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Aspects of the sensory physiology of the pollination of "Petunia axillaris" and mating in moth pests
Les composés produits par les plantes ont un impact important dans plusieurs aspects de la biologie de nombreux insectes et les plantes sont une source de nourriture particulièrement importante. A l’état adulte, les insectes utilisent ces messages chimiques pour identifier et localiser une source de nourriture qui leur convient. La spécificité de la plante est aussi cruciale pour le bon développement des larves peu mobiles. Le choix du lieu de ponte est donc important pour la survie de la progéniture et est également grandement déterminé par l’odeur spécifique des plantes hôtes. Il a aussi été prouvé que le comportement sexuel des insectes est influencé par les odeurs de plante hôte en augmentant la sensibilité des mâles aux phéromones sexuelles.
Petunia est un genre de plante particulièrement intéressant pour étudier le rôle des caractères floraux dans la spéciation, car toutes les espèces connues sont capables de se croiser artificiellement. Toutefois, l’hybridation sur le terrain reste rare. L’isolation reproductive est alors assurée par l’attraction sélective des pollinisateurs. Il existe chez Petunia trois syndromes de pollinisation distincts correspondant à autant de guildes de pollinisateurs : abeilles, sphingidés ou colibris. P. axillaris attire Manduca sexta, un sphingidé, en produisant une puissante odeur. En revanche, P. exserta qui est pollinisé par des colibris ne relâche aucune odeur. Le croisement de ces deux espèces permet d’étudier la base génétique de l’évolution du parfum chez Petunia et son importance dans la préférence de butinage de M. sexta. Nous avons caractérisé le parfum de P. axillaris et confirmé que P. exserta ne produisait pas d’odeur. Nous avons montré que M. sexta est très sensible à ces composés, particulièrement au methyl benzoate, benzyl alcohol et méthyl salicylate de P. axillaris. Finalement, nous avons observé par le comportement en chambre de vol que les plantes produisant des odeurs étaient toujours préférées, quel que soit la couleur de la fleur. Nous en avons déduit que la production de parfum et un trait floral déterminant dans la relation plante-insecte et que ce trait peut à lui seul changer la préférence de butinage de M. sexta. Les conséquences de ces résultats sur la spéciation chez Petunia sont discutées.
Chez les insectes l’attraction spécifique par certaines odeurs est en grande partie modulée par la présence de nourriture. Nous nous sommes intéressés à la perception de M. sexta aux différents nutriments énergétiques essentiels que sont les sucres. Après avoir caractérisé les sensilles gustatives de son proboscis, nous avons mesuré la réponse neuronale des sensilles styloconiques et basiconiques au glucose, fructose et sucrose. Pour les deux types sensillaires, la réponse au fructose est légèrement plus intense qu’au sucrose alors que celle au glucose est imperceptible à la dose testée. Parallèlement, la préférence de nourrissage du papillon a été évaluée en choix binaires. Il en découle que les papillons préfèrent se nourrir de sucrose ou de fructose par rapport au glucose. De plus il parvient à détecter de faible concentration de sucrose et préfère se nourrir sur les solutions les plus concentrées. Finalement, il semble que le volume de solution de sucrose soit déterminé par sa concentration. La préférence comportementale pour ces sucres est bien corrélée avec leur perception neuronale.
Le ver de la grappe, Lobesia botrana, et le ver de la pomme, Cydia pomonella, sont tous deux de très importants insectes ravageurs des cultures à l’échelle de la planète. Sans mesures de contrôle adéquates, les pertes financières sur les cultures peuvent être considérables. La confusion sexuelle est une méthode spécifique de lutte utilisant la phéromone sexuelle pour attirer les mâles vers des leurres et ainsi diminuer les probabilités d’accouplement. Utiliser des produits de plantes hôtes pour améliorer l’attraction des mâles par les phéromones sexuelles présente une possibilité intéressante. Nous avons mesuré l’attraction des mâles de L. botrana à différent doses d’heptane ou d’octane en combinaison avec une concentration sous-dosée de phéromone. Alors que l’attractivité du mélange augmente avec la dose pour les deux produits, nous obtenons une proportion maximale de papillons arrivant à la source avec 10 ng/min d’alcane relâché avec la phéromone, un niveau d’attraction comparable avec celui obtenu avec des phéromones directement relâché avec des femelles. Alors que ces alcanes sont inactifs seuls, la phéromone directement dilué dans l’heptane induit non seulement autant de contact avec la source qu’avec un solvant classique, mais recrute plus de papillons dans les premières phases d’attraction. Un autre composé de plante, le 2-phénylethanol augmente également l’attraction de la phéromone lorsqu’il est relâché à 100 pg/min. De plus, lorsque l’un de ces composés de plante est ajouté à la phéromone, le temps que met le papillon pour atteindre la source est réduit de moitié. Tous ces résultats sont confirmés également chez C. pomonella. Le large spectre de concentrations où ces alcanes sont actifs chez ces deux espèces offre un outil prometteur pour améliorer le contrôle des populations sur le terrain en utilisant la confusion sexuelle.
Au travers de cette thèse, nous avons étudié les interactions plantes-insectes sous plusieurs facettes. Nous avons montré comment une plante arrive à manipuler un pollinisateur pour parvenir à se reproduire, ou comment un papillon utilise les stimuli chimiques d’une plante pour se nourrir. Nous avons également démontré que certaines odeurs de plantes amélioraient les chances des papillons mâles à trouver une femelle., Compounds produced by plants have an important impact on many aspects of the biology of insects from whom plants are a particularly important source of food. As an adult, insects use chemical messages to identify and locate a suitable food source. The specificity of the host plant relationship is also crucial for healthy development of larvae. The choice of oviposition site is determinant for the survival of offsprings and is largely selected by the specific array of host plants stimuli. It has also been shown that the sexual behaviour of insects is influenced by host plant odours by increasing the sensitivity of males to sex pheromones of females.
The genus Petunia is particularly interesting to study the role of floral traits in speciation because all the known species are artificially crossable. However, hybridization in the field is rare as the reproductive isolation is provided by the selective attraction of pollinators. Three distinct pollination syndromes have emerged in Petunia, corresponding to as many guilds of pollinators: bees, hummingbirds or hawkmoths. P. axillaris attracts hawkmoths such as Manduca sexta, a Sphingidae, by releasing a strong sweet odour. In contrast, P. exserta which is pollinated by hummingbirds is devoid of scent. Crossings between these two species were exploited here to study the genetic basis of the evolution of fragrance in Petunia and its importance in foraging preferences of M. sexta. We characterized the scent of P. axillaris and confirmed that P. exserta produces no odour. We show that the antennal olfactory receptor cells of M. sexta is very sensitive to the compounds released by P. axillaris, especially methyl benzoate, benzyl alcohol and methyl salicylate. Finally, we observed through choice tests in a wind tunnel that plants producing odours were always preferred, regardless of the colour of the flower. We conclude that the production of fragrance is an important floral trait in this plant-insect relationship and that this feature alone can modify the foraging preference of M. sexta. The implications of these findings on speciation processes in Petunia are discussed.
In insects specific attraction by odours is largely modulated by the presence of food. We were interested in the perception of different essential energy nutrients including nectar sugars by M. sexta. We have characterized the taste sensilla on the proboscis and measured the neural response of the gustatory receptor cells of styloconic and basiconic sensilla to glucose, fructose and sucrose. For both sensillar types, the response to fructose is slightly stronger than to sucrose while glucose was not detected at the dose tested. Meanwhile, the feeding preference of the moth was assessed through binary choices experiments. It turns out that the M. sexta prefers to feed on sucrose or fructose compared to glucose. In addition, it can detect low concentrations of sucrose and prefers to feed on the most concentrated solutions. Finally, it seems that the volume of sucrose solution imbibed is determined by its concentration. Behavioural preferences by M. sexta for these sugars correlate well with their mouthpart sensory cell responses.
The European grapevine moth, Lobesia botrana, and the codling moth, Cydia pomonella, are both very important worldwide insect pests. Without adequate control, fruit damage can be important and the arising financial losses substantial. Mating disruption is a specific control method using the female sex pheromone to attract males to lures and thus reduce their chances of mating. The use of host plant volatiles to improve the attractiveness of males to sex pheromones presents an interesting possibility to improve the mating disruption control method. We measured the attraction of male L. botrana to different doses of heptane and octane in combination with the underdosed sex pheromone. While the attractiveness of the mixture increases with dose for both products, a maximum number of males arrive at the source with a release rate of 10 ng/min of the alkanes released with the pheromone. This level of attraction is comparable with that obtained with the sex pheromones released directly from calling females. While the alkanes are inactive on their own, the pheromone diluted directly in heptane induces not only contact to the source no different to the control, but recruits more moths in the early stages of flight. Another plant compound, 2-phenylethanol also increases the attraction of the underdosed L. botrana sex pheromone to males when released at 100 pg/min. In addition, when one of these plant compounds is added to the pheromone, the time needed to reach the source is halved in L. botrana. The findings with these plant compounds were confirmed in C. pomonella. The wide range of concentrations over which these alkanes are active in both species provides a promising mean to improve control of field populations using mating disruption.
Throughout this thesis we studied plant-insect interactions from different angles. We have shown how a plant can manipulate a pollinator to achieve pollination, alternatively, how a moth selects plant stimuli to cover its energy needs. We have also shown that hitherto unstudied plant volatiles improved the chances of male moths to encounter females.
Responses of the tropical bont tick, Amblyomma variegatum (Fabricius), to its aggregation-attachment pheromone presented in an air stream on a servosphere
Male Amblyomma variegatum ticks feeding on a host release a mixture of o-nitrophenol and methyl salicylate which serves to attract conspecifics. The behavioural responses of A. variegatum on a servosphere to these volatiles presented in an air stream are detailed hers. In still air, ticks walked on all eight legs, but with long halts. In contrast, the air stream caused continuous walking and induced a reaching response where the forelegs actively sampled the air. Such reaching increased the angular velocity and reduced walking speed, effects that were amplified in the presence of vapours from o-nitrophenol and methyl salicylate in the air flowing over the ticks. Vapour from a 1:1 mixture of o-nitrophenol and methyl salicylate was attractive over a 10(4)-fold concentration range providing an increase in upwind displacement of 20-40%, significantly higher than the natural ratio where o-nitrophenol vapour predominates. Although the responses to o-nitrophenol vapour were variable when presented alone, this chemical was consistently attractive when delivered with steer hair odour - unattractive on its own. Moreover, the upwind walk to this combination did not cause a change in speed or angular velocity. This supports the hypothesis that the response to the pheromone is enhanced by host odour.
Plant volatile compounds shorten reaction time and enhance attraction of the codling moth (Cydia pomonella) to codlemone
BACKGROUND: The codling moth is the most serious pest of deciduous tree fruit (apples, pears, crabapples, walnuts, quince) worldwide. The high frequency of insecticide treatments per season has resulted in breakdown of codling moth control owing to insecticide resistance. As an alternative, integrated pest management includes mating disruption to achieve population suppression in orchards. Under this scheme, the sex pheromone of the codling moth, (E, E)-8,10-dodecadien-1-ol (codlemone), is released from dispensers in crops to hinder mating by luring males. Increasing the attractiveness of codlemone formulations to codling moth males can be regarded as a key to increasing the efficacy of mating disruption. With this aim, the effects of adding plant volatiles on the behavioural responses of codling moth males to codlemone were tested. RESULTS: Adding R(+)-limonene, linalool, (E)-beta-farnesene or ethyl (E, Z)-2,4-decadienoate to codlemone significantly increases the proportion of males flying to the pheromone source in a wind tunnel. The response level is equivalent to that of males responding to females releasing codlemone. Using real-time recordings, it is shown how these four plant products also shorten the response time of males to codlemone under the behavioural criteria time to activation, time till upwind flight is induced and time to pheromone source contact. CONCLUSION: Shortening the response time and increasing source location by males of dispensers releasing codlemone with R(+)-limonene, linalool, (E)-beta-farnesene or ethyl (E, Z)-2,4-decadienoate added would enhance mating disruption through better engagement ofmales with dispensers, to the detriment of females. (C) 2011 Society of Chemical Industry
Contact chemostimuli in the mating behaviour of the cattle tick, Boophilus microplus
Mating of the cattle tick Boophilus microplus is mediated by chemical stimuli on the cuticle of females. Males are arrested on the dorsum of females attached to the host, frequently sample the substrate, and then tip-over to the ventrally located gonopore. These behaviours are also observed in vitro when males are placed on a small glass bead treated with a female extract. Time spent and tip-over by male ticks on dummies is used in an assay to test the behavioural significance of fractions of the extract. TLC separation yields one apolar fraction that arrests males, though much less so than the whole extract, but lost tip-over behaviour. This apolar fraction contains a series of cholesteryl esters that, when tested individually, show no arrestment activity at levels present in the extract but, when combined, are as active as the fraction. When a small silica column is used for fractionation, all biological activity is reproduced after recombining the fractions. In addition to the early eluting apolar fraction containing cholesteryl esters, a set of highly active more polar fractions is isolated. Electrophysiological recordings from gustatory sensilla on the pedipalps of male B. microplus, which are regularly brought into contact with the cuticle of the female during mating, provide evidence for receptors in two of them responding to the whole extract and to the behaviourally active polar fractions. Mating behaviour involving arrestment and tip-over is clearly initiated by a mixture of chemical stimuli, and tip-over behaviour is associated with the more polar material.
Identification of host-plant chemical stimuli for the European grape berry moth Eupoecilia ambiguella
Olfaction is of major importance for survival and reproduction in moths. Males possess highly specific and sensitive olfactory receptor neurones to detect female sex pheromones. However, the capacity of male moths to respond to host-plant volatiles is relatively neglected and the role that such responses could play in the sensory ecology of moths is still not fully understood. The present study aims to identify host-plant stimuli for the European grape berry moth Eupoecilia ambiguella Hb. (Tortricidae, Lepidoptera), a major pest of vine in Europe. Headspace volatiles from Vitis vinifera L. cv. Pinot Noir, Vitis vinifera subsp. sylvestris and five other host-plant species comprising five different families are analyzed by gas chromatography linked to electroantennogram (EAG) recording from male E. ambiguella antennae and by gas chromatography-mass spectrometry. This procedure identifies 32 EAG-active compounds, among them the aliphatic compounds 1-hexanol, (Z)-3-hexenol, (Z)-3-hexenyl acetate and 1-octen-3-ol; the terpenes limonene, β-caryophyllene and (E)-4,8-dimethyl-1,3,7-nonatriene; and the aromatic compounds benzaldehyde and methyl salicylate. Male and female E. ambiguella show similar EAG response amplitudes to individual chemical stimuli and also to mixtures of plant volatiles, as represented by essential oils from ten other plant species. This possibly indicates a common role for plant compounds in the sensory ecology of the two sexes of E. ambiguella.
Contact chemostimuli in the mating behaviour of the cattle tick, Boophilus microplus
Mating of the cattle tick Boophilus microplus is mediated by chemical stimuli on the cuticle of females. Males are arrested on the dorsum of females attached to the host, frequently sample the substrate, and then tip-over to the ventrally located gonopore. These behaviours are also observed in vitro when males are placed on a small glass bead treated with a female extract. Time spent and tip-ever by male ticks on dummies is used in an assay to test the behavioural significance of fractions of the extract. TLC separation yields one apolar fraction that arrests males, though much less so than the whole extract, but lost tip-over behaviour This apolar fi action contains a series of cholesteryl esters that, when tested individually, show no arrestment activity at levels present in the extract but, when combined, are as active as the fraction. When a small silica column is used for fractionation, all biological activity is reproduced after recombining the fractions. In addition to the early eluting apolar fraction containing cholesteryl esters, a set of highly active more polar fractions is isolated. Electrophysiological recordings from gustatory sensilla on the pedipalps of male B. microplus, which are regularly brought into contact with the cuticle of the female during mating, provide evidence for receptors in two of them responding to the whole extract and to the behaviourally active polar fractions. Mating behaviour involving arrestment and tip-over is clearly initiated by a mixture of chemical stimuli, and tip-over behaviour is associated with the more polar material. Arch. Insect Biochem. Physiol. 39:65-80, 1998. (C) 1998 Wiley-Liss, Inc.