A learning-related variation in electroantennogram responses of a parasitic wasp

ABSTRACT Odour responses of parasitic insects, in search of their hosts, can change due to experience. Leptopilina heterotoma (Thomson) (Hymenoptera; Eucoilidae), a parasitic wasp of drosophilid larvae, is known to alter its preference for odours emanating from host food substrates through learning. These kinds of behavioural modifications in insects are assumed to be the result of complex processes in the brain. The results presented in this report, however, suggest that this learning-related behavioural variation is not restricted to brain processes but that it involves changes in sensitivity of olfactory receptor neurones.     

In-flight orientation to volatiles from the plant-host complex in Cotesia rubecula (Hym.: Braconidae): increased sensitivity through olfactory experience

Abstract. Plasticity in in-flight orientation to odours from the plant-host complex (PHC: plant infested by the host) was investigated in Cotesia rubecula , a specialist larval parasitoid of Pieris rapae which feeds almost exclusively upon cruciferous plants. A wind tunnel was used to study effects of both concentration of volatile emissions and females' experience. A low proportion of naive wasps located weak odourant sources, i.e. either a single cabbage leaf or a leaf with two first stadium P.rapae larvae. This rate could be elevated by increasing the odour concentration or by providing the wasps with either a previous oviposition experience on the PHC or an exposure to the PHC odour. Previous oviposition on washed larvae (diet-fed, starved and then rinsed with distilled water) in an odourless environment had no effect, which suggested that increased sensitivity to the PHC odour resulted from olfactory experience. The number of mature eggs in a female was affected by oviposition on the PHC or washed larvae but not by exposure to the PHC odour. Therefore the number of mature eggs available was not correlated to the observed differences in orientation behaviour. Possible mechanisms of the behavioural changes described are discussed in the light of the host specificities of C.rubecula and P.rapae.     

Environmental variation in physical and chemical cues used by the parasitic wasp,Aphytis melinus, for host recognition

O-caffeoyltyrosine is a host recognition kairomone forAphytis melinus DeBach (Aphelinidae) found in the covers of its host, California red scale,Aonidiella aurantii (Maskell) (Diaspidae). This study tests the hypothesis that the concentration ofO-caffeoyltyrosine and scale cover size are reliable indicators of scale body size, an important component of host quality forA. melinus, over a range of scale rearing conditions. Both scale cover area andO-caffeoyltyrosine concentrations were only qualitatively related to scale body size during the third instar, the scale life stage most suitable forA. melinus. Scale cover area andO-caffeoyltyrosine concentrations were reduced, relative to scale body size, when scale were reared on bark and leaves compared to fruits. Scale cover area andO-caffeoyltyrosine concentration were also relatively reduced when scales were reared in mid-summer compared to spring and fall, and when reared on orange cultivars compared to lemon cultivars in the field. Finally, scale cover area andO-caffeoyltyrosine concentration were reduced when scale were reared at 52% compared to 100% humidity in the laboratory. Scales appear to be chemically conspicuous toA. melinus for a short period of the time in which they are physiologically susceptible. Scales that minimize their cover size and maximize the incorporation rate ofO-caffeoyltyrosine into covers may minimize their conspicuousness toA. melinus. Minimizing scale cover size, but not necessarily incorporation rates, may make scales more vulnerable to predators, however.     

Flight responses of tsetse flies (Glossina) to octenol and acetone vapour in a wind-tunnel

Abstract. Female Glossina morsitans morsitans Westwood were video-recorded in a wind-tunnel as they entered, in crosswind flight, a broad plume of either octenol or acetone (two components of ox odour). Both odours produced upwind turning responses (in-flight anemotaxis) to a range of concentrations, with thresholds at around 10^-8mg1^-l for octenol and 10^-6mg1^-1 for acetone. Kinetic responses were unaffected by octenol at low concentrations, but flight speed was significantly reduced and sinuosity (^om^-1) and angular velocity (^os^-1) significantly increased by concentrations at or above those in ox breath; for acetone, these effects were apparent but inconsistently related to concentration. It is concluded that octenol and acetone vapour are used by tsetse flies to locate hosts by upwind anemotaxis, probably combined with kinetic responses. The behavioural basis for the 'repellency' of high octenol concentrations in the field is discussed in the context of the virtual loss of upwind anemotaxis to octenol at the highest concentration tested in the tunnel (30 × ox breath).     

Electrophysiological and behavioral responses of a parasitic wasp to plant volatiles induced by two leaf miner species

In the present study, Y-tube olfactometric assays demonstrated that headspace volatile extracts collected from leaf miner-damaged, or artificially damaged, bean plants were more attractive to naive females of the parasitoid insect Opius dissitus than those collected from healthy plants. Headspace extracts from both Liriomyza huidobrensis and Liriomyza sativae second-instar larvae-damaged beans were analyzed by coupled gas chromatography-electroantennographic detection (GC-EAD). Of nine EAD-active volatiles identified, (3E)-4,8-dimethyl-1,3,7-nonatriene, (3Z)-hexenyl acetate, (syn)-2-methylpropanal oxime, and (syn)-2-methylbutanal oxime were the most abundant compounds that evoked significant electroantennogram (EAG) responses. Compounds (3Z)-hexen-1-ol, (anti)-2-methylbutanal oxime, linalool, beta-caryophyllene, and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene also elicited clear EAG responses but were present in smaller amounts. Choice experiments in a Y-tube olfactometer indicated that synthetic versions of (3Z)-hexen-1-ol, 2-methylpropanal oxime, 2-methylbutanal oxime, 3-methylbutanal oxime, linalool, (E,E)-alpha-farnesene, and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene were attractive individually, while (3Z)-hexenyl acetate and (3E)-4,8-dimethyl-1,3,7-nonatriene were unattractive at concentrations similar to those obtained from the headspace collection. Moreover, a blend of nine EAD-active volatiles was significantly more attractive relative to hexane (solvent). A mixture of oximes, tereponids, and green leaf volatiles may facilitate host location by female O. dissitus.     

Flight behaviour of tsetse flies in host odour plumes: the initial response to leaving or entering odour

ABSTRACT. Free-flying, wild male and female Glossina pallidipes Aust. and G. m. morsitans Westw. were video-recorded in the field in Zimbabwe as they entered or left the side of a host-odour plume in cross-wind flight, or as they overshot a source of host odour in upwind flight (camera 2.5 m up looking down at a 3 times 2.5 m field of view at ground level). 80% of cross-wind odour leavers turned sharply ( turns 95^o), but without regard to wind direction (overshooters behaved essentially the same except that nearly 100% turned). Many fewer flies entering a plume cross wind turned ( c . 60%), and when they did they made much smaller turns ( 58^o); these turns were, however, significantly biassed upwind ( c . 70%). All three classes of fly had similar groundspeeds ( 5.5–6.5 m s^_1) and angular velocities ( 350–400^o s^-1). Clear evidence was obtained of in-flight sensitivity to wind direction: significantly more flies entering odour turned upwind than downwind, and odour losers turning upwind made significantly larger turns than average. The main basis for the different sizes of turn was the different durations of the turning flight, rather than changes in angular velocity or speed. No evidence was found of flies landing after losing contact with odour.     

Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula

Comparison of closely related species can elucidate adaptive differences in species characteristics. The present study compares the effect of experience on the host-finding behaviour of two Cotesia (Hymenoptera: Braconidae) parasitoid species that differ in their degree of specialization. After multiple experiences with host larvae, females of the generalist parasitoid Cotesia glomerata showed a clear preference for volatiles from Pieris brassicae-infested Brussels sprouts leaves over P. rapae-infested Brussels sprouts leaves in two-choice tests (preference learning at herbivore level). A single experience with a host did not lead to such preferences.Experience of adult C. glomerata with different P. brassicae-infested cabbage varieties or nasturtium (Tropaeolum majus L.) led to preferences for the experienced plant-host complex in most cases (preference learning at plant level). No effect of rearing plant (early adult learning) on plant preference was found.In contrast to the generalist C. glomerata, females of the specialist C. rubecula did not show preference learning at the herbivore level. At the plant level, experience with different P. rapae-infested cabbage varieties in no case resulted in a difference in preference between treatments. The results support the hypothesis that learning plays a more important role in searching in generalists than in specialist parasitoids. The behaviour of the generalist C. glomerata was more easily changed by experience than that of the specialist C. rubecula.     

Host Search behaviour by Rhagoletis pomonella files: inter-tree movement patterns in response to wind-borne fruit volatiles under filed conditions

Abstract. Responses of Rhagoletis pomonella (Wash) (Diptera: Tephritidae) to synthetic host fruit violates were studied in the field. Individually marked females were released in the centre of a 25 m² patch containing twenty-five host trees ( Crataegus mollis var, toba ) and followed as they moved within and between trees. Fly response to three experimental conditions was studied: (1) 'clean' air; (2) synthetic host fruit violates (apple) permeating the patch; and (3) a single point source of odour placed c 1m away from the edge of the patch. Files in a patch permeated with host odour moved faster, exhibited more straightened-out moves, and reached the edges of the patch more quickly than those exposed to clean air. Flies exposed to a point source of odour exhibited clear orientation responses, arriving consistently at the tree harbouring the source of odour. Odour exposure was intermittent and usually brief ( c . 20s^-1 exposure) with intervals between exposure periods averaging 103s. Wind speed and direction were highly variable. Flies moved during wind ranging in speed form 0.5 to 4.4 m s^-1, with their activity being greatest at winds below 2m s^-1. Strong winds (>3.5 ms^-1) either arrested movement or enhanced downwind displacement. Our observations tend to support the 'series-of-steps' hypothesis reviewed by Gibson & Brandy (1985) as a mechanism of close-range host location (1-5m from odour source). Our findings are discussed with respect to theoretical and practical implications of insect orientation mechanisms to odours, dispersal, and control strategies.     

Odour-conditioned anemotaxis of apterous aphids (Cryptomyzus korschelti) in response to host plants

ABSTRACT. Orientation responses of adult apterous virginoparae of Cryptomyzus korschelti Börner were recorded using a locomotion-compensator in front of a wind tunnel. Individual aphids were tested under four consecutive treatments: without wind; clean wind; and wind carrying odour of the host plant Stachys sylvatica or odour of a non-host plant Solanum tuberosum. The walking tracks were tortuous in all treatments except when the odour of host plants was used. Host plant odour induced upwind orientation of aphids (odour-conditioned positive anemotaxis). Track variables such as vector length, straightness, upwind time and upwind length, increased when the aphids moved upwind. Walking speeds were not affected. The simultaneous stimulation by wind and host plant odour caused aphids to walk upwind for more than 1 m in 10 min. These findings suggest that olfactory attraction of aphids is involved in host plant selection.     

The olfactory response of cabbage root fly Delia radicum to the host plant volatile allylisothiocyanate

The responses of gravid female cabbage root flies, Delia radicum (L.), to brassica odour and allylisothiocyanate (ANCS) presented in either a discrete plume or uniformly dispersed in air passing through a wind tunnel were investigated. Relatively fast, straight flights occurred in diffuse odour conditions, while in discrete plumes flights were slower with more frequent changes of direction.Flies maintained a constant ground speed and track angle over the straight legs of their flight tracks in two different wind speeds by changing air speed and course. As flies approached an odour source in a discrete plume ground speed was progressively decreased and frequency of turning increased but track angles remained constant. This was achieved by reducing air speed and course angle.Flies released at increasing distances from an odour source moved upwind towards it in a series of short flights, the number relating to distance.The results are discussed in the light of current theories of anemotactic odour source locations and a sequence of orientated behaviour for host plant finding is proposed.

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Les réactions olfactives de Delia radicum à l'allylisothiocyanate volatil émis par les plantes-hôtes

Résumé L'étude a porté sur les réactions de femelles fécondées de Delia radicum L. à l'odour de chou et à l'allylisothiocyanate (ANCS) offerts, soit sous forme d'un fin panache, soit uniformément répartis dans l'air traversant un tunnel à vent.Avec une odeur diffuse les vols étaient relativement rapides et rectilignes, tandis qu'avec un fin panache les vols étaient plus lents avec des changements de direction plus fréquents.En présence de deux vitesses du courant d'air les mouches ont maintenu leur vitesse au sol et leur angle de vol par rapport à la direction du déplacement constants en modifiant leur vitesse de vol et leur direction.Quand les mouches approchaient de la source odorante dans un fin panache, la vitesse au sol diminuait progressivement et la fréquence des virages augmentait, les angles de vol restant constant. Ceci était obtenu en réduisant de la vitesse de l'air et l'angle du déplacement.Les mouches paraissent utiliser une anémotaxie optomotrice et mécanique pendant la localisation de l'hôte. Les résultats sont discutés à la lumière des théories classiques sur la localisation anémotactique des sources odorantes.

     

Host plants of the herbivorous insect Mythimna separata (Lepidoptera: Noctuidae) affect its susceptibility to parasitism by the larval parasitoid Cotesia kariyai (Hymenoptera: Braconidae)

Previous studies have shown that the food plant species consumed by herbivorous insects affect their parasitism by parasitoid wasps or flies, but this phenomenon has only been observed in a limited number of systems. Here, we investigate how feeding on different plant species affects the survival of the rice armyworm Mythimna separata (Walker) (Lepidoptera: Noctuidae) and its successful parasitism by the larval endoparasitoid Cotesia kariyai (Watanabe) (Hymenoptera: Braconidae). Survival rate and pupal weight of unparasitised M. separata fed with daikon Raphanus sativus L. var. longipinnatus was lower than with maize Zea mays L. In addition, caterpillars fed with daikon were less susceptible to parasitism by C. kariyai than those fed with maize, and parasitised M. separata larvae fed with daikon had higher survival rates than those fed with maize. These results indicate that while daikon is not an optimal food for unparasitised caterpillars, it may protect the larvae from death by C. kariyai parasitism.     

Functional response to host density in a parasitic wasp,with reference to population regulation

1. The functional response to, and preference for, the host density in a parasite were examined experimentally using an icheumon wasp, Exidechthis canescens, and its host Cadra cautella under controlled conditions.
2. Wasps were more active in host-searching at higher than lower host densities. Percent parasitism increased rapidly with initial increments in host density and then tended to increase more slowly at higher host densities. A sigmoid functional response curve is indicated, which implies that the parasite is able to control its host even at low densities.
3. Wasps actively selected areas of high host density in which to concentrate host-searching behavior.
4. Host-searching by E. canescens is stimulated by the odor of the host when present, and by food in which hosts have developed but have been removed.
5. Both the functional response and the host-density preference of the parasite are mediated by its host-searching behavior. This relationship is discussed in the context of population regulation.

     

Short Distance Cues Used by the Adult Parasitoid <Emphasis Type="Italic">Microctonus hyperodae</Emphasis> Loan (Hymenoptera: Braconidae,Euphorinae) for Host Selection of a Novel Host <Emphasis Type="Italic">Listronotus oregonensis</Emphasis> (Coleoptera: Curculionidae)

Insect parasitoids use host kairomone to detect their hosts. However, in parasitoid species that attack adult hosts, the mobility of adult insect may mean that the host can move away for kairomone sources. The effect of Listronotus oregonensis LeConte (Coleoptera: Curculionidae) adult sex, feces and movement on host selection behavior by Microctonus’’ hyperodae Loan (Hymenoptera: Braconidae; Euphorinae) females was evaluated in the laboratory. We hypothesized that, in addition of using host kairomones, parasitoids of adult stage should use host movement for host selection. The sex of L. oregonensis did not affect the host selection behavior of M. hyperodae. However, host feces decreased the number of weevil antennations done by M. hyperodae. Microctonus hyperodae stopped less frequently near immobile L. oregonensis than near walking ones and these latter were frequently pursued by M. hyperodae. Host movement was the stimulus that elicited oviposition by M. hyperodae. The adaptive implications of these results are discussed.     

Mammal pollinators lured by the scent of a parasitic plant

To communicate with animals, plants use signals that are distinct from their surroundings. Animals generally learn to use these signals through associative conditioning; however, signals are most effective when they elicit innate behavioural responses. Many plant species have flowers specialized for pollination by ground-dwelling mammals, but the signals used to attract these pollinators have not been elucidated. Here, we demonstrate the chemical basis for attraction of mammal pollinators to flowers of the dioecious parasitic plant Cytinus visseri (Cytinaceae). Two aliphatic ketones dominate the scent of this species; 3-hexanone, which elicits strong innate attraction in rodents, and 1-hexen-3-one, which repels them in isolation, but not in combination with 3-hexanone. The aliphatic ketone-dominated scent of C. visseri contrasts with those of insect-pollinated plants, which are typically dominated by terpenoids, aromatic or non-ketone aliphatic compounds. 3-hexanone is also known from some bat-pollinated species, suggesting independent evolution of plant signals in derived, highly specialized mammal-pollination systems.     

Manoeuvres used by flying male oriental fruit moths to relocate a sex pheromone plume in an experimentally shifted wind-field

ABSTRACT. In a wind-field experimentally shifted in direction by 35d?, flying male Grapholita molesta (Busck) zigzagging upwind either maintained contact with a pheromone plume and followed it across during the shift or lost it and commenced casting at c. 90d? across the shifting windline to locate it eventually in its new position. Males accomplished both of these results by integrating the previously described systems of optomotor anemotaxis and self-steered counterturning, but with faster reaction-times to pheromone on and off than heretofore calculated for this species. We found no evidence that males following the plume across used chemotaxis as proposed for another species, Rather, the sawtoothed-shaped tracks were a result of the anemotactic and counterturning systems responding rapidly and reiteratively to each loss and gain of pheromone along the plume in the shifting wind. The response to an increase or decrease in pheromone concentration by males was to change their course angle to more upwind or more crosswind, respectively, on the very first reversal (within c. 0.15 s) after the concentration changed. Because males adjusted their airspeeds more slowly to changes in concentration, the groundspeeds along the more upwind-orientated legs were lower than those along cross-wind legs, contributing to the sawtoothed shape of tracks of plume-followers. The self-steered counterturning programme also reacted quickly to concentration changes, the reversal intervals tending to be shorter following each contact with pheromone than after each excursion into cleaner wind. Following casting after losing the plume, males relocating the pheromone plume exhibited an upwind ‘surge’ of narrow zigzagging flight because on the first leg in the plume they steered a course more directly upwind than on the previous leg and increased the frequency of counterturning to its highest value while maintaining the relatively high airspeed acquired while casting.     

Zigzagging and casting as a programmed response to wind-borne odour: a review

ABSTRACT. 'Counterturning' (meaning here the execution of a succession of alternating left and right turns) is the common feature in upwind zigzagging and cross-wind casting by flying insects manoeuvring towards a small source of wind-borne odour. Recent progress in understanding its control and function is discussed. Counterturning is internally controlled ('self-steered') in the limited sense that, once initiated by a chemical stimulus, it continues without further changes in the chemical input both in clean air and in a homogeneous cloud of odour. As a reaction it appears to be the kind of chemotaxis distinguished as longitudinal klinotaxis, for which the stimulus is a difference of chemical concentration detected over time along the insect's path, not across it. The new directions taken in response to the stimulus, being self-steered in the above sense, have no necessary relation to the direction of the chemical gradient that provided the stimulus but are influenced by the visual cues generated by wind drift. In wind, the counterturning programme is modulated by changes in the chemical input and simultaneously integrated with anemotaxis, but it can then continue in similar form after the wind has ceased. Unambiguous evidence for these conclusions is so far available only for certain flying male moths responding to sex pheromone. The primary function of counterturning, of all amplitudes and in both zigzagging and casting, appears to be the regaining of contact with an elusive scent.     

Electroantennogram responses of a parasitic wasp, Microplitis croceipes, to host-related volatile and anthropogenic compounds

The parasitic wasp Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) showed its own characteristic electroantennogram (EAG) response profiles to 13 host‐related (cis‐3‐hexenol, α‐pinene (R)‐(+)‐limonene (S)‐(–)‐limonene, trans‐β‐ocimene (±)‐linalool, (–)‐trans‐caryophyllene, α‐humulene, nerolidol, trans‐nerolidol, cis‐nerolidol, methyl jasmonate and indole) and four anthropogenic (2‐diisopropylaminoethanol, 2,2′‐thiodiethanol, 2‐methyl‐5‐nitroaniline and cyclohexanone) volatile compounds. These profiles were similar between males and females except for 2‐diisopropylaminoethanol, which elicited significantly larger EAG responses in males. Among the compounds tested, cis‐3‐hexenol, linalool and cyclohexanone elicited the largest EAG responses. EAG responses were not influenced by the age of wasps between 1 and 13 days after emergence. EAG responses were dose‐dependent, and highly EAG‐active compounds elicited significant EAG responses with less than 10 μg of the compounds at source. Quantification of compounds released from an odour cartridge indicates that release rate is highly dependent on the chemical nature of stimuli, showing up to 10 000‐fold differences in the amount released between different compounds when the same amount was loaded in the odour cartridge. Wasps having undergone a behavioural training regime to be attracted to either cyclohexanone or methyl jasmonate did not show any differences in EAG responses from those of untrained wasps.     

Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch

Optimal host selection models based on dynamic programming predict that the physiological state of a foraging insect, i.e. egg load, energy reserves etc., influences behavioral decisions. To test this prediction, the effect of physiological state on host acceptance of the ectoparasitic wasp Agrothereutes lanceolatus was investigated. Female wasps in plastic cups (regarded as patches) were presented with hosts, and their responses to the hosts were continuously observed. After observations, the wasps were dissected and the number of mature and immature eggs they carried were counted. The results showed that behavioral decisions by the female wasps were influenced by mature egg load, but not by wasp size or immature egg load. Hence the wasps with higher egg loads were more likely to oviposit. The number of hosts previously encountered in a patch (i.e. wasp experience) also had an independent effect on females' host acceptance, indicating that female informational state was updated during foraging in that patch. Female wasps host-fed only when mature egg load approached zero. Concurrent host-feeding was not observed. Parasitoid survival was almost zero when parasitoid eggs were transferred onto hosts that were fed upon, indicating that concurrent host-feeding could cause a high degree of offspring mortality. These three results supported the assumption and prediction of optimal host-feeding models. Parasitoid host selection and host-feeding are discussed in the context of recent models.