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Host Location and Selection Cue in Phytophagous Insects?

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Polarized light - host location and selection cue in phytophagous insects? by Adam James Blake M.Sc. (Ecology), University of Alberta, 2010 B.Sc. (ENCS), University of Alberta, 2006 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biological Sciences Faculty of Science © Adam James Blake 2020 SIMON FRASER UNIVERSITY Fall 2020 Copyright in this work rests with the author. Please ensure that any reproduction or re-use is done in accordance with the relevant national copyright legislation. Declaration of Committee Name: Adam Blake Degree: Doctor of Philosophy Polarized light - host location and selection cue Title: in phytophagous insects? Committee: Chair: Ronald Ydenberg Professor, Biological Sciences Gerhard Gries Supervisor Professor, Biological Sciences Iñigo Novales Flamarique Committee Member Professor, Biological Sciences Almut Kelber Committee Member Professor, Biology Lund University Leithen M'Gonigle Examiner Assistant Professor, Biological Sciences Martin How External Examiner Royal Society University Research Fellow with Proleptic Lectureship School of Biological Sciences University of Bristol ii Abstract Insect herbivores exploit plant cues to discern host and non-host plants. Studies of visual plant cues have focused on color despite the inherent polarization sensitivity of insect photoreceptors and the information carried by polarization of foliar reflectance, most notably the degree of linear polarization (DoLP; 0-100%). The DoLP of foliar reflection was hypothesized to be a host plant cue for insects but was never experimentally tested. I investigated the use of these polarization cues by the cabbage white butterfly, Pieris rapae (Pieridae). This butterfly has a complex visual system with several different polarization-sensitive photoreceptors, as characterized with electrophysiology and histology. I applied photo polarimetry revealing large differences in the DoLP of leaf-reflected light among plant species generally and between host and non-host plants of P. rapae specifically. As polarized light cues are directionally dependent, I also tested, and modelled, the effect of approach trajectory on the polarization of plant-reflected light and the resulting attractiveness to P. rapae, showing that certain approach trajectories are optimal for discriminating among plants based on these cues. I then demonstrated that P. rapae exploit the DoLP of foliar reflections to discriminate among plants. In experiments with paired digital plant images that allowed for independent control of polarization, color and intensity, P. rapae females preferred images of the host plant cabbage with a low DoLP (31%) to images of the non-host plant potato with a high DoLP (50%). These results indicated that the DoLP had a greater effect on foraging decisions than the differential color, intensity or shape of the two plant images. To investigate potential neurological mechanisms, I designed behavioral bioassays presenting choices between images that differed in color, intensity and/or DoLP. The combined results of these bioassays suggest that several photoreceptor classes are involved and that P. rapae females process and interpret polarization reflections in a way different from that described for other polarization-sensitive taxa. My work has focused on P. rapae and its host plants but there is every reason to believe that the DoLP of foliar reflection is an essential plant cue that may commonly be exploited by foraging insect herbivores Keywords: Behaviour; Insect Vision; Polarization Vision; Photo Polarimetry; Degree of Linear Polarization; Pieris rapae iii Acknowledgements I have to thank Dr. Gerhard Gries for taking me on as a student and giving me the opportunity to pursue a “career that will keep [me] entertained all [my] life”. Your enthusiasm for my project findings and for science in general was unwavering even when my own enthusiasm faltered. I would like to thank Drs. Iñigo Novales Flamarique and Almut Kelber for having agreed to serve on my advisory committee and for having provided expert advice and constructive feedback throughout my study. I thank Dr. Martin J. How and Dr. Leithen M'Gonigle for having agreed to serve as the External Examiner and the Internal Examiner, respectively, of my thesis defense. I also thank Dr. Ronald Ydenberg for chairing the defense. I must thank Dr. Kentaro Arikawa (Graduate University for Advanced Studies, SOKENDAI) for hosting me in his laboratory and for being so generous with his time and expertise. The brief time I spent in his lab was invaluable for my PhD research and my growth as a vision scientist. I must thank Atsuko Matsushita for assistance and instruction with microscopy and histology, Dr. Doekele G. Stavenga for his immense expertise on the optics of butterfly eyes, and Dr. Primož Pirih for his tireless instruction on epi-illumination light microscopy. I gratefully acknowledge financial support from Contech, Scotts Canada, BASF Canada, the Natural Sciences and Engineering Research Council of Canada, and Simon Fraser University. Without this support none of this work would have been possible. My research has benefited greatly from the hard work, dedication, and intellectual contributions of my coauthors and former research assistants Samuel Couture, Dr. Matthew C. Go, Gina S. Hahn, Hayley Grey, Shelby A. Kwok, and Deby McIntosh. You are the most talented group of research assistants I’ve had the pleasure of working with, and I am sure you will have great success in whatever you choose to undertake. I must recognize the Gries lab. I can think of no better environment to learn, hone my skills, and broaden my understanding. The comradery, conversation, and collaborations have made me a far better scientist. Regine Gries is truly the linchpin of iv this group; it is her hard work that paves the way for all of our success. I thank Drs. Sean McCann, Catherine Scott and Bekka Brodie, you at times set an intimidatingly high bar of success for me when I first entered the lab. I would also specifically like to thank current and former lab-mates Sebastian Ibarra, Dr. Daniel Peach, Nathan Derstine, Josh Pol, Asim Renyard, Elton Ko, Yonathan Uriel, and Jaime Chalissery. I cherish the times we’ve spent together even those spent in “Glorious” distraction. I thank my friend, colleague, coauthor and bubble-mate Dan Peach for his advice, kindness and for also “being such an all-around fantastic person”. The passion for science you inspire in others is truly admirable. The friendship of you and Grace have been a boon in these “interesting” times. I must thank my parents Lorrie and Tony, and my brother Brendan. I would not be on the path I find myself on today without you. Lastly, I must thank my wonderful wife Sara. Without her love, understanding, support, and (sometimes not so) gentle encouragement, I would not have reached the end of this PhD. She was always a willing sounding board, and has assisted with more lab and field work than I can ever truly repay. I count myself truly lucky to share this and all my accomplishments with her. v Table of Contents Declaration of Committee .................................................................................................. ii Abstract ............................................................................................................................. iii Acknowledgements ........................................................................................................... iv Table of Contents .............................................................................................................. vi List of Tables ..................................................................................................................... ix List of Figures ................................................................................................................... x List of Acronyms ........................................................................................................... xviii Chapter 1. Introduction ............................................................................................... 1 1.1. Polarized Light ....................................................................................................... 1 1.1.1. Physics of Polarized Light ............................................................................... 1 1.1.2. Measuring Polarized Light .............................................................................. 2 1.1.3. Sources of Polarized Light .............................................................................. 4 1.1.4. Polarized Reflections from Plant Surfaces ...................................................... 5 1.2. Arthropod Photoreceptors ...................................................................................... 6 1.2.1. Rhabdomeric Photoreceptors ......................................................................... 6 1.2.2. Dorsal Rim Area .............................................................................................. 7 1.2.3. Photoreceptor Twist ........................................................................................ 8 1.2.4. Ventral Polarization Vision .............................................................................. 8 1.2.5. Perception of Polarized Light ........................................................................ 10 1.3. Polarization-Related Behaviors ...........................................................................
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