How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunnel

Abstract The orientation behaviour of Trichogramma egg parasitoids (T.evanescens Westwood and T.pretiosum Riley) in response to the sex pheromone of their noctuid hosts {Mamestra brassicae L. and Heliothis tea (Boddie)) was investigated in a wind tunnel. Wasps were released on platforms which served as models of leaves, and were exposed to overhead light and an air stream that was either clean or loaded with host sex pheromone. The wasps exhibited: upwind anemotaxis, which was not affected by odour; odour-modulated positive phototaxis; and odour-induced inverse orthokinesis. Compared with clean air, residence times, walking times and path lengths on a platform were higher in pheromone-loaded air than in clean air. In pheromone-loaded air, walking velocity was reduced. During locomotion on a horizontal platform, net movement was upwind, regardless of the presence or absence of pheromone in the air. On a platform inclined at 45^o, anemotaxis appeared offset by positive phototaxis. If wasps were released on top of a glass rod above a platform, host sex pheromone caused wasps to land shortly after take-off. These results are used to explain higher rates of parasitism of moth eggs in pheromone-treated plots in earlier field experiments.     

Differential response of Trichogramma wasps to extreme sex pheromone types of the noctuid moth Heliothis virescens

1. Chemical espionage in nature may occur when predators or parasitoids home in on animal or plant communication signals. Parasitoid wasps are known to use pheromones emitted by adults hosts to locate host eggs, larvae or pupae. The response of Trichogramma egg parasitoids to a synthetic sex pheromone blend of moths has been shown in a number of studies over the past 40 years. 2. Trichogramma pretiosum (Hymenoptera, Trichogrammatidae) is a tiny parasitic wasp, attacking the eggs of the noctuid moth Heliothis virescens (Lepidoptera, Noctuidae). This study investigated whether T. pretiosum homes in on the sex pheromone of H. virescens at close range. The arrestment response of the wasps to sex pheromone gland extracts of two types of female moths, so‐called high and low females, was also tested, referring to two selected extreme pheromone types of H. virescens. The study also investigated whether the wasps would mount females, possibly to hitchhike with them. 3. The wasps were arrested by the common, ‘low’ pheromone, but not by the rare, ‘high’ pheromone or by extracts from male hairpencils. The wasps did not show a preference for separate sex pheromone compounds, but when pre‐exposed to the major sex pheromone component of H. virescens before the tests together with H. virescens eggs, they did show a preference, indicating learning behaviour. In the mounting experiments, mated females were mounted significantly more than virgin females or males, suggesting that hitchhiking is a strategy used by these wasps to locate moth eggs. 4. This represents the first study to show a differential response of parasitoid wasps to two different sex pheromone types in a single host species. The results warrant further investigations into the potential role of parasitic wasps in the evolution of sexual communication in moths.     

Biomechanics of the release of sex pheromone in moths: effects of body posture on local airflow

ABSTRACT. The calling posture of Spilosoma congrua Walker (Lepidoptera: Arctiidae) affects local airflow in ways that may impact on the release of chemical signals. Dried specimens of S. congrua imitating resting moths, calling moths, and moths with intermediate postures were placed in a wind tunnel. The wind speed was measured near the abdomenal tip where sex pheromone emission occurs. The calling posture, wings-up, gave significantly greater mean wind speeds near the surface of the sex pheromone gland, effectively eliminating the dead air space that surrounds a non-calling moth. The calling posture also decreased the relative intensity of turbulence near the pheromone gland surface.     

Olfactory attraction of egg parasitoids to virgin females of noctuid stemborers

To locate hosts, egg parasitoids rely on infochemicals of the adult host stage, e.g. pheromones, rather than cues emitted by the inconspicuous egg themselves. Here, we show that three different egg parasitoid species the scelionids Telenomus busseolae Gahan and Telenomus isis Polaszek and the trichogrammatid Trichogramma bournieri Pintureau & Babault were attracted to both calling and non-calling females of the noctuids Busseola fusca (Fuller), Sesamia calamistis (Hampson) and Sesamia nonagrioides (Lefebvre). In Y-tube olfactometer experiments this study revealed a preference of all three parasitoids for non-calling (general odors of virgin females) and calling moth (sex pheromone) over the control (clean air), and for calling over the non-calling moth. However, the three parasitoids were equally attracted to calling moth of B. fusca and S. calamistis indicating low host specificity. The findings indicated that all three parasitoids used the pheromones released by the calling moth in host finding. It is suggested that the low host specificity may affect egg parasitism of the target pest in crop fields.     

Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids

Codling moth is the main pest affecting apples and pears worldwide. Most pest control strategies used against this insect have relied on the use of broad‐spectrum insecticides which have led to non‐desirable effects like pesticide resistance, residues in the environment, human health concerns and the reduction of access to international markets. Therefore, alternative pest control strategies that would result in sustainable fruit production systems while taking care of the environment are strongly promoted. The use of the sterile insect technique has proven to be a valuable pest control tactic within area‐wide integrated pest management strategies, and its synergistic effect for Lepidoptera pests when combined with other biological control tactics such as parasitoids has been documented. The purposes of this research were to evaluate the response of an Argentinean codling moth strain to a sub‐sterilizing radiation dose of 100 Gy and to assess the acceptability and suitability of sterile codling moth eggs by the egg parasitoids, Trichogramma cacoeciae (Marchal) and Trichogramma nerudai (Pintureau and Gerding). Irradiated female moths survived better than irradiated male moths and non‐irradiated male and female moths. Also, the fecundity of irradiated female moths was reduced by more than 30% as compared to non‐irradiated ones whereas their fertility was close to zero. The F₁ generation was male biased with a lower fertility (inherited sterility) than the parental generation. Trichogramma cacoeciae and T. nerudai parasitized both fertile and sterile eggs. However, there was a significant reduction in acceptability for sterile eggs. Trichogramma nerudai parasitized more eggs than T. cacoeciae, but egg acceptability for this species was proportionally lower than for T. cacoeciae especially on eggs oviposited by irradiated females. Development to adult of both parasitoids species was not substantially affected by the origin of the eggs and the wasps had acceptable levels of adult emergence, survival and fecundity. These results provided useful information on the potential for controlling the codling moth using egg parasitoids and the sterile insect technique in Argentina.     

Response of the egg parasitoid Trichogramma pretiosum to the sex pheromone of its host Heliothis zea

This paper presents results of olfactometer experiments with the egg parasitoid Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) and its host the corn earworm moth, Heliothis zea (Boddie) (Lepidoptera: Noctuidae). The sex pheromone of the host significantly reduced the total number of border crossings between odour fields in the olfactometer. Also, female parasitoids made significantly more visits to the calling moth odour field than to the opposite control field in the olfactometer. Further, the wasps spent significantly more time in the olfactometer field containing the sex pheromone released by calling virgin moths, than in control fields. If non-calling virgin moths were used as odour source, the response was reversed and wasps were repelled by the odour of the moths, and the numbers of visits were evenly distributed over the four flow fields. These results are discussed in the context of foraging ecology of egg parasitoids.

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Résumé Des expériences menées en olfactométrie avec le parasite oophage Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) et son hôte, Heliothis zea (Boddie) (Lepidoptera: Noctuidae) donnent les résultats suivants. La présence de la phéromone sexuelle de l'hôte réduit de façon significative le nombre de passages entre les champs odorisés. De mème, les parasites visitent plus fréquemment le champ qui dispense l'odeur de la femelle en appel que le champ témoin placé à l'opposé. Par ailleurs, le temps passé dans le champ qui contient la phéromone sexuelle émise par les femelles vierges en appel est significativement supérieur à la durée de visite des champs témoins. Si l'on utilise comme source d'odeur des femelles vierges qui ne sont pas en appel, la réponse est inversée, les parasites sont alors repoussés par l'odeur de ces papillons et le nombre de visites est distribué de façon aléatoire entre les quatre champs. Ces résultats sont discutés dans le contexte de l'écologie du comportement de recherche chez les parasites oophages.

     

Pheromone pre-exposure and mating modulate codling moth (Lepidoptera: Tortricidae) response to host plant volatiles

Abstract 1 Two codling moth Cydia pomonella kairomonal attractants, ethyl (E,Z)‐2,4‐decadienoate (pear ester) and (E)‐β‐farnesene, were tested in an insecticide‐sprayed apple orchard and an orchard treated for mating disruption with synthetic pheromone (E,E)‐8,10‐dodecadienol (codlemone). Male captures with pear ester were higher in the pheromone‐treated than in the insecticide‐treated orchard, whereas captures with (E)‐β‐farnesene were not different. Subsequent wind tunnel experiments confirmed that pre‐exposure to sex pheromone codlemone increased the behavioural response of codling moth males to pear ester. This supports the idea that male attraction to the plant volatile pear ester and sex pheromone codlemone is mediated through the same sensory channels. 2 Pear ester is a bisexual codling moth attractant and even captures of female moths were significantly increased in the pheromone‐treated orchard. In the laboratory wind tunnel, pheromone pre‐exposure had no effect on female response to pear ester, but significantly more mated than unmated codling moth females flew upwind towards a pear ester source. Differences in mating status in insecticide‐treated vs. pheromone‐treated orchards may thus account for the differences in female trap captures with pear ester. 3 These findings are important with respect to monitoring of codling moth with pear ester in mating disruption orchards. They also emphasize the importance of host plant volatiles in pheromone‐mediated mating disruption, which has been neglected to date.     

Evaluation of dyes for marking painted apple moths (Teia anartoides Walker, Lep. Lymantriidae) used in a sterile insect release program

Abstract  Two methods of marking painted apple moth ( Teia anartoides Walker, Lepidoptera: Lymantriidae), internal and external dyes, were investigated for use with the sterile insect technique, to ensure that wild and released moths could be distinguished absolutely during the eradication program. Calco Red dye was used to mark all moths internally. It was added to artificial diet and was detectable in the adults. Dye was incorporated into the larval diet at four rates. No differences were observed in mortality of the larvae, fertility of the adult female or response of male moths to virgin females in a flight tunnel. Fluorescent powder dyes were used throughout the sterile insect program to identify irradiated moths, as well as their release location and colony. However, the powdered dyes reduced the ability of male moths to detect a component of the sex pheromone in electro-antennogram tests and to respond to a calling virgin female in flight tunnel trials. Field trials suggest that moths may subsequently overcome these negative effects and respond to female moths, as moths heavily coated in dye were recaptured.     

棉铃虫成虫对高浓度性信息素的行为反应

室内行为实验表明,在高浓度性信息素环境中棉铃虫Helicoverpa armigera (Hübner) 雌蛾更加活跃、觅偶行为更加积极主动、求偶时间显著延长,而雄蛾主动求偶时间显著缩短、静止时间显著延长。高浓度性信息素并未引起成虫在取食活动和产卵行为的明显改变,也未能有效阻断其交配行为,而是推迟了它们的交配日期、夜间初始交配时间,缩短了交配蛾的交配持续时间。因此,高浓度性信息素主要影响其交配质量,而不是交配率。     

Investigations of Mechanisms of Pheromone Communication Disruption of Choristoneura rosaceana (Harris) in a Wind Tunnel

Although atmospheric treatment with synthetic pheromone is used commercially to control several lepidopteran pests, little is known about how mate-finding behavior is altered by this procedure. Mechanisms of disruption of the mate-finding behavior of Choristoneura rosaceana (Lepidoptera: Tortricidae) were examined in wind tunnel bioassays. Male moths were exposed to synthetic sex pheromone or pheromone components prior to or during upwind flight to a calling virgin female. The proportion of males successfully contacting a calling female was reduced only when the synthetic pheromone treatment was presented simultaneously. A synthetic source of the attractive four-component pheromone placed upwind of a calling female was more effective than a less attractive two-component blend in achieving disorientation. Habituation of the central nervous system does not appear to be a significant factor in disruption of mate-finding behavior of male C. rosaceana, as exposure to pheromone prior to the bioassay did not alter the proportion of males that achieved subsequent upwind flight. Disruption of mate-finding behavior of C. rosaceana in a wind tunnel is probably the result of a combination of mechanisms including adaptation of antennal receptors, camouflage of the female-produced plume, and false-trail following which contributed to the additive disruption effect observed with the most attractive four-component pheromone.     

棉铃虫Helicverpa armigera对性外激素和植物气味物质的嗅觉反应(英文)

本文用EAG技术研究棉铃虫对性外激素和植物气味物质的嗅觉反应。供试的气味物质有棉铃虫性外激素的二种主要组分和36种与棉铃虫寄主植物有关的植物气味物质。试验结果表明：1）只有棉铃虫雄蛾对性外激素组分产生反应,二种性外激素的组分中,Z-11-16：AL能引起较强的EAG反应。2）对植物气味物质,雌雄棉铃虫之间的嗅觉反应没有明显的差异。棉铃虫对性外激素和植物气味组分的嗅觉感受过程是一个有选择性的感受过程：不同种类的气味物质能引起不同的EAG反应。只有棉铃虫雄蛾才对性外激素组分起反应,在二种性外激素组分中：主要组分：Z-11-16：AL引起的EAG反应最高,高于大多数植物气味物质。次要组分Z-9-16：AL引起的EAG反应很弱。雌、雄棉铃虫对植物气味组分的嗅觉反应的选择性表现出一致的规律：对苯甲醛和绿叶气味物质的反应最高。单萜类中的萜烯衍生物（萜类醇、醛、酯等）的触角电位反应次之。棉铃虫对大多数的供试化合物的EAG反应都很小。最后,作者讨论了性外激素和植物气味物质对棉铃虫行为的作用。     

Habituation of sexual response in male Heliothis moths

It has been generally hypothesized that habituation mediates the effects of pheromone‐based disruption strategies used in the management of moth pests. The current study demonstrates that pheromone‐mediated sexual response in the tobacco budworm moth, Heliothis virescens (F.) (Lepidoptera: Noctuidae), can in fact be modulated by conditions consistent with the production of habituation. An ethogram was used to measure response strength in a wind tunnel experiment where male moths were allowed to respond freely to one of two different blends of female pheromone in 16 trials over 4 days. Post‐test measures were collected to investigate stimulus specificity and long‐term effects. In conditions appropriate to the formation of habituation, habituation will develop and disrupt male sexual response to female sex pheromone. Males repeatedly exposed to plumes of synthetic pheromone blends display a habituated response lasting up to 96 h. Habituation rate and spontaneous recovery of response strength are greater with less intense stimuli. Additionally, males habituated to one blend express no habituation of sexual response when exposed to a different blend. This indicates a high degree of stimulus specificity, which could facilitate outbreeding, and that moths attend to the configuration of the pheromone blend, not simply to its elements.     

OLFACTORY RESPONSES OF COTTON BOLLWORM,HELICOVERPA ARMIGERA TO SEX PHEROMONE AND PLANT VOLATILE COMPONENTS*

Abstract Electroantennograms (EAGs) were recorded from unmated, laboratory-reared male and female Helicover pa armigera (Lepidoptera:Noctuidae) adults to two sex pheromone components and a range of plant volatile components, some of which are known volatiles from leaves and fruits. The female-produced sex pheromone was not detected by other female moths. The sex pheromone components to which male moths responded previously show to possess biological activity. As for plant volatile components, a large degree of EAG response uniformity between male and female moth was observed. The greatest EAG responses of all plant volatiles tested were elicited by monoenic C-6 alcohol and aldehyde. They are constituents of the “general green-leaf odor” that emanates from most plants. The potential adaptive benefit of selective perception to sex pheromone and green-leaf volatile components is discussed.     

Male orientation to trail sex pheromones in parasitoid wasps: does the spatial distribution of virgin females matter?

We studied male locomotory response to trails and patches of sex pheromone (left respectively by free-ranging females and females constrained to stay on a small area) in the two parasitoids Aphelinus asychis (Hymenoptera: Aphelinidae) and Trichogramma brassicae (Hymenoptera: Trichogrammatidae). Under the hypothesis that the spatial distribution of virgin females differs between these species (scattered among host plants in A. asychis, gregarious at emergence sites in T. brassicae), we predicted that male locomotory response to their sex pheromones should also differ: A. asychis males should follow pheromone trails on plants in order to encounter the females along these trails, whereas T. brassicae males should stay on pheromone patches, at emergence sites, and mate the females on these patches. Using an improved video-tracking system, we found that males of both species respond to conspecific sex pheromone trails and patches, but that the response does not differ much between species. Males released on marked substrates walked in a more convoluted pattern (i.e. higher path fractal dimension and higher number of crossings within tracks) than males released on unmarked substrates. On pheromone patches, males turned persistently in the same direction when leaving the patch, which explains a higher number of visits on marked patches than on unmarked patches, and possibly, higher track convolution on pheromone trails. Contrary to our hypothesis, male A. asychis did not follow female trails more accurately than male T. brassicae, and male T. brassicae did not stay longer on pheromone patches than male A. asychis. We argue that these discrepancies between our predictions and the observed responses originates from discrepancies between the assumed spatial distribution of virgin females and their actual distribution in the wild.     

Evidence for a female sex pheromone in the brassica pod midge Dasineura brassicae

ABSTRACT. The responses of Dasineura brassicae Winn. (Diptera, Cecidomyiidae) to odours from both male and female midges and from their host ( Brassica napus ) and non-host ( Vicia faba ) plants were studied using a Y-tube olfactometer. Female but not male D. brassicae are attracted to crushed B. napus leaves but not to those of V. faba. Males are attracted to live virgin females, to crushed virgin and mated females and to hexane washes of females, suggesting that the female produces a sex pheromone that attracts males. Males were also attracted to hexane washes of female ovipositors, but not to washes of the bodies of females without ovipositors, suggesting that the ovipositor is the site of pheromone release or production. Males were not attracted to live mated females or to other live or crushed males and mated females were not attracted to other mated females.     

楸螟行为观察及性信息素粗提物生物活性测定

本文报道了楸螟Omphisa plagialis Wileman的羽化昼夜规律和（25±1）℃、光周期L∶D=14∶10条件下的雌蛾求偶节律,用Y形管法测定了雄蛾对雌蛾性信息素粗提物的行为反应。结果表明：楸螟的羽化发生在10：00到23：00之间;雌蛾在羽化当天即开始求偶,求偶行为集中在暗周期的23：30到01：30之间。采用正己烷提取的雌蛾性信息素粗提物存在性信息素成分,对雄蛾具有一定的引诱活性。     

Composite asymmetry as an indicator of quality in the beneficial wasp Trichogramma nr. brassicae (Hymenoptera: Trichogrammatidae)

Trichogramma are egg parasitoids that are widely cultured for the control of moth pests in commercial insectaries. Stock quality is often maintained by releasing wasps from a mass culture in an area with target host eggs and initiating fresh stocks from parasitized eggs. Here we test if variability among individuals as measured by fluctuating asymmetry can be used as an additional method of quality control in Trichogramma nr. brassicae by comparing fluctuating asymmetry levels between a random sample of wasps before release and wasps that successfully reach host eggs. Although the asymmetry of individual traits was not associated with wasp fitness, a total asymmetry measure based on combining the uncorrelated asymmetries of nine traits did predict the ability of wasps to reach the eggs.     

Visual cues collimate the trajectories of almond moth Cadra cautella males flying in wind and still air within a wind‐formed plume of pheromone

Male Cadra cautella (Walker) moths are videotaped in three dimensions in a 3‐m long wind tunnel as they fly within a 65‐cm wide plume of pheromone. Moths are presented two floor patterns, either ‘aligned’, a 25‐cm wide ‘trail’ of solid red circles along the tunnel's midline, or ‘offset’, in which the trail veers 25 cm to the left at the tunnel's midpoint. These visual patterns are presented either in a continuous airflow or airflow that is stopped before moths reach the tunnel's halfway point. Moths fly relatively straight paths over the aligned pattern in still air after the wind is stopped. With the offset pattern in wind and when the wind is stopped, moths swerve towards the offset pattern before again progressing along the plume. Prominent visual cues appear to ‘collimate’ (i.e. align with a directional cue) the moth's course as long as the moth remains in contact with pheromone. In wind, these moths appear to favour trajectories that enhance visual feedback, even if the path taken is not directly upwind. During wind lulls, this manoeuvre may enable moths to continue progress towards calling females along a visually set course. The centring of trajectory over prominent visual cues suggests that these moths favour a route that enhances visual feedback.     

The development of an improved model trap for monitoring Ephestia cautella

Delta, Covered funnel and Uni-traps containing pheromone used for monitoring male Ephestia cautella (Walker) (Lepidoptera: Phycitidae) moths were compared in a wind tunnel in moving and still air. The shape and design of the traps and the form of pheromone plume emitted from them determined the moth's latency time, numbers orientating, alighting on the traps and captured. To improve trap design, the visual responses of the moths to rectangles of different colours and sizes and to brown and white stripes, showed that more moths were attracted to darker coloured 6×50 cm vertical rectangles on a white background and to 7.5 mm brown and white stripes. A cylindrical trap containing pheromone incorporating these features captured 90% and 80% of the moths released in the wind tunnel in moving and still air respectively, compared with 70% and 35% for the best commercial traps.     

Antennal responses of Cydia pomonella (L.) exposed to surfaces treated with methoxyfenozide

Electroantennogram (EAG) measurements were recorded from the antennae of male and female codling moth, Cydia pomonella L., to determine whether adult moths exposed to surfaces treated with the ecdysteroid agonist methoxyfenozide experience a decline in their antennal reception and thus olfactory sensitivity. Such a phenomenon would offer a possible mechanism for the previously reported decreased responsiveness from moths treated with methoxyfenozide to pheromone‐ and plant volatile‐based monitoring lures. Mean EAG data revealed that the antennae from methoxyfenozide‐treated male moths appear to be just as sensitive to various doses of synthetic codlemone as the antennae from the control and surfactant‐treated moths, but they appeared to be less sensitive to the pheromone component 12OH (collected from female effluvia) than the control male antennae. Mean male EAG responses to the pheromone components E8,E10‐12Al and codlemone collected from methoxyfenozide‐treated females were significantly less than the responses towards those two pheromone components collected from the control and surfactant‐treated females. Female moth exposure to methoxyfenozide did not negatively impact the sensitivity of female antennae to the plant volatile pear ester, but it did towards the apple volatile butyl hexanoate. Data from this study show that adult C. pomonella exposure to methoxyfenozide‐treated surfaces does appear to negatively impact, in a minor way, the (i) olfactory sensitivity (or detection) of male antennae towards some components of the female sex pheromone, (ii) the female antennal sensitivity towards a key apple volatile and (iii) the attractiveness of female pheromone effluvia.