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Gravity Acts As an Environmental Cue for Oriented Movement in the Monarch Butterfly, Danaus Plexippus (Lepidoptera, Nymphalidae)

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Gravity Acts As an Environmental Cue for Oriented Movement in the Monarch Butterfly, Danaus Plexippus (Lepidoptera, Nymphalidae) Gravity Acts as an Environmental Cue for Oriented Movement in the Monarch Butterfly, Danaus plexippus (Lepidoptera, Nymphalidae) A thesis submitted to the Graduate School of the University of Cincinnati in partial fulfillment of the requirements for the degree of Master of Science in the Department of Biological Sciences of the College of Arts and Sciences by Mitchell J. Kendzel B. S. Biology, University of Cincinnati, May 2018 Committee Chair: Patrick A. Guerra, Ph.D. Committee Members: Stephen F. Matter, Ph.D., John E. Layne, Ph.D. July 2020 ABSTRACT Gravity is an especially important environmental cue on which to focus animal movement and sensory biology research, both because of its consistency through evolutionary time, and because it is an essential force for which all organisms must compensate for, whether they move on land or in the air. In this thesis, I used the monarch butterfly, Danaus plexippus (Lepidoptera, Nymphalidae) as a system to study how organisms move and orient their body using gravity as a cue for directionality. To do this, I developed two assays, one designed to study directed locomotion and the other designed to study orientation via righting behavior. By focusing on directed movements and righting behavior, I was able to define how monarchs respond to gravity and identify how other environmental cues (that can provide directional information) interact with gravity when eliciting a behavioral response. In my locomotion assay, monarchs displayed negative gravitaxis only, manifested by walking opposite the direction of the gravity vector (i.e., up), even in the absence of other cues that could convey directionality, or in the presence of cues that typically elicit their own directional response (e.g., light cues). The upwards movement of butterflies only occurred once the apparatus was 30° above the horizontal. When individuals were forced to have a body orientation opposite the direction of their negative gravitaxis response during trials, butterflies would quickly correct their body position to face upwards and they then resumed negative gravitaxis. Monarchs moved upwards more vigorously when gravity and light cues were in agreement. Using the righting response assay, I showed that monarchs orient upwards to achieve a head up position and can use gravity when it is the only cue available or the only cue that can be sensed for directionality. In subsequent experiments, I showed that light biased their gravity- ii based righting orientation. When presented with a lateral light stimulus, the final head up righting orientation of monarchs was deflected toward the light source. When light cues came from below, directly opposite of the preferred head up orientation of the butterflies, their righting response to a head up position was unaffected. The antennae were found to be important sensory organs for a proper righting response. When antennae were removed and light cues were present, monarchs did not perform the righting response, but instead directly oriented towards the light source. When antennae-less monarchs were tested in darkness, monarchs oriented and righted themselves toward their default upward direction, suggesting the presence of a secondary mechanism for sensing gravity. Finally, the magnetic field was also shown to affect the righting response as the head up position of monarchs was deflected equatorward, with this response related to the monarchs using the inclination angle of the presented artificial magnetic field. My study demonstrates that monarch butterflies can use environmental sensory cues from different modalities for orientation behavior. In particular, the orientation response driven by a specific cue can be modulated by the presence of cues from other sensory modalities. iii iv ACKNOWLEDGEMENTS I would like to start by thanking my advisor, Patrick Guerra, for his guidance and support during the 4 years of working with him at the University of Cincinnati. Because of that time, I have grown immensely in my ability to conduct research and built a solid skill base that has allowed me to continue my pursuit in academia. I am extremely thankful for your willingness to help me conduct research as an undergraduate and to make it possible to pursue graduate school. To my research committee John Layne and Stephen Matter, thank you for taking the time to meet with me and discuss my work. Being available to discuss and work with me, was integral in the completion of my thesis on schedule. The suggestions you both made helped center the rational for my work and strengthen my findings. To my fellow lab members Jered Nathan, Sam Stratton, and Adam Parlin, thank you for helping rear monarchs and discuss experimentations. Jered, we worked together for 4 years and during that time you helped me in innumerable situations to organize, rear, plan coursework, and prepare for deadlines. Thank you for your contributions in and outside the lab. Adam, your R skills are amazing and the reason I was able to prepare this much material in such a short amount of time. Thank you for your willingness to teach me these techniques and to help with my writing. Sam, thank you for helping me graph my circular based data. There are unfortunately not a lot of resources available to express circular data, so your help was vital to making my data presentable. Finally, I would like to thank my wife, Hannah Kendzel, whose continued support made this thesis possible. Thank you for helping and motivating me to work hard and push into new v and sometimes uncomfortable situations. I am truly blessed to have a partner who supports me as much as you do in my career. vi TABLE OF CONTENTS Abstract…………………………………………………………………………………………..ii Acknowledgments………………………………………………………………………………..v List of Tables and Figures…………………………………………………………………….viii Chapter 1: Monarch Butterflies, Danaus plexippus, (Lepidoptera, Nymphalidae) Use Gravity as a Directional Cue that can Supersede the Effects of Other Cues, for Oriented Upwards Movement…………………………………………………………………………………….…...1 Abstract……………………………………………………………………………………2 Introduction………………………………………………………………………………..3 Methods……………………………………………………………………………………5 Results……………………………………………………………………………………11 Discussion………………………………………………………………………………..14 References………………………………………………………………………………..21 Chapter 2: Multimodal Sensory Integration for Executing Oriented Movement in the Monarch Butterfly, Danaus plexippus (Lepidoptera, Nymphalidae)………………………………………33 Abstract………………………………………………………………………………..…34 Introduction………………………………………………………………………………35 Methods…………………………………………………………………………………..38 Results……………………………………………………………………………………45 Discussion………………………………………………………………………………..48 References………………………………………………………………………………..55 vii LIST OF TABLES AND FIGURES Chapter 1 Figure 1.1 General tube maze assay and corresponding light wavelengths used in each experiment………………………………………………………………………………………..27 Figure 1.2 Monarch butterflies respond to gravity with negative gravitaxis and not positive gravitaxis…………………………………………………………………………………………28 Figure 1.3 Monarchs display negative gravitaxis behavior starting at a 30° incline………….....29 Figure 1.4 Light affects gravitaxis response only when it comes from above the organism………………………………………………………………………………………….30 Table 1.1 Descriptive Statistics and summary of comparisons for Negative Gravitaxis, Positive Gravitaxis, and Role of Light experiments………………………………………………………31 Table 1.2 Pairwise comparisons for incline trials………………………………………………..32 Chapter 2 Figure 2.1 Rotation assay design to measure orientations on a vertical plane……..……………61 Figure 2.2 Orientation assay used to test the use of gravity and magnetic cues for righting behavior………………………………………………………………………………………..…62 Figure 2.3 Gravity cues on their own are sufficient for monarch butterfly righting responses in the vertical plane…………………………………………………………………………………63 Figure 2.4 Monarchs from Fall and Summer of 2018 display identical righting responses……..64 viii Figure 2.5 Monarchs antennae are important for proper righting behavior along the vertical plane……………………………………………………………………………………………...65 Figure 2.6 Monarchs can orient without their antennae and without the aid of light cues………66 Figure 2.7 Monarchs use both gravity and magnetic cues together during righting behavior …..67 Table 2.1 Rayleigh’s test results for all trials with a Von Mises distribution……………………68 Table 2.2 V-test results for all trials that did not have a Von Mises distribution………………..69 ix CHAPTER ONE Monarch Butterflies, Danaus plexippus, (Lepidoptera, Nymphalidae) Use Gravity as a Directional Cue for Oriented Upwards Movement Mitchell J. Kendzel and Patrick A. Guerra* Department of Biological Sciences University of Cincinnati Cincinnati, OH, USA *Mitchell J. Kendzel principally composed the work presented here, with the assistance of Patrick A. Guerra. This manuscript is formatted for submission to the Journal of Experimental Biology. 1 ABSTRACT: Gravity is an important environmental cue that provides organisms with directional information in the vertical plane. Using the monarch butterfly (Danaus plexippus) as a model system, we studied how animals responded behaviorally to gravity and how this response could be modulated by other cues that also provide directional information. To do this, we tested monarchs in a behavioral assay that examined their walking movement in a tube maze whose position could be adjusted relative to the vector of gravity. This assay design allowed for changing the vertical position of the tube, the manipulation of light cues, and
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