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How Spatial Constraints on Efficacy and Dynamic Signaling Alignment Shape a Nimal Communication

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How Spatial Constraints on Efficacy and Dynamic Signaling Alignment Shape a Nimal Communication How Spatial Constraints on Efficacy and Dynamic Signaling Alignment Shape A nimal Communication How Spatial Constraints on Efficacy and Dynamic Signaling Alignment Shape Animal Communication by Sebastian Alejandro Echeverri B.S. in Biology and Applied Physics, University of Miami, 2013 Submitted to the Graduate Faculty of the Dietrich School of Arts and Sciences in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Pittsburgh 2020 Committee Page UNIVERSITY OF PITTSBURGH DIETRICH SCHOOL OF ARTS AND SCIENCES This dissertation was presented by Sebastian Alejandro Echeverri Becerra Osorio It was defended on May 21, 2020 and approved by Dr. Walter Carson, Associate Professor, Department of Biological Sciences, University of Pittsburgh Dr. Mark Rebeiz, Associate Professor, Department of Biological Sciences, University of Pittsburgh Dr. Tia-Lynn Ashman, Distinguished Professor, Department of Biological Sciences, University of Pittsburgh Dr. Nathan Morehouse, Associate Professor, Department of Biological Sciences, University of Cincinnati Dissertation Advisor: Dr. Corinne Richards-Zawacki, Associate Professor, Department of Biological Sciences ii Copyright © by Sebastian Alejandro Echeverri Becerra Osorio 2020 iii Abstract How Spatial Constraints on Efficacy and Dynamic Signaling Alignment Shape Animal Communication Sebastian Alejandro Echeverri, PhD University of Pittsburgh, 2020 Effective communication is important to the survival and reproduction of many organisms. Signal transmission and reception have spatial constraints that interact to determine effectiveness. Signals are often best perceived from specific angles, and sensory systems may be limited in their ability to detect or interpret incoming stimuli from certain directions. Alignment between these directional biases can be critical to effective communication. Misalignment of either signal or sensor may disrupt signal perception. Signals also degrade during the distance traveled from signaler to receiver. Thus, how animals position themselves during communication may be under selection. Despite this, we know little about the spatial arrangement of signalers and receivers, what behaviors influence positioning, or the causes and consequences of variation in positioning. To address this fundamental gap in knowledge, I developed a geometric framework for studying the spatial constraints of communication and how they shape positioning across visual, sound, and chemical signaling. To investigate respective roles of signaler and receiver in managing these spatial constraints, I then characterized the spatial dynamics of visual signaling in the jumping spider Habronattus pyrrithrix. Males perform an elaborate courtship dance which includes arm waves and colorful ornaments; the latter are not visible from the side. The female can only perceive colors of male displays when they are presented in her frontal field of view. I recorded relative positions and orientations of both actors throughout courtship and established the role of each sex in maintaining signaling alignment. Finally, I tested how males control female orientation, and iv respond to signaling challenges. Using video playback, I asked how males’ arm-waving display and the visual environment determine how effectively they attracted female attention, as well as how males respond to variation in their signaling environment. These studies reveal that signaling alignment is frequently disrupted by females turning away from males, but that male arm-waving effectively re-captures her attention. Males also modulate displays in response to changing spatial and environmental conditions. Overall, this dissertation reveals the widespread role of spatial constraints in driving signaling behavior, and demonstrates that the spatial arrangement of signaler and receiver must be managed dynamically through behavioral responses. v Table of Contents Preface .......................................................................................................................................... xii 1.0 Signals in Space: Geometry as a Framework to Analyze the Inherent Spatial Constraints on Communication Efficacy .................................................................................... 1 1.1 Introduction .................................................................................................................... 1 1.2 Geometry of Visual Communication ............................................................................ 4 1.2.1 Viewing Distance ..................................................................................................5 1.2.2 Directionality of Visual Signals .........................................................................12 1.2.3 Directionality of Sight ........................................................................................21 1.2.4 Positioning within the Visual Environment .....................................................24 1.2.4.1 Directional Illumination ........................................................................ 25 1.2.4.2 Physical Structures ................................................................................ 28 1.2.4.3 Visual Background ................................................................................ 29 1.2.5 Critical Needs and Opportunities .....................................................................31 1.3 Geometry of Sound Communication .......................................................................... 33 1.3.1 Distance of Sound Communication ..................................................................34 1.3.2 Directionality of Sound Signals .........................................................................38 1.3.3 Directionality of Sound Sensors ........................................................................43 1.3.4 Positioning within the Sound Environment .....................................................44 1.3.5 Critical Needs and Opportunities .....................................................................47 1.4 Geometry of Chemical Communication ..................................................................... 48 1.4.1 Fluid Flow and the Directionality of Semiochemical Movement ...................49 vi 1.4.2 Critical Needs and Opportunities .....................................................................52 1.5 Conclusions ................................................................................................................... 53 2.0 Control of Signaling Alignment During the Dynamic Courtship Display of a Jumping Spider ........................................................................................................................... 63 2.1 Introduction .................................................................................................................. 63 2.2 Methods ......................................................................................................................... 69 2.2.1 Study Species and Maintenance ........................................................................69 2.2.2 Courtship Interactions .......................................................................................69 2.2.3 Interactions Between Live Males and Females ...............................................70 2.2.4 Interactions Between Live Males and Female Models....................................71 2.2.5 Video Analysis ....................................................................................................72 2.2.6 Statistical Methods .............................................................................................73 2.3 Results ............................................................................................................................ 75 2.3.1 Interactions Between Live Males and Females ...............................................75 2.3.2 Interactions Between Live Males and Female Models....................................79 2.4 Discussion ...................................................................................................................... 81 2.4.1 Control of Signaling Alignment ........................................................................81 2.4.2 Implications for Communication ......................................................................82 2.4.3 Selection for Control of Receiver Attention.....................................................83 2.4.4 Signaling Behavior in Response to Spatio-social Cues ...................................86 2.4.5 Conclusions .........................................................................................................88 2.5 Acknowledgements ....................................................................................................... 89 2.5.1 Funding Statement .............................................................................................89 vii 3.0 Jumping Spider Adjusts Attention-Grabbing Display to Spatial and Environmental Context .............................................................................................................. 90 3.1 Introduction .................................................................................................................. 90 3.2 Methods ......................................................................................................................... 95 3.2.1 Collection and Maintenance ..............................................................................95 3.2.2
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