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Community Ecology and Sirex Noctilio: Interactions with Microbial Symbionts and Native Insects

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Community Ecology and Sirex Noctilio: Interactions with Microbial Symbionts and Native Insects ABSTRACT Title of Document: Community Ecology and Sirex noctilio: Interactions with Microbial Symbionts and Native Insects Brian Matthew Thompson, Doctor of Philosophy, 2013 Directed By: Assistant Professor, Daniel S. Gruner, Department of Entomology Sirex noctilio is an invasive woodwasp with a global distribution that feeds on the sapwood of pine trees. Wood-feeding in the basal Hymenoptera (sawflies) arose out of sequential adaptations to feeding on nutrient poor and digestively refractive internal plant organs (xylem). Symbiotic association with White-rot fungi are thought to aid overcoming nutritional and digestive barriers, including exceedingly low nitrogen (N) and refractory lignocellulosic polymers. In this dissertation I evaluate wood-feeding relative to nutrition, symbiosis and biotic resistance to invasion of exotic North American habitats in Sirex noctilio [Hymenoptera: Siricidae]. I evaluated nutrient relations within fungal mutualism using: 1) functional morphological analysis of insect feeding, 2) sterol molecules to determine diet sources and 3) metagenomic and isotopic analyses for discovery of novel microbial associates and their associated nutrient pathways. Nutritional constraints of wood feeding are potentially compounded by the presence of diverse fungal and insect communities as they divide the tree resource. I examined the role biotic resistance to Sirex and its fungal mutualist, Amylostereum, in North America using field and laboratory experiments. Morphological evidence supported a role for Amylostereum in external digestion of wood. Observational evidence confirmed Sirex larvae did not ingest wood biomass but preferentially extracted liquid substances via specialized structures of mandibles. Sterol analysis indicated plant compounds as the primary constituent of the diet, while metagenomic analysis of bacteria and their metabolic pathways showed a bacterial microbiome adapted to short chain plant polymers, starch and sugar metabolism. Stable isotopes suggested an additional symbiotic association with nitrogen fixing bacteria enriched the nitrogen deficient food substrate. These studies point toward herbivory with microbial supplementation of nutrients as a tri-partite relationship, pending conclusive identification of the bacterial symbiont for Sirex. Specific constraints of wood feeding by the Sirex symbiotic complex were antagonized by intraguild predation and fungal competition in North America. Competition interfered with Amylostereum, while intraguild predation accounted for an additional 15% mortality of larval populations. This research describes the evolutionary role of microbial symbionts in wood-feeding in the Hymenoptera and the internal and external constraints to foraging this ubiquitous, yet nutrient poor food resource. COMMUNITY ECOLOGY AND SIREX NOCTILIO: INTERACTIONS WITH MICROBIAL SYMBIONTS AND NATIVE INSECTS By Brian Matthew Thompson Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2013 Advisory Committee: Assistant Professor Daniel S. Gruner, Chair Assistant Professor Priscila Chaverri Professor Michael Raupp Assistant Research Scientist Dennis vanEngelsdorp Professor Irwin N. Forseth Jr. © Copyright by Brian Matthew Thompson 2013 Dedication To Abby, for a thousand smiles ii Acknowledgements I would like to thank my advisor, Dan Gruner, for his relentless editing and an attitude that ‘goes to 11!’. A special thanks goes to my loving wife, Abby Thompson, for lending patience, wisdom and inspiration. I thank Miriam and Jim Dunham for opening their ‘forest’ to a budding entomologist. Were it not for their kindness to a complete stranger I may never have completed three field seasons in Pennsylvania. Editing and discussion in early stages are credited to GRUBOSA (Pedro Barbosa, Cora Johnston, Mayda Nathan, Alex Forde, Erin Wilson and many others) & Washington Plant Interaction Group. I thank Jake Bodart, James Tauber, Susan and Brice Keown, George Reahl, Elmer Haapala, Nathan Judd, Sarah Dewitt, Kiesha Gray & Alan Leslie for ‘logging’ and carrying my heavy data points over three years of collections. Funding credit goes to the United States Forest Service, Sigma Xi, The University of Maryland Gahan Fellowship, University of Maryland Summer Research Fellowship and The Washington Explorers Club. Thanks to Pennsylvania DCNR Dept. of State Parks and USDA-APHIS for permitting and sample collection. Many thanks to my graduate committee Mike Raupp, Dennis vanEngelsdorp, Priscila Chaverri, and Irwin Forseth for much needed constructive criticism and an attention to detail that I have come to depend on. I thank Spencer Behmer, Robert Grebenok Aaron Adams, Matt Ayres and Garret Suen, Jeff Shultz, and Raymond St. Leger for helpful revisions and comments and hypothesis generation. Special thanks to Joanne Lewis, Jo Ann Smith, Greg Hess, Bill Kastereles and Avis Koeman for programmatic support without which I could not have navigated the ‘system’. Lastly, I would like to thank my friends and family for their continued and much appreciated support. iii Table of Contents Dedication ..................................................................................................................... ii Acknowledgements ...................................................................................................... iii Table of Contents ......................................................................................................... iv List of Tables ............................................................................................................. viii List of Figures .............................................................................................................. ix List of Equations .......................................................................................................... xi Chapter 1: Introduction and Project Summary ............................................................. 1 Chapter 2: Behavioral and morphological adaptations reveal insights into xylophagy and obligate symbiosis in the European woodwasp, Sirex noctilio .............................. 8 2.1 Abstract ............................................................................................................... 8 2.2 Introduction ......................................................................................................... 9 2.3 Methods............................................................................................................. 14 2.3.1 Sample Collection ...................................................................................... 14 2.3.2 Foraging Spatial Dispersion ....................................................................... 15 2.3.3 Foraging Sirex & Internal Anatomy .......................................................... 16 2.3.4 Statistical Analysis ..................................................................................... 17 2.4 Results ............................................................................................................... 18 2.4.1 Foraging Spatial Dispersion ....................................................................... 18 2.4.2 Foraging Sirex & Internal Anatomy .......................................................... 19 2.5 Discussion ......................................................................................................... 20 2.6 Figures & Tables ............................................................................................... 27 2.6.1 Tables ......................................................................................................... 27 iv 2.6.2 Figures........................................................................................................ 28 Chapter 3: Microbial symbionts shape the sterol profile of the xylem profile of the xylem-feeding woodwasp, Sirex noctilio .................................................................... 35 3.1 Abstract ............................................................................................................. 35 3.2 Introduction ....................................................................................................... 36 3.3 Methods............................................................................................................. 40 3.3.1 Study System ............................................................................................. 40 3.3.2 Sample Collection ...................................................................................... 41 3.3.3 Fungal Isolation ......................................................................................... 42 3.3.4 Tracking Fungal Growth ............................................................................ 44 3.3.5 Sterol Analysis ........................................................................................... 45 3.3.6 Statistical Analysis ..................................................................................... 47 3.4 Results ............................................................................................................... 49 3.4.1 Sirex Sterols ............................................................................................... 49 3.4.2 Sterol in Food Resources ........................................................................... 51 3.5 Discussion ........................................................................................................
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