Exploitation of Electromagnetic Radiation as a Foraging Cue by Conophagous Insects by Tracy Daniela Zahradnik M.Sc. (Zoology), University of Guelph, 2005 B.Sc. (Zoology), University of Guelph, 2003 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biological Sciences Faculty of Science Tracy Daniela Zahradnik 2012 SIMON FRASER UNIVERSITY Summer 2012 All rights reserved. However, in accordance with the Copyright Act of Canada, this work may be reproduced, without authorization, under the conditions for “Fair Dealing.” Therefore, limited reproduction of this work for the purposes of private study, research, criticism, review and news reporting is likely to be in accordance with the law, particularly if cited appropriately. Approval Name: Tracy Daniela Zahradnik Degree: Doctor of Philosophy (Biology) Title of Thesis: Exploitation of electromagnetic radiation as a foraging cue by conophagous insects Examining Committee: Chair: Dr. E. Elle, Associate Professor Dr. G. Gries, Professor, Senior Supervisor Department of Biological Sciences, S.F.U. Dr. F. Breden, Professor, Supervisor Department of Biological Sciences, S.F.U. Dr. W. Strong, Research Scientist, Supervisor B.C. Ministry of Forests, Lands , and Natural Resource Operations Dr. I. Novales Flamarique, Professor Department of Biological Sciences, S.F.U. Internal Examiner Dr. P. Kevan, Professor Emeritus School of Environmental Sciences, University of Guelph External Examiner Date Defended/Approved: May 9, 2012 ii Partial Copyright Licence iii Abstract Many insects exploit sections of the electromagnetic spectrum as foraging or attraction cues, detecting wavelengths in the ultraviolet (UV; ~ 300–400 nm), human visible (400– 750 nm) and infrared (> 750 nm) range. Two distinct types of receptors are involved. Compound eyes in the head detect UV and human visible light, and IR receptors on the thorax or abdomen detect radiant IR which contrasts against the background and is therefore dectable. I investigated the potential use of electromagnetic foraging cues in three members of the conophagous insect guild: the diurnal Western conifer seed bug, Leptoglossus occidentalis Heidermann (Hemiptera: Coreidae), the nocturnal fir coneworm moth, Dioryctria abietivorella Groté (Lepidoptera: Pyralidae), and the diurnal Douglas-fir cone gall midge, Contarinia oregonensis Foote (Diptera: Cecidomyiidae). In electrophysiological recordings, two-choice laboratory bioassays, and field trapping experiments, I tested the hypotheses that during (cone) foraging C. oregonensis, D. abietivorella and L. occidentalis (1) rely on IR receptors that receive and respond to cone-derived radiant IR, (2) receive and respond to cone or plant-derived colour cues, and (3) integrate radiant IR and insect visible light cues. My data support these hypotheses, at least in part. Male and female L. occidentalis were more attracted to radiant IR from heat sources within but not outside the natural cone temperature range. Male and female D. abietivorella have IR receptors on their ventral prothorax which help them detect and discriminate between IR stimuli. Both D. abietivorella and C. oregonensis are attracted to warm objects with IR signatures resembling or corresponding to those of tree branches but not those of cones. No insects oriented towards cone-reflected light as a singular foraging cue, but mated female L. occidentalis preferred the complete light spectrum of conifer needles (their oviposition site) to a iv narrow bandwidth of visible light. Visible (blue) light combined with radiant IR from a 40 ºC heat source were synergistic in attracting female L. occidentalis, indicating that the central nervous system of L. occidentalis is capable of processing and integrating information from compound eyes and IR receptors. Such integration of visible stimuli and IR was previously known only in viperid snakes. Keywords: Leptoglossus occidentalis, Dioryctria abietivorella, Contarinia oregonensis, infrared (IR) receptor, compound eye, foraging cue v Quotation “A man who carries a cat by the tail learns something he can learn in no other way.” - Mark Twain vi Acknowledgements I thank Tamara Richards, Nicole Tunbridge, Caroline Whitehouse, Thomas Cowan, Robb Bennett, Stephen Takács, and Jim Corrigan for input, Stephanie Dumas for rearing Dioryctria abietivorella specimen, Bradley Sinclair for identification of Contarinia oregonensis specimen, James Drummond for taking ESEMs, and Peter Belton, Raymod Holland, and Pawel Kowalski for making customized equipment. I thank Patti Brown, Cathy Cook, Tim Crowder and Chris Walsh for access to field sites. I thank my assisants Allison Gamble, Anastasia Kuzman, Audrie Labrie, Laurie Lin, Keiko Nabetani, and Michelle Tsang for assistance in the field and laboratory. I think the External Examiner Peter Kevan, Internal Examiner Inigo Novales Flamarique and Chair Elizabeth Elle who attended my defense. I thank my supervisory committee, Gerhard Gries, Felix Breden, and Ward Strong for thesis revisions. Funding was provided by the Forestry Genetics Council of British Columbia, British Columbia Ministry of Forests and Range, Canadian Forestry Products, and by a Natural Sciences and Engineering Research Council of Canada (NSERC) – Industrial Research Chair to G.G., with Contech Enterprises Inc. and Global Forest Science as sponsors. vii Table of Contents Approval .......................................................................................................................... ii Partial Copyright Licence ............................................................................................... iii Abstract .......................................................................................................................... iv Quotation ....................................................................................................................... vi Acknowledgements ....................................................................................................... vii Table of Contents .......................................................................................................... viii List of Tables ................................................................................................................. xii List of Figures................................................................................................................ xiii 1. Introduction .......................................................................................................... 1 1.1. Electromagnetic spectrum ...................................................................................... 1 1.2. Colour vision and response to specific wavelengths ............................................... 2 1.3. UV vision ................................................................................................................ 4 1.4. IR receptors and IR detection ................................................................................. 5 1.5. Combinations of visible light and radiant IR ............................................................ 7 1.6. Conophagous insects in seed orchards .................................................................. 8 1.7. Research species ................................................................................................... 8 1.7.1. Leptoglossus occidentalis ........................................................................... 8 1.7.2. Dioryctria abietivorella ................................................................................. 9 1.7.3. Contarinia oregonensis ............................................................................. 10 1.8. Hypotheses and chapters ..................................................................................... 10 1.9. Literature Cited ..................................................................................................... 15 2. Douglas-fir cone gall midges respond to shape and infrared wavelength attributes characteristic of host tree branches ............................ 21 2.1. Abstract ................................................................................................................ 21 2.2. Introduction .......................................................................................................... 23 2.3. Materials and methods ......................................................................................... 25 2.3.1. Surveys 1-3: Effect of cone colour, cone orientation, and tree components (cone, foliage, branch) on apparent temperatures ................. 25 2.3.2. Survey 4: Effect of cone colour on oviposition by female C. orengonensis ............................................................................................ 27 2.3.3. General design of trapping experiments .................................................... 27 2.3.4. Experiments 1-4: Effect of trap colour, temperature, and shape on attraction of C. oregonensis ...................................................................... 28 2.4. Results ................................................................................................................. 30 2.5. Discussion ............................................................................................................ 31 2.6. References ........................................................................................................... 34 2.7. Figure captions ....................................................................................................