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Phdthesis RF2010 COMMUNAUTE FRANCAISE DE BELGIQUE ACADEMIE UNIVERSITAIRE WALLONIE-EUROPE UNIVERSITE DE LIEGE–GEMBLOUX AGRO-BIO TECH Foraging and oviposition behaviour in the predatory hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae): a multitrophic approach Raki ALMOHAMAD Essai présenté en vue de l’obtention du grade de docteur en sciences agronomiques et ingénierie biologique Promoteurs : Professor Eric HAUBRUGE Dr. François VERHEGGEN 2010 Copyright. Aux termes de la loi belge du 30 juin 1994, sur le droit d’auteur et les droits voisins, seul l’auteur a le droit de reproduire partiellement ou complètement cet ouvrage de quelque façon et forme que ce soit ou d’en autoriser la reproduction partielle ou complète de quelque manière et sous quelque forme que ce soit. Toute photocopie ou reproduction sous autre forme est donc faite en violation de la dite loi et des modifications ultérieures. Almohamad Raki (2010). Le comportement de recherche et de ponte des femelles du syrphe ceinturé, Episyrphus balteatus DeGeer (Diptère, Syrphidae) : approche multitrophique (Thèse de doctorat en anglais). Gembloux, Belgium, Université de Liège – Gembloux Agro-Bio Tech, 165p, 24 fig., 8 tab. Résumé : Les larves du syrphe aphidiphage Episyrphus balteatus (Diptère, Syrphidae) ont une capacité de déplacement limitée. Le choix du site d’oviposition des femelles est donc crucial pour la survie larvaire. Pour cela, les femelles de ce diptère devraient optimiser leurs choix de sites d’oviposition pour maximiser les chances de survie de leurs progénitures. Le but de cette thèse de doctorat était de comprendre comment les femelles d’ E. balteatus évaluent la qualité de patches de pucerons au cours de leur comportement de ponte. La réponse de ponte des femelles d’ E. balteatus observées à travers plusieurs facteurs a été réalisée, parmi lesquels: la plante hôte, l’espèce de pucerons, la taille de la colonie de pucerons, les substances sémiochimiques émises par les pucerons et leurs associations avec leurs plantes hôtes, la présence de compétiteurs intra- ou interspécifiques et l'âge de la femelle. Dans la première partie de ce travail, les résultats obtenus ont permis de mettre en évidence que les femelles d’ E. balteatus sélectionnent le site de ponte en fonction de la plante hôte et l’espèce de puceron, et ce comportement a été aussi montré comme étant lié avec la performance du prédateur (fitness). La combinaison puceron/plante M. persicae /Solanum tuberosum a été la plus préférée par les femelles d’ E. balteatus, et le fitness de ce prédateur était plus élevé en particulier lorsque les larves sont nourries avec M. persicae élevées sur une plante de pomme de terre. De même, les femelles d’ E. balteatus ont montré une même préférence pour les deux combinaisons M. viciae /V. faba et A. pisum /V. faba , et un fitness supérieur du prédateur adulte a été aussi observé lorsque les larves sont nourries avec les deux espèces de pucerons. De plus, nous avons aussi montré que les femelles d’ E. balteatus en recherche de site de ponte sont guidées par des substances volatiles, en particulier le E-(β)-farnésène, émises par les pucerons infestant leur plante hôte. Dans la deuxième partie, le système feuille-disque est démontré comme étant une méthode pratique et efficace pour évaluer le comportement de ponte d’ E. balteatus au laboratoire sous différentes conditions. Les résultats ont aussi démontré qu’il y a une relation quadratique entre l’émission de l’E-(β)-farnésène et la taille de colonie de pucerons, ce qui permet de s’effectuer que cette molécule a un rôle important dans le comportement de ponte des femelles d’ E. balteatus en réponse à la taille de la colonie de pucerons. Les résultats obtenus dans la troisième partie, nous ont permis de montrer que les femelles d’ E. balteatus réduisent leurs pontes dans une colonie de pucerons contenant préalablement des larves de leur propre espèce ou leurs traces. Une réponse similaire a été aussi montrée en présence des substrats préalablement visitées par les larves de coccinelle Harmonia axyridis . Ainsi, la réduction de la ponte des femelles d’ E. balteatus est provoquée par des substances volatiles émises par les substrats des larves de syrphe. Nous avons aussi démontré que la présence du parasitoïde Aphidius ervi dans une colonie de pucerons a un effet significatif sur le comportement de ponte des femelles d’ E. balteatus . Les femelles d’ E. balteatus ne distinguent pas les plants infestées par les pucerons parasités ou non parasités, cependant les femelles réduisent leur pontes en réponse à la présence des pucerons momifiés ou des exuvies de momies. De plus, un fitness supérieur du prédateur a été aussi observé lorsque les larves sont nourries avec l’espèce de pucerons A. pisum parasités ou non parasités. Enfin dans la dernière partie, l’âge de la femelle d’ E. balteatus influence significativement leur reproduction, ce qui permet de proposer que les jeunes femelles (2 à 5 semaines) peuvent être plus efficaces dans la lutte biologique contre les pucerons car elles ont une grande efficacité de reproduction. Toutes les expériences ont été effectuées au laboratoire et la plupart des résultats obtenus sont discutés en relation avec le contexte de la lutte biologique. Almohamad Raki (2010). Foraging and oviposition behaviour in the predatory hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae): a multitrophic approach (PhD thesis). University of Liege – Gembloux Agro-Bio Tech, 165p., 24 fig., 8 tab. Summary: The larvae of predatory hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae), have limited dispersal ability to forage. The selection of the oviposition site by gravid females is crucial for the survival larvae. Therefore hoverfly females should optimise their foraging behaviour by choosing suitable oviposition sites. The aim of this PhD thesis was to understand how hoverfly females assess aphid patch quality during their egg-laying behaviour. The impact of several factors on the oviposition response of E. balteatus females including host plant, aphid species, aphid colony size, semiochemicals emitted from aphids or their association with host plants, presence of intra- or interspecific competitors and female’s age, was clearly demonstrated during this research. In the first part, we have shown that E. balteatus females select their oviposition site according to aphid-host plant and aphid species, which is also shown to be related to offspring performance (fitness). Aphid species Myzus persicae (Sulzer) infested-Solanum tuberosum L. was the most preferred aphid-plant combination as an oviposition site by syrphid females. The E. balteatus survival was enhanced in this system and females laid numerous eggs when larvae were reared with M. persicae as prey, especially when the host plant was potato. Broad bean plants Vicia faba infested with Megoura viciae (Buckton) or Acyrthosiphon pisum (Harris) were equally attractive for E. balteatus females. Aphis fabae (Scopoli) was the least preferred aphid. Higher hoverfly fitness was also observed when larvae were reared on M. viciae or A. pisum compared to those reared on A. fabae . Moreover, it was also demonstrated that foraging hoverfly females is guided by different infochemical cues emitted by aphid host plant, such as ( E)-β-farnesene, enabling them to locate aphid infested plant and to select an adequate oviposition site. In the second part, the leaf disc system was found to be a practical and efficient method to assess the hoverfly reproductive behaviour under different laboratory conditions. Results also showed that there was a significant quadratic relationship between the released ( E)-β- farnesene amounts and aphid colony size, which means that this molecule play important role in oviposition decision made by hoverfly females in response to aphid colony size. In the third part, we have highlighted that the E. balteatus females avoid aphid colonies in which conspecific larvae or their tracks were already present. Similar response was also shown by females to the presence of Harmonia axyridis (Pallas) larval tracks. This oviposition deterring stimulus was also shown to be mediated by odourant cues emitted from larval tracks extracts. It was also demonstrated that the foraging behaviour of hoverfly females was modified by the presence of parasitoids Aphidius ervi (Haliday) in aphid colonies. Females did not exhibit any preference for plants infested with unparasitised or parasitised aphids for 7 days, but they are reluctant to lay eggs in response to the presence of mummies or their exuvia on broad bean plants. Oviposition preference of predatory hoverfly females according to the developmental state of the parasitoid larvae in aphid prey was also found to be related with larval performance. Finally, the age of hoverfly females was found to be an important factor affecting their reproduction ability, suggesting that younger E. balteatus females (2 to 5 weeks old) could be have potential to play a role in biological control of aphids because of their higher reproductive efficiency. All experiments were performed in a laboratory environment and most results obtained are discussed in relation to the context of biological control efforts. I dedicate this work to my Father and mother and I hope that they are satisfied and honored. I also dedicate this work to my wife Fatima and my childrens, Mohamad, Rahma, Ebraheem and Salsabyl for their patience, encouragement and help during the period of study from the first days until the day of these final lines. I can not imagine that I could complete this work without help and support of my loving wife, Fatima Al Aref, I dedicate this work to you my love. Acknowledgements Acknowledgements It is not possible to achieve my PhD study without the help and blessing of God. I must always thank God and ask him to accept this work. The messenger of Allah, Prophet Mohamad (peace and blessing be upon him) said: whoever does not thank people did not thank the God, for this several people have substantially helped me toward this PhD thesis.
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