Interactions Between the Cereal Aphid Pests Sitobion Avenae and Rhopalosiphum Padi and Their Fungal Natural Enemies

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Interactions Between the Cereal Aphid Pests Sitobion Avenae and Rhopalosiphum Padi and Their Fungal Natural Enemies Norwegian University of Life Sciences Faculty of Biosciences Department of Plant Sciences Philosophiae Doctor (PhD) Thesis 2019:70 Interactions between the cereal aphid pests Sitobion avenae and Rhopalosiphum padi and their fungal natural enemies Samspill mellom kornbladlus (Sitobion avenae), havrebladlus (Rhopalosiphum padi) og deres naturlige fiender i korn Stéphanie Saussure Interactions between the cereal aphid pests Sitobion avenae and Rhopalosiphum padi and their fungal natural enemies Samspill mellom kornbladlus (Sitobion avenae), havrebladlus (Rhopalosiphum padi) og deres naturlige fiender i korn Philosophiae Doctor (PhD) Thesis Stéphanie Saussure Norwegian University of Life Sciences Faculty of BioSciences Department of Plant Sciences Ås (2019) Thesis number 2019:70 ISSN 1894-6402 ISBN 978-82-575-1630-7 i PhD supervisors Assoc. Prof. Richard Meadow Norwegian University of Life Sciences (NMBU) Ås, Norway Research Prof. Ingeborg Klingen Norwegian Institute for Bioeconomy Research (NIBIO) Ås, Norway Dr. Anne-Grete Roer Hjelkrem Norwegian Institute for Bioeconomy Research (NIBIO) Ås, Norway Dr. Therese With Berge Norwegian Institute for Bioeconomy Research (NIBIO) Ås, Norway Evaluation committee Prof. Italo Delalibera, Jr. University of São Paulo (USP-ESALQ) Piracicaba, SP, Brazil Prof. Helen Elizabeth Roy, Centre for Ecology and Hydrology (NERC) Oxfordshire, United-Kingdom Assoc. Prof. Siv Fagertun Remberg Norwegian University of Life Sciences (NMBU) Ås, Norway ii À ma famille, iii i Acknowledgements A PhD is many things. It is an education, a work but mostly a human adventure. This work wouldn’t had been possible without the wonderful people I met and helped me in different ways making this thesis possible. This thesis is pluridisciplinary and I, therefore, met many people that I want to thank. First, I wish to thank my supervisors Richard Meadow, Ingeborg Klingen, Anne-Grete Roer Hjelkrem and Therese With Berge. Thank you for offering me the possibility to work with you and welcoming me in your team. I am grateful for your trust, guidance and support during these four challenging and interesting years. Secondly, I would like to thank my opponents Helen Elizabeth Roy and Italo Delalibera, Jr. for taking the time to read my work and accepting to be a part of my committee. Thank you to Siv Fagertun Remberg for being my committee administrator and organising the defence. I had the pleasure to work with several co-authors. First, I had the chance to create zombie aphids in silico with Niels Holst. Thank you for your support, guidance and teaching. Jørgen Eilenberg, Annette Bruun Jensen, and Ibtissem Ben Fekih, thank you for inviting me on a fruitful and nice collaboration, and for interesting discussions. Marie Louise Davey and Annette Folkedal Schjøll, thank you for offering a bit of help when I was in need; and then becoming significant and interesting partners. Finally, Karin Westrum, thank you for teaching me how to handle these divas of fungi and being supportive when obstacles occurred e.g. suddenly fungi decided to stop growing in vitro. (Why? This was supposed to be the easy part.) I am grateful to my skilled colleagues at NIBIO who always helped me with a smile, squeezed me into their tight schedule and offered me advice and answers to my (sometimes strange) questions. Thank you, Andrea, Monica and Toril. I have been energized by my most reliable allies and support, my friends, who were there to share the ups with me and give me perspective during the downs. Thank you Chloé, Christophe, Claire, Marta, Nicolai, Roger, Simeon, Simon. And many others who shared a gym course, a coffee or a train ride with me! Support from outside your work environment is essential too. Thanks to Charlotte, Stefaniya and Sylvain for being supportive around chocolate cakes or on Skype and debating with me on many topics. Finally, thanks to my old friends who have been by my side for many years already: Arnaud, Chloé, Jean-Noël, Sebastien. Enfin merci à ma famille pour leur soutien longue distance et pour m’avoir permis de développer et de garder l’envie d’apprendre : Merci à ma mère, mon père, ma frangine, mamie, papi, Josette et Jean-Claude. Stéphanie iv Table of Contents Abstract ............................................................................................................................................................... vii Sammendrag ....................................................................................................................................................... ix List of publications ........................................................................................................................................... xi Foreword ............................................................................................................................................................... 1 1. Agronomical and ecological context .................................................................................................. 2 1.1. Agroecosystems and plant protection ...................................................................................... 2 1.2. Integrated Pest Management and biological control .......................................................... 3 2. Aphids and entomopathogenic fungi in cereals: a case study ................................................. 4 2.1. Pest aphids in cereals ...................................................................................................................... 4 2.2. Entomopathogenic fungi infecting aphids .............................................................................. 8 3. Epizootiology and biological control of aphids in cereals ..................................................... 12 3.1. The specific case of one pest, one pathogen ........................................................................ 12 3.2. The case of several pest and pathogen species .................................................................. 16 4. Objectives .................................................................................................................................................. 18 5. Results and Discussion ........................................................................................................................ 21 5.1. Factors driving susceptibility and resistance in cereal aphids .................................... 21 5.2. Entomophthoromycotina overwinter with Rhopalosiphum padi ............................... 22 5.3. The disease triangle effect on disease expression of Pandora neoaphidis .............. 24 5.3.1. Variability within the host community ......................................................................... 24 5.3.2. Variability within the fungus population ..................................................................... 25 5.3.3. Variability of environmental conditions ...................................................................... 26 5.4. Modelling the population dynamics ....................................................................................... 27 6. Conclusion and perspectives for biological control ................................................................. 30 7. References ................................................................................................................................................ 34 Papers I-IV .......................................................................................................................................................... 42 Errata………………………………………………………………………………………………………………………147 v vi Abstract In agronomy, efficient plant protection strategies are required to reduce pest pressure and increase crop yield. Pesticide application has been the dominant method for plant protection for almost a century. However, the over-reliance on pesticides has several detrimental consequences. Therefore, alternative plant protection strategies have been developed and promoted to reduce pesticide use. An overall approach to using alternative strategies is Integrated Pest Management (IPM), defined as a sustainable approach to manage pests by combining eight principles (according to the EU regulation that Norway implemented in 2015) in a way that minimizes economic, environmental and health risks. These include the use of natural enemies and the manipulation of their trophic interactions with pests in order to protect the crop yield (i.e. biological control). In Europe, two main aphid species cause damage in cereals such as winter wheat: the English grain aphid Sitobion avenae and the bird cherry-oat aphid Rhopalosiphum padi. Both species have many natural enemies, among which are entomopathogenic fungi in the sub-phylum Entomophthoromycotina. In this fungal group, the most interesting species for biological control of aphids are Pandora neoaphidis and Entomophthora planchoniana. As for any host-pathogen interactions, three important groups of factors are important potential drivers for an epidemic development: host population, pathogen population and environment. Together they are called the disease triangle. The aim of this PhD thesis was to identify important drivers of the disease triangle influencing (1) the success of fungal infection of aphids in cereals and (2) the capacity of the fungus to spread in these aphid populations. In this thesis I first reviewed, the factors driving the aphid host susceptibility or resistance to fungal pathogens by considering the model system composed of S.
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