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Bottom-Up Effects of Abiotic Factors on Aphid Parasitoid Specialization Effet

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Bottom-Up Effects of Abiotic Factors on Aphid Parasitoid Specialization Effet École doctorale Sciences de la Vie et de la Santé Unité de recherche : UMR Inra 1355, CNRS 7254, UNS THESE DE DOCTORAT Présentée en vue de l’obtention du Grade de docteur en Sciences de la Vie et de la Santé UNIVERSITE CÔTE D’AZUR par Le-Thu-Ha NGUYEN Bottom-up effects of abiotic factors on aphid parasitoid specialization Effet bottom-up du stress hydrique sur la gamme d’hôtes des parasitoïdes de pucerons Dirigée par Eric Wajnberg, Directeur de Recherche, INRA Sophia Antipolis et codirigée par Nicolas Desneux, Directeur de Recherche, INRA Sophia Antipolis Soutenue le 20 Décembre 2017 devant le jury composé de: Yvan Rahbé Directeur de recherche, INRA Lyon Rapporteur François Verheggen Professeur, Univ. de Liège (Belgique) Rapporteur Yvan Capowiez Chargé de recherche, INRA Avignon Examinateur Anne Violette Lavoir Maître de Conférence, Université Côte d’Azur Examinateur Eric Wajnberg Directeur de recherche, INRA Sophia Antipolis Codirecteur de thèse Nicolas Desneux Directeur de recherché, INRA Sophia Antipolis Codirecteur de thèse Cette thèse a été effectuée au sein de l’INRA (Institut National de la Recherche Agronomique), de l’équipe CEA (Écologie des Communautés dans les Agros‐systèmes). 400 Route des Chappes 06903 Sophia‐Antipolis France For my parents, Tony Anh-Khôi, and Lisa Bảo-Anh 2 This page is intentionally left blank. 1 Acknowledgments The pursuit of knowledge and the wind of change brought me to INRA to start this Ph.D. adventure. This project would not have been successful without the cooperation of many people. First, I would like to express my great gratitude to my supervisor, Dr. Nicolas Desneux for his brilliant research strategies and for creating such a dynamic and diverse lab environment. My very grateful thanks to Dr. Anne‐Violette Lavoir whose guidance and insight for every step of the Ph.D. course as well as for her enthusiasm and pedagogical skills. I would like to express my appreciation for Dr. Eric Wajnberg for agreeing to be the director of my Ph.D., for his scientific expertise and his valuable advice on data analyses. I also acknowledge Dr. Yvan Rahbé (INRA Lyon), Prof. François Verheggen (U. Liège, Belgique), Dr. Yvan Capowiez (INRA Avignon), Dr. Anne Violette Lavoir, Dr. Eric Wajnberg, Dr. Nicolas Desneux for agreeing to be the members of my Ph.D. thesis jury. Special thanks to Prof. François Verheggen and Dr. Yvan Rahbé for being rapporteurs. I thank all those who participated in my work. Many thanks to Christianne Métay‐Merrien for accompanying me during main experiments, Philippe Bearez, Edwige Amiens‐Desneux for their technical support. I would like to thank my colleagues Lucie Monticelli and María Concepción Velasco‐Hernández for their collaboration, Abid Ali, Wouter Plouvier and Han Peng for sharing their experience. I also thank Sylvain Benhamou, Morgane Canovas, and Sandra Ougier for their involvement in my experiments. Bless all my dear friends from every part of the world, Maria, Ali, Eva, Awawing, Yanyan, Yusha, Christine, Mateus, Marianne, Sylla, Wenyen, Liu, Rihem, Ricardo, Michele and all colleagues and friends for their good humor, for a trusting, warm and colorful ambiance. Most of all, I thank my family, my parents, my husband, my sister and others for their love, encouragement and unconditional support during this study. My gratitude is to Dr. Gérard Blanc for his thorough reliability and Dr. Pascal Gantet (U. Montpellier) for giving me this opportunity. I am especially grateful to them. This Ph.D. thesis was supported by a fellowship from the French government and funds from the French National Institute for Agricultural Research and the FP7‐IRSES APHIWEB project. I acknowledge this financial support. My stay has been joyful and fruitful thanks to your presence. I have treasured my life in INRA PACA and the chance to meet all of you. This page is intentionally left blank. Abstract Biological control (BC ‐ the use of natural enemies to control pests) is a sustainable, environmentally friendly and cost‐effective method for potential pest management without relying on chemical pesticides. Aphid parasitoids are common natural enemies of aphids, the major worldwide pests in agriculture. The study of parasitoid host specificity contributes to (1) understanding ecological and evolutionary mechanisms underneath ecosystem functioning, and (2) evaluating the efficiency of biocontrol agents, and (3) the ecological risks for non‐target species when using these biocontrol agents. This study focuses on the parasitoids fundamental host specificity at individual level, regarding resource requirements and the context of multi‐trophic interactions under environmental abiotic stress, i.e. water limitation. Aphidius ervi (Hymenoptera: Braconidae: Aphidiinae) was chosen for the present work; this aphid parasitoid is used widely as an ecological model, and is a commercial biological control agent (BCA). On a first hand, A. ervi host specificity index was measured on a broad range of aphid species. On a second hand, the indirect effects of water limitation in plants bearing aphid hosts were investigated on the host specificity of the parasitoid. Furthermore, water stress‐induced modifications in the plant and the aphid life‐history traits were measured. A. ervi was shown to be an intermediate specialist species who attacked all aphid species at high rates but was unable to develop well on many of them. The few that enabled parasitoid development were phylogenetically close and/or belong to the Macrosiphini tribe. Interestingly, a positive preference – performance relationship was found. Under water stress, both preference and performance of parasitoids were affected causing loss of the significant relationship. Water limitation negatively altered the plant nutritional quality resulting in low aphid performance on host plants. This in turn decreased the suitability of aphid hosts for the parasitoid. The impacts of water limitation were not similar across all plant‐aphid combinations and depended on several factors, notably stress‐adapted plant mechanisms and the host specialization of both aphids and parasitoids. Keywords: host specificity, preference‐performance hypothesis, tritrophic interactions, water limitation, biological control 0 This page is intentionally left blank. 1 Table of Contents Résumé de la thèse en français................................................................................................. 8 Summary 14 Chapter 1. Host range testing: biological control practice requiring ecological understanding18 1.1. Biological control of pests in the ecological context ............................................ 18 1.2. Aphid parasitoids as biological control agents ..................................................... 24 1.2.1. Aphids: biology, agricultural importance, and natural enemies ................................ 24 1.2.2. Aphid parasitoids: biology and application in biological control................................ 26 1.2.3. Co‐evolution of parasitoids and aphid hosts .............................................................. 29 1.2.4. The significance of parasitoid host specificity in biological control ........................... 29 Ecology and importance of host specificity ............................................................................ 30 1.1.1. Ecological specialization concept................................................................................ 30 1.3. Ecology of host specificity ..................................................................................... 34 1.3.1. Ecological specialization concept................................................................................ 34 1.3.2. Shades of ecological specialization: specialist vs. generalist species ......................... 35 1.3.3. The continuum of specialization patterns: specialist ‐ generalist .............................. 36 1.3.4. Evolutionary mechanisms of ecological specialization ............................................... 39 1.4. How to evaluate the host specificity of aphid parasitoids? ................................. 41 1.4.1. Host specificity index .................................................................................................. 43 1.4.2. Host specificity specter of Aphidiinae parasitoids ...................................................... 45 1.4.3. The optimal foraging behavior: correlation preference‐performance. ..................... 46 1.4.4. The host specificity testing process in biological control ........................................... 49 Chapter 2. Bottom‐up and top‐down forces in ecological network....................................... 53 2.1. Ecological networks and interactions ................................................................... 53 2.2. Bottom‐up versus top‐down forces ...................................................................... 57 2.3. Bottom‐up forces of abiotic factors on a tritrophic plant‐aphid‐parasitoid system58 2.3.1. How could plant traits mediate bottom‐up and top‐down forces? ..................... 58 2 2.3.2. How could aphid traits mediate bottom‐up and top‐down forces? .................... 60 2.3.3. How abiotic stresses level‐up to parasitoids through the tri‐trophic interaction?61 2.3.4. Bottom‐up and top‐down forces in biocontrol context ....................................... 64 Chapter 3. Objectives ............................................................................................................. 67 Chapter 4. Aphid‐parasitoid host specificity .........................................................................
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