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The Magnetic Sense of Honey Bees - Analyses of Underlying Mechanisms and Potential Function

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The Magnetic Sense of Honey Bees - Analyses of Underlying Mechanisms and Potential Function The magnetic sense of honey bees - analyses of underlying mechanisms and potential function by Veronika Lambinet Diplom Biologist, Johann Wolfgang Goethe University, 2010 Biological Technical Assistant, Naturwissenschaftliches Technikum Dr. Künkele, 2004 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biological Sciences Faculty of Science © Veronika Lambinet SIMON FRASER UNIVERSITY Fall 2017 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. Approval Name: Veronika Lambinet Degree: Doctor of Philosophy (Biological Sciences) Title: The magnetic sense of honey bees – analyses of underlying mechanisms and potential function Examining Committee: Chair: Dr. Julian Guttmann Professor Dr. Gerhard Gries Senior Supervisor Professor Dr. Michaele Hayden Co-Supervisor Professor Dr. Gordon Rintoul Supervisor Professor Dr. Staffan Lindgren Internal Examiner Professor Emeritus Department of Ecosystem Science and Management University of Northern British Columbia Dr. Joseph Kirschvink External Examiner Professor Geological and Planetary Sciences California Institute of Technology Date Defended/Approved: November 10, 2017 ii Abstract I studied a potential function and underlying mechanism(s) of the magnetic sense in honey bees, Apis mellifera. A waggle-dancing bee informs hive mates about a food source. Directional information pointing to the food source relative to the sun's azimuth is encoded in the angle between the straight segment of her waggle dance and a reference line such as gravity or the local geomagnetic field (LGMF). Neither cancelling the LGMF nor shifting its declination affected the recruitment success of waggle-dancing bees, implicating gravity as the reference line for the dance alignment. To study the underlying mechanism(s) of the bees’ magnetic sense, I analyzed lyophilized and pelletized bee tagmata by a Superconducting Quantum Interference Device. A distinct hysteresis loop for the abdomen but not for the thorax or the head of bees indicated the presence of magnetite in the abdomen. Magnetic remanence of abdomen pellets produced from bees that I did, or did not, expose to an NdFeB magnet while alive differed, indicating that magnet-exposure altered the magnetization of this magnetite in live bees. Following exposure of live bees to the same magnet, magnetized bees, unlike sham-treated control bees, failed to sense the presence of a magnetic anomaly, demonstrating a functional connection between magnetite in the abdomen and the magnetoreceptor, and temporary or permanent disablement of the receptor through magnet-exposure. To test whether bees sense the polarity of a magnetic field, I trained bees to associate a magnetic anomaly with a sugar water reward. I then presented trained bees with a sugar water reward in two separate watch glasses, placing one reward in the center of the anomaly that I either kept the same as during bee training (control experiment) or that I altered by reversing its polarity (treatment experiment). That bees continued to recognize the magnetic anomaly when its polarity was kept unaltered, but failed to recognize it when its polarity was reversed, indicates that bees have a polarity-sensitive magnetoreceptor. To increase the detectability of magnetite in bee tissues, I lyophilized samples to reduce water content, maximized the signal amplitude by pelletizing samples, and accounted for sample dimensions in data analyses. iii Keywords: Honey bees; Communication; Magnetoreception; Magnetite-based magnetoreception; Behavioural two-choice experiments; SQUID measurements iv Dedication To my parents: Fritz and Gitta Lambinet v Acknowledgements My biggest thank you goes out to my supervisor Dr. Gerhard Gries. He has supported me every step of the way during my graduate studies at SFU. He has never blocked any of my (sometimes crazy) research ideas (e.g., the waggle dance machine or the disco dome) but instead has always encouraged and financially supported my research. Also, he and his wife, Regine Gries, have always been kind, helpful and understanding when life wasn’t easy. Thank you both for all you did for me! I also want to sincerely thank my co-supervisor Dr. Mike Hayden who has made significant contributions throughout my PhD research. I was deeply impressed by his abilities to joggle numbers and abstract functions in his mind and by his continued patience even after I had asked the same question for the 10th time. I really loved working with you, Mike! Because of your help my research has proceeded as far as it did. Thank you for all your time, expertise and effort you have put into my research! I want to thank my committee member Dr. Gordon Rintoul who provided helpful input during committee meetings. Thank you, Gordon, for your patience, good vibes, and insights! Furthermore, I would like to thank Dr. Joseph Kirschvink and Dr. Staffan Lindgren for having kindly agreed to serve as the External Examiner and the Internal Examiner, respectively, for my thesis defense. I would also like to thank Dr. Julian Guttman for having kindly agreed to chair the defense. I further want to thank all my great research assistants: Stephen Yu, David Breault, Marco Bieri, Katharina Reigl, Brian Andrade, Chloe Reid, Surath Gomis and Hannah Crisp. I appreciated our great working relationships and I cherish your friendship. Thank you friends! I would like to extend my gratitude to Vancouverites and farmers in both Sicamous and Lillooet that accommodated me and my research experiments on their land. Especially, I thank Lisa and Michael for access to their backyard in Vancouver; Sam Quinlan and Tim Hazard (HooH Hops Inc.) in Lillooet; my neighbors Hal and Kathy Stathers, Allyson Mcquee and Elijah Michel for having been friends and for having vi supported me on my journey; Tristan Banwell and Aubyn Banwell (Spray Creek Ranch) for hands-on help with my research, great work conditions and for having been good friends; Eckhart Zeidler and Deanne Zeidler (Texas Creek Ranch) for amazing work conditions and their friendship. For introducing me to the subject of magnetoreception in animals, I want to thank my former mentors Dr. Roswitha Wiltschko and Dr. Wolfgang Wiltschko. I am grateful that you took me under your wings and that you were always approachable to chat about my project when I came home for Christmas. Further I want to thank Werner Gysi and Bob Meredith for introducing me to honey bees and for help with my work. Your enthusiasm for bees inspired my interest in studying these amazing little creatures that I deeply fell in love with. I also want to thank all current and past members of the Gries-lab. You all have made my journey very interesting not least because of the diverse projects you have been working on. I appreciate that I was able to learn in a “multimodal” research environment inspired by your fun characters. Thank you! And of course, I want to thank my family and friends; my mother Gitta and my father Fritz, who always have taken great interest in my education, have always believed in me, and have never given up on me. You guys have been the best parents to me I could have wished for. I love you! Furthermore, I want to thank my partner Rob Davis and my dog Gixlie who became my family here in Canada. You play the biggest role in my life, and every day I am excited to come home to you. Thanks for all your support! Thank you also to Angela und Bjorn Sermersheim, Linus and Moritz Sermersheim, my grandmothers and grandfathers (Hilde und Franz Lambinet, Marianne und Kurt Schroeder), Valli und Heinz Hilscher-Will and family. I am happy you all are and were in my life. vii Table of Contents Approval ............................................................................................................................ ii Abstract .............................................................................................................................iii Dedication ......................................................................................................................... v Acknowledgements .......................................................................................................... vi Table of Contents ............................................................................................................ viii List of Tables .................................................................................................................... xi List of Figures ...................................................................................................................xii List of Acronyms ............................................................................................................. xvii Glossary ........................................................................................................................ xviii Chapter 1. Introduction ................................................................................................ 1 Background on magnetic fields and magnetic materials ......................................... 2 1.1.1. Properties of the earth’s magnetic field ........................................................... 2 1.1.2. Magnetic nanoparticles ................................................................................... 3 Paramagnetic, superparamagnetic and ferromagnetic particles ................................ 3 Diamagnetism ...........................................................................................................
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