UC Irvine UC Irvine Electronic Theses and Dissertations Title Deconstructing visual signals in social butterflies Permalink https://escholarship.org/uc/item/0jd725qm Author Finkbeiner, Susan Diane Publication Date 2015 License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA, IRVINE Deconstructing visual signals in social butterflies DISSERTATION Submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in Ecology and Evolutionary Biology by Susan Diane Finkbeiner Dissertation Committee: Professor Adriana D. Briscoe, Co-chair Professor Robert D. Reed, Co-chair Professor Nancy T. Burley Professor Kailen A. Mooney 2015 Chapter 1 © 2012 The Royal Society Chapter 2 © 2014 John Wiley and Sons All other materials © 2015 Susan D. Finkbeiner DEDICATION To My parents: Mary and David Finkbeiner, for their unconditional support throughout my lifelong endeavors to become an entomologist and study tropical butterflies; My sisters: Brenda Finkbeiner and Karla DeFazio, for their patience enduring my obsession with insects; And to the late Dr. Thomas Eisner: who encouraged me to never loose curiosity for the fascinating insects and butterflies that I love. “No one changes the world who isn’t obsessed.” -Billie Jean King “In Wildness is the preservation of the world” - Henry David Thoreau ii TABLE OF CONTENTS Page LIST OF FIGURES……………………………………………………………… iv LIST OF TABLES………………………………………………………………. vi ACKNOWLEDGEMENTS……………………………………………………… vii CURRICULUM VITAE...………………………………………………………. ix ABSTRACT OF THE DISSERTATION……………………………………….. xi INTRODUCTION………………………………………………………………. 1 CHAPTER 1: Anti-predator benefits of communal roosting behavior in Heliconius butterflies Introduction……………………………………………………………… 14 Methods………………………………………………………………….. 17 Results…………………………………………………………………… 22 Discussion……………………………………………………………….. 25 Literature Cited………………………………………………………….. 29 CHAPTER 2: Relative contributions of color versus pattern to predator avoidance and mate attraction in Heliconius butterflies Introduction……………………………………………………………… 39 Methods………………………………………………………………….. 41 Results…………………………………………………………………… 50 Discussion……………………………………………………………….. 53 Literature Cited………………………………………………………….. 59 CHAPTER 3: Adaptive function of ultraviolet (UV) and fluorescence in Heliconius butterflies Introduction……………………………………………………………… 70 Methods………………………………………………………………….. 71 Results…………………………………………………………………… 74 Discussion……………………………………………………………….. 77 Literature Cited…………………………………………………….……. 79 CHAPTER 4: True UV color vision in a butterfly with two UV opsins Introduction……………………………………………………………… 92 Methods………………………………………………………………….. 94 Results…………………………………………………………………… 99 Discussion……………………………………………………………….. 104 Literature Cited………………………………………………………….. 107 SUMMARY OF DISSERTATION CONCLUSIONS …………………………. 116 iii LIST OF FIGURES Page Figure 1.1 Natural and artificial roosts of Heliconius erato with examples of bird attacks………………………………………………….…. 36 Figure 1.2 Reflectance spectra of natural and artificial butterfly wings used in discriminability calculations……………………………….…… 37 Figure 2.1 Color- and pattern-manipulated wing models experience different predation rates and different probabilities of inducing pre-mating approach behavior in male butterflies ……………………………. 66 Figure 2.2 Reflectance spectra of the natural and artificial model dorsal wing colors used in mate preference studies…………………..… 67 Figure 2.3 Evidence of predation attempts on butterfly models……………. 68 Figure 2.4 Graphical model of approach and courtship behavior…………… 69 Figure 3.1 Natural and artificial Heliconius butterfly wings and excitation and emission spectra of 3-hydroxy-DL-kynurenine (3-OHK)…… 83 Figure 3.2 Reflectance spectra of artificial H. erato butterfly models with and without UV…………………………………………………… 84 Figure 3.3 Reflectance spectra of artificial H. erato butterfly models with and without fluorescence…………………………………………. 85 Figure 3.4 Reflectance spectra of Eueides isabella non-fluorescing yellow wing pigment, and non-fluorescing H. erato butterfly models…… 86 Figure 3.5 Irradiance spectra of open sunlight and cloud cover, and the experimental cage under open sunlight and cloud cover…………. 87 Figure 3.6 Male and female H. erato butterflies approach and court UV- and fluorescence-manipulated butterfly models at varying rates……… 88 Figure 3.7 Specific male and female H. erato approach and courtship behaviors toward UV- and fluorescent-manipulated artificial butterfly models…………………………………………………… 89 Figure 3.8 Artificial butterfly models with and without UV and fluorescence experience similar predation rates in field studies………………… 91 iv Figure 4.1 A male H. erato butterfly is shown on the light source apparatus during a trial………………………………………………………. 111 Figure 4.2 Proportion of correct choices to the trained wavelength stimulus of 390 nm for H. erato and E. isabella butterflies under varying light intensities……………………………………………………. 112 Figure 4.3 Proportion of correct choices to the trained wavelength stimulus of 380 nm for H. erato and E. isabella butterflies under varying light intensities……………………………………………………. 113 Figure 4.4 Proportion of correct choices to the trained wavelength stimulus of 400 nm for H. erato and E. isabella butterflies under varying light intensities……………………………………………………. 114 Figure 4.5 Proportion of correct choices to the trained wavelength stimulus of 436 nm for H. erato and E. isabella butterflies under varying light intensities……………………………………………………. 115 v LIST OF TABLES Page Table 1.1 Results from discriminability calculations for butterfly models using low light intensity and open habitat irradiance……………… 34 Table 1.2 Data representing attacks on butterfly models at field sites in Costa Rica and Panama, categorized by aggregation size…………. 35 Table 2.1 Achromatic contrasts for both the natural wing spectra and artificial wing gray spectra…………………………………………………… 64 Table 2.2 The ratios of approach and courtship occurrences are for male butterflies during paired mate choice trials………………………… 65 vi ACKNOWLEDGEMENTS First and foremost I thank my graduate advisors, Dr. Adriana Briscoe and Dr. Robert Reed, for unparalleled guidance and support throughout my graduate career, and for recognizing my potential as a researcher. I admire their intelligence, accomplishments, and dedication, and I am grateful for their time and effort teaching me valuable skills that I will use throughout the rest of my career. This dissertation, along with my other academic achievements and successes as a graduate student, truly reflects their superior advising capabilities. This work would not have been possible without their contributions. I am also very grateful to my advising committee members, Dr. Nancy Burley and Dr. Kailen Mooney, for their suggestions and helpful discussions about my research project ideas. They provided invaluable knowledge, especially with respect to project design and statistical analyses, for ecology and behavior-based assays. Thank you for pushing me to broaden my background in those disciplines. A sincere thank you to my friends and family for helping me through this journey. I deeply thank my parents, Mary and David Finkbeiner, for their endless love and support throughout my lifetime preparing for a career as a scientist. They never once hesitated to help me reach my lifelong dream of becoming and entomologist and studying tropical butterflies, from taking me on collecting trips when I was five years old to letting me study abroad in Costa Rica. Thank you to my sisters, Karla and Brenda, for being patient with my insect obsession since I was two years old. And thank you to Santiago Meneses Ospina, the other bug-loving half of me, who has not only helped me with field work, statistics, and project ideas, but also provided mental and emotional support when I needed it most, even from the time applied to graduate school. Thanks for being there for me. Many thanks to those who have provided additional research advice and aided in project development, including Dr. W. Owen McMillan with the Smithsonian Tropical Research Institute (STRI), and other STRI personnel and researchers in Panama, including Adriana Tapia, Megan Supple, Elizabeth Evans, Brett Seymoure, Barbara Huber, Moises Abanto, and Oscar Paneso; and to those with the Organization for Tropical Studies (OTS) at the La Selva Biological Station that helped make my field seasons a success. It goes without saying that I thank everyone who has assisted with butterfly model assembly and field work, and endured hot, humid days in the rainforest and greenhouses, rain or shine: Angela Oh, Nina Chiu, Ella Yuen, Maggie McDuffee, Jimena Golcher Benavides, Talia Gustafson, Micki Kellinger, and Jasmine Velez – a big thank you to all you for toughing it out in the field! I am also grateful to Daniel Osorio for his ideas and recommendations, as well as Larry Gilbert, Jim Mallet, Chris Jiggins, Richard Merrill, Patricio Salazar, Johannes Spaethe, and Christian Salcedo for giving tips on making artificial butterfly models and/or advice working with Heliconius in the field. Thank you also to Michael D. Lee for contributing our hierarchical Bayesian analysis for Chapter 2, and to Michael Phelan, Kameryn Denaro, and Fabio Macciardi who have helped with statistical analyses; and thanks to Georg Striedter for his time and input as a member of my advancement to candidacy committee.