la recherche au hasard, comme cela a été indiqué dans de nombreuses études antérieures sur la quête alimentaire des Coccinelles.

     

Spectral preference and temporal modulation of photic orientation by Colorado potato beetle on a servosphere

The Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), is a diurnal insect that strongly relies on visual cues to guide its walk. In the present study, we investigated the orientation behavior of non‐diapausing walking CPB in response to emissive colors produced by light emitting diodes (LEDs) in a dual choice arena adapted to a servosphere, where the only illumination available came from the photo‐stimuli. Our results demonstrate that CPB show positive phototactic behavior when stimulated with different wavelengths of light; they preferred to orient towards white (420–775 nm), ultraviolet (UV) (351 nm), blue (472 nm), green (570 nm), yellow (585 nm), orange (590 nm), and red (660 nm) over darkness when both alternatives were offered, but no orientation responses were elicited by infrared (940 nm). Both males and females preferred yellow and green over other colors, but did not show any particular preference between them, thus correlating with their preference for wavelengths reflected by vegetation. Sexual differences were noted in that male CPB preferred white over either red or UV, whereas female CPB did not show any preferences when offered these colors. Female CPB preferred UV and blue over red, whereas males showed no preferences when these colors were offered. Colorado potato beetles turned at higher angles and performed more tortuous walks in complete darkness and when infrared vs. darkness were offered compared with the rest of the colored lights. Both sexes preferred continuous over pulsed yellow light. Colorado potato beetles subjected to pulsed yellow light showed a temporal alteration of their walking performance by walking less, slower, and turning at a higher rate. The results are discussed with regard to the role of color in the CPB attraction to host plants and conspecifics as well as the role of intermittent photic stimuli in their orientation behavior. The information provided here provides a basis for the improvement of trapping devices for detection and survey of incipient or invasive CPB, and development of alternate control strategies for this important pest of potatoes and other solanaceous crops.     

Ontogenetic changes in responses to settlement cues by Anemonefish

Population connectivity for most marine species is dictated by dispersal during the pelagic larval stage. Although reef fish larvae are known to display behavioral adaptations that influence settlement site selection, little is known about the development of behavioral preferences throughout the larval phase. Whether larvae are attracted to the same sensory cues throughout their larval phase, or exhibit distinct ontogenetic shifts in sensory preference is unknown. Here, we demonstrate an ontogenetic shift in olfactory cue preferences for two species of anemonefish, a process that could aid in understanding both patterns of dispersal and settlement. Aquarium-bred na?ve Amphiprion percula and A. melanopus larvae were tested for olfactory preference of relevant reef-associated chemical cues throughout the 11-day pelagic larval stage. Age posthatching had a significant effect on the preference for olfactory cues from host anemones and live corals for both species. Preferences of olfactory cues from tropical plants of A. percula, increased by approximately ninefold between hatching and settlement, with A. percula larvae showing a fivefold increase in preference for the olfactory cue produced by the grass species. Larval age had no effect on the olfactory preference for untreated seawater over the swamp-based tree Melaleuca nervosa, which was always avoided compared with blank seawater. These results indicate that reef fish larvae are capable of utilizing olfactory cues early in the larval stage and may be predisposed to disperse away from reefs, with innate olfactory preferences drawing newly hatched larvae into the pelagic environment. Toward the end of the larval phase, larvae become attracted to the olfactory cues of appropriate habitats, which may assist them in identification of and navigation toward suitable settlement sites.     

Disentangling olfactory and visual information used by field foraging birds

Foraging strategies of birds can influence trophic plant–insect networks with impacts on primary plant production. Recent experiments show that some forest insectivorous birds can use herbivore‐induced plant volatiles (HIPVs) to locate herbivore‐infested trees, but it is unclear how birds combine or prioritize visual and olfactory information when making foraging decisions. Here, we investigated attraction of ground‐foraging birds to HIPVs and visible prey in short vegetation on farmland in a series of foraging choice experiments. Birds showed an initial preference for HIPVs when visual information was the same for all choice options (i.e., one experimental setup had all options with visible prey, another setup with hidden prey). However, if the alternatives within an experimental setup included visible prey (without HIPV) in competition with HIPV‐only, then birds preferred the visual option over HIPVs. Our results show that olfactory cues can play an important role in birds’ foraging choices when visual information contains little variation; however, visual cues are preferred when variation is present. This suggests certain aspects of bird foraging decisions in agricultural habitats are mediated by olfactory interaction mechanisms between birds and plants. We also found that birds from variety of dietary food guilds were attracted to HIPVs; hence, the ability of birds to use plant cues is probably more general than previously thought, and may influence the biological pest control potential of birds on farmland.     

Effects of mummy consumption on fitness and oviposition site selection on Harmonia axyridis

Intraguild predation (IGP) has been commonly reported between predators and parasitoids used as biological control agents as predators consuming parasitoids within their hosts. However, the effect of parasitoid–mummy consumption on the fitness of the predator and subsequent oviposition site selection have not been well studied. In our study, we conducted two laboratory experiments to examine the influence of Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) mummies as prey on fitness and subsequently oviposition site selection of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Results indicate that when H. axyridis was reared on A. gifuensis mummies only, its larval development was prolonged, and body weight of the 4th instar larvae and newly emerged adults, and fecundity decreased. Moreover, H. axyridis did not exhibit oviposition preference on plants infested with unparasitized aphids or aphids parasitized for shorter than 9 days. However, compared with plants with mummies (parasitized ≥9 days), H. axyridis laid more eggs on plants with unparasitized aphids. In contrast, H. axyridis previously fed with A. gifuensis mummies did not show a significant oviposition preference between plants with unparasitized aphids and those with mummies (parasitized ≥9 days). Overall, our results suggest that mummy consumption reduced the fitness of H. axyridis. Although H. axyridis avoided laying eggs on plants with A. gifuensis mummies, prior feeding experience on A. gifuensis mummies could alter the oviposition site preference. Thus, in biological control practice, prior feeding experience of H. axyridis should be carefully considered for reduction of IGP and increase of fitness of H. axyridis on A. gifuensis.     

Olfactory mate recognition in a sympatric species pair of three-spined sticklebacks

Mate recognition is critical to the maintenance of reproductiveisolation, and animals use an array of sensory modalities toidentify conspecific mates. In particular, olfactory informationcan be an important component of mate recognition systems. Weinvestigated whether odor is involved in mate recognition ina sympatric benthic and limnetic species pair of three-spinedsticklebacks (Gasterosteus spp.), for which visual cues andsignals are known to play a role in premating isolation. Weallowed gravid females of each species to choose between waterscented by a heterospecific male and water scented by a conspecificmale. Benthic females preferred the conspecific male stimuluswater significantly more often than the heterospecific malestimulus water, whereas limnetic females showed no preference.These species thus differ in their odor and may also differin their use of olfaction to recognize conspecific mates. Thesedifferences are likely a consequence of adaptation to disparateenvironments. Differences in diet, foraging mode, habitat, andparasite exposure may explain our finding that odor might bean asymmetric isolating mechanism in these sympatric sticklebackspecies.