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Boisea Rubrolineata (Barber) (Heteroptera: Rhopalidae)

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Boisea Rubrolineata (Barber) (Heteroptera: Rhopalidae) THE CHEMICAL ECOLOGY OF HOST FORAGING, AGGREGATION, AND PROPHYLACTIC MICROBIAL DEFENSE IN THE WESTERN BOXELDER BUG, BOISEA RUBROLINEATA (BARBER) (HETEROPTERA: RHOPALIDAE) by Joseph J. Schwarz B.A. (BioI. Major/Chern. Minor), Kean University, 2002 THESIS SUBMITTED IN FULFILLNIENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE In the Department ofBiological Sciences © Joseph J. Schwarz SIMON FRASER UNIVERSITY Summer 2008 All rights reserved. This work may not be reproduced in whole or in part, by photocopy or other means, without permission ofthe author. APPROVAL Name: Joseph Schwarz Degree: Master of Science Title of Thesis: The chemical ecology of host foraging, aggregation, and prophylactic microbial defense in the western boxelder bug, Boisea rubrolineata (Barber) (Heteroptera: Rhopalidae) Examining Committee: Chair: Dr. S. Bisgrove, Assistant Professor Dr. G. Gries, Professor, Senior Supervisor Department of Biological Sciences, S.F. U. Dr. B. Roitberg, Professor Department of Biological Sciences, S.F. U. Dr. A. Carroll, Research Scientist Pacific Forestry Centre, Natural Resources Canada Public Examiner 12 August 2008 Date Approved 11 SIMON FRASER UNIVERSITY LIBRARY Declaration of Partial Copyright Licence The author, whose copyright is declared on the title page of this work, has granted to Simon Fraser University the right to lend this thesis, project or extended essay to users of the Simon Fraser University Library, and to make partial or single copies only for such users or in response to a request from the library of any other university, or other educational institution, on its own behalf or for one of its users. The author has further granted permission to Simon Fraser University to keep or make a digital copy for use in its circulating collection (currently available to the public at the "Institutional Repository" link of the SFU Library website <www.lib.sfu.ca> at: <http://ir.lib.sfu.ca/handle/1892/112>) and, without changing the content, to translate the thesis/project or extended essays, if technically possible, to any medium or format for the purpose of preservation of the digital work. The author has further agreed that permission for multiple copying of this work for scholarly purposes may be granted by either the author or the Dean of Graduate Studies. It is understood that copying or publication of this work for financial gain shall not be allowed without the author's written permission. Permission for public performance, or limited permission for private scholarly use, of any multimedia materials forming part of this work, may have been granted by the author. This information may be found on the separately catalogued multimedia material and in the signed Partial Copyright Licence. While licensing SFU to permit the above uses, the author retains copyright in the thesis, project or extended essays, includill9 the right to change the work for subsequent purposes, including editing and publishing the work in whole or in part, and licensing other parties, as the author may desire. The original Partial Copyright Licence attesting to these terms, and signed by this author, may be found in the original bound copy of this work, retained in the Simon Fraser University Archive. Simon Fraser University Library Burnaby, BC, Canada Revised: Fall 2007 ABSTRACT The boxelder bug (BEB), Boisea rubrolineata (Heteroptera: Rhopalidae), is a specialist herbivore ofboxelder trees, Acer negundo. BEBs form spectacular aggregations on (i) pistillate A. negundo when seeds are maturing, (ii) in and around shelters in fall and winter, and (iii) in response to warm sunlight. When sunbathing, BEBs release from their posterior dorsal abdominal gland an odorous blend ofmonoterpenes with heretofore unknown biological function. We reveal that (1) BEBs exploit semiochemicals (phenylacetonitrile, 2-phenethyl acetate) from host trees to locate them during foraging and colonization, (2) aggregation and sexual communication ofBEBs are mediated by a complex pheromone system, and (3) BEBs in warm sunlight, but not in shade, exude and spread copious amounts ofmonoterpenes onto their cuticle. These monoterpenes do not serve as a pheromone, but rather a means ofsanitation that interferes with spore germination and growth ofthe pathogenic fungus Beauvaria bassiana. Keywords: Boxelder bugs, Boisea rubrolineata, Heteroptera, Rhopalidae, Serinethinae, boxelder trees, Acer negundo, semiochemicals, phenylacetonitrile, host foraging, plant defense, seed predation, aposematism, feces, aggregation pheromone, ventral abdominal gland, sex-pheromone, 2-phenylethanol, posterior dorsal abdominal gland, monoterpenes, microbial defense, fungal pathogen, Beauveria bassiana, sunbathing, secretion-grooming iii DEDICATIONS PJ::'tJf!/ molil/ji~, tf/iI,(J I(/Ilffill me lopllotf/ 11;(/ ilea!}'/; (//I/rllo '}'ea(/~~ tJ~!/ r!re(/l/Jl6. .. JIoIJ~!I,(JII'. PJ::'tJ!fyf7Ii1-ey, llJiI,(J6e #11/rl~niJlff;lO(,1I6erlme 01// Ih,e hI/Pillute work! (l'II(/llll}'e,.Jl//iI/~!lme Wilhl (/' 6e1l6e !!,I6i!(/I//rltf/ollrle~. iv 6t6wIottc!ed11' tk endw/7l~beatIfY r/tIw iiMJzinent daum/, J O'Inbmee lIJid 6an1f! tk dta!Ien~tItat cuttait t!l~ nett? cia;; - Joseph J. Schwarz v ACKNOWLEDGEMENTS I sincerely thank Ian Wilson (Urban Forest manager, Kelowna, BC, Canada) and homeowners in Kelowna, Westbank, and Princeton, BC, Canada, for access to their property for insect and host-plant collections; Geoffrey G.B. Scudder for confirming taxonomic identity ofthe boxelder bug, Boisea rubrolineata (Barber); Zamir Punja, Neil Vickers, Kirk Hillier, and Mark Goettel for use of lab space and equipment, field assistance; and valuable intellectual discussions; Bob Birch for graphical illustrations, Bruce Harwood for glasswork, and Ian Bercovitz and Carl Schwarz for ·statistical consultation. I especially thank my supervisor, Gerhard Gries, for his warm-heartedness, enthusiasm, guidance, and support throughout my research. Gerhard, you surely kept the color ofmy words within the lines. I thank supervisory committee member Bernhard Roitberg for support and insightful and constructive comments; Allan L. Carroll for accepting the position of Public Examiner; Regine Gries for much technical support and assistance, and delightful conversations-you are a great inspiration; Grigori Khaskin for chemical syntheses, friendship and conversations; Eberhard Kiehlmann for proofreading of manuscripts; fellow students in the Gries-lab, Roitberg-Iab, Punja-Iab, Plettner-Iab, Plant-lab, and Nicholson-lab for their friendship, discussions and encouragement. This research was supported by SFU Graduate Fellowships and by a Natural Sciences and Engineering Research Council ofCanada (NSERC) - Industrial Research vi Chair to Gerhard Gries with Pherotech International Inc., SC Johnson Canada, and Global Forest Science (GF-18-2007-226; GF-18-2007-227) as industrial sponsors. vii TABLE OF CONTENTS Approval ii Abstract iii Dedications iv Quotation v Acknowledgements vi Table of Contents viii List of Figures x List of Tables xiv I Introduction 1 1.1 Hemiptera 1 1.2 Scentless plant bugs '" 2 1.3 Distribution and morphology ofB. rubrolineata .4 1.4 Exocrine system ofB. rubrolineata 6 1.5 Life history ofB. rubrolineata 7 1.6 Characteristics ofboxelder maple, Acer negundo 7 1.7 Research opportunities and objectives 9 1.8 References 11 2 Phenology of semiochemical-mediated host foraging by the western boxelder bug, Boisea rubrolineata, an aposematic seed predator 16 2.1 Abstract. 16 2.2 Introduction 17 2.3 Methods and Materials 21 2.3.1 Collection and Maintenance ofExperimental Insects 21 2.3.2 Collection ofA. negundo volatiles 22 2.3.3 Analyses ofExtracts .23 2.3.4 General Bioassay Procedures 24 2.3.5 Specific Experiments (Table 2.2) 25 2.3.6 Statistical Analyses .26 2.4 Results '" 27 2.5 Discussion 29 2.6 References 38 viii 3 2-Phenylethanol: context-specific aggregation or sex pheromone of the western boxelder bug, Boisea rubrolineata, (Heteroptera: Rhopalidae) an aposematic seed predator 74 3.1 Abstract 74 3.2 Introduction 75 3.3 Methods and Materials 78 3.3.1 Collection and Maintenance ofExperimental Insects 78 3.3.2 Collection ofB. rubrolineata feces volatiles 78 3.3.3 Collection ofHeadspace Volatiles from Adults 79 3.3.4 Extracts ofthe Ventral Abdominal Gland (VAG) 80 3.3.5 Design ofY-tube Olfactometer Experiments 80 3.3.6 Design ofStill-air Olfactometer Experiments 81 3.3.7 Specific Experiments 82 3.3.8 Analyses ofExtracts 83 3.3.9 Statistical Analyses 83 3.4 Results 84 3.5 Discussion 86 3.6 References 97 4 Do boxelder bugs sunbath for sanitation? 126 4.1 Abstract. 126 4.2 Introduction 126 4.3 Materials and Methods 130 4.3.1 Collection and maintenance ofexperimental insects 130 4.3.2 Excision and extraction ofposterior dorsal abdominal glands (PDAG) from bugs exposed to sun or shade 130 4.3.3 Bodywashes of bugs exposed to sun or shade 131 4.3.4 Collection ofhead-space volatiles 13 2 4.3.5 Analyses ofextracts 132 4.3.6 Behavioral experiments 133 4.3.7 Specific experiments 13 5 4.3.8 Ability ofmonoterpenes to inhibit germination ofB. bassiana conidia spores 135 4.3.9 Ability ofmonoterpenes to suppress growth ofB. bassiana 136 4.3.10 Statistical Analyses 13 7 4.4 Results 13 7 4.4.1 Analyses ofExtracts 137 4.4.2 V-tube and still-air olfactometer experiments 138 4.4.3 Effect ofmonoterpenes on B. bassiana 13 8 4.5 Discussion 139 4.6 References 144 5 Conclusional summary 170 ix LIST OF FIGURES Figure 2.1 Graphical illustration depicting aspects ofthe seasonal phenology ofboxelder trees, Acer negundo, and boxelder bugs (BEBs),
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