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VISUAL AND ELECTROSENSORY ECOLOGY OF BATOID ELASMOBRANCHS by Christine N. Bedore A Dissertation Submitted to the Faculty of The Charles E. Schmidt College of Science in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Florida Atlantic University Boca Raton, FL August 2013 Copyright by Christine N. Bedore 2013 ii ACKNOWLEDGEMENTS This work would not be possible without the advice, help, and support that I have received from so many people. To all of you: I am eternally grateful, thank you! Several funding sources provided financial support of this work, including Florida Atlantic University Department of Biological Sciences and Graduate College, American Elasmobranch Society, Society for Integrative and Comparative Biology, Sigma Xi Scientific Research Society, and American Museum of Natural History. The Bank of Dad helped to financially supported my research before grant funds were secured, thanks Dad! I would like to offer my sincere gratitude to my dissertation committee for their years of support, advice, and encouragement. John Baldwin, Tammy Frank, Bob Hueter, and Mikki McComb have all significantly contributed to my scientific development, each in a unique way. A special thanks goes to Tammy Frank and Mikki McComb who have each allowed me to borrow their ERG equipment and have spent countless hours combing over data, reviewing manuscripts, writing letters of recommendation, and troubleshooting with me. Another very special thanks goes to my committee Chair, Steve Kajiura. Steve taught me more than I ever expected to learn about biology, physics, and life. He stood by me through my successes and failures, offered me some amazing opportunities, allowed me the freedom to follow my crazy iv ideas and interests, and gave me free reign over his office. For that, I am forever indebted and thankful. I am fortunate to have the absolute best lab mates I could ever ask for. I am lucky to have you as part of my extended family. Tricia Meredith, Laura Macesic- Ekstrom, Dave McGowan, Shari Tellman, Kier Smith, Sara McCutcheon, Marianne Porter, Kyle Newton, Jordan Snyder, Theresa Gunn, Eloise Cave, Avery Siciliano, Nicole Blahut, Kim Denesha, Gabby Barbarite, and Joey Perez have endured collection trips, tank cleaning, animal food prep, fixing gillnets, have helped teach me electrophysiology, run my experiments, and edit grant proposals and manuscripts. I am especially thankful to Lindsay who has been my partner in crime for the past five years. We have been through a lot together and she will always be my favorite Lamenologist! Several other FAU people have offered advice and support: Mark Royer, Neal Tempel, Jeanette Wyneken, Mike Salmon, Margueritte Koch, Tanja Godenschwege, Jenny Govender, Michelle Cavallo, Jim Nichols, Kristen Ware, Elisa Gaucher, Dennis Hanisak, Rod Murphey, and Gary Perry. Personnel at Gumbo Limbo and Mote Marine have provided experimental, technical, and husbandry assistance: Kirt Rusenko, Cody Mott, Jack Morris, Carl Luer, Krystle Harvey, Jayne Gardiner, Jim DelBene, Andy Stamper, and Lynne Byrd. Florida Fish and Wildlife Commission in Tequesta, FL, Dynasty Marine, and Keys Marine Lab have helped provide fish for experiments. Rich Brill, Nathan Hart, Kara Yopak, Dean Grubbs, Matt Kolmann, Alan Henningson, Robert Fischer, Joe Bizzarro, Eric Noonburg, Sönke Johnsen, and Yakir Gagnon have provided invaluable advice on statistics, visual biology, and elasmobranch ecology. Ellis Loew graciously afforded me the opportunity to visit his lab and entertained me with his tales v of his adventures in visual ecology. Many friends have been supportive in every aspect of my dissertation and they made the good days great and the bad days tolerable. Finally, I need to give respectful appreciation to all of the rays that gave their lives for my research. They inspired me to ask questions and investigate their quirks as an answer to those questions, provided intellectual stimulation for my fellow graduate and undergraduate students, and provided entertainment and an opportunity for learning for thousands of Gumbo Limbo visitors over the years. “You are capable of more than you know. Choose a goal that seems right for you and strive to be the best, no matter however hard the path. Aim high. Behave honorably. Prepare to be alone at times, and to endure failure. Persist! The world needs all you can give.” - E.O. Wilson vi ABSTRACT Author: Christine N. Bedore Title: Visual and electrosensory ecology of batoid elasmobranchs Institution: Florida Atlantic University Dissertation Advisor: Dr. Stephen M. Kajiura Degree: Doctor of Philosophy Year: 2013 The electrosensory and visual adaptations of elasmobranchs to the environment have been more studied than most other senses, however, work on these senses is mostly limited to descriptive analyses of sensitivity, morphology, and behavior. The goal of this work was to explore electrosensory and visual capabilities in a more ecological context. To gain an understanding of the content of bioelectric signals, the magnitude and frequency of these stimuli were recorded from a broad survey of elasmobranch prey items. Teleosts produced a greater voltage than invertebrates and elasmobranchs and there was no correlation between voltage strength with frequency, mass, or total length as assumed in previous studies. The DC bioelectric field was reproduced in a behavioral assay and the sensitivity of two batoid elasmobranchs, the cownose ray (Rhinoptera bonasus) and the yellow stingray (Urobatis jamaicensis) to these stimuli was quantified. Cownose rays demonstrated a median sensitivity of 107nV cm-1, vii which was considerably less sensitive than yellow stingrays that demonstrated a sensitivity of 22nV cm-1. Cownose rays may have reduced sensitivity as a mechanism to prevent overstimulation of the electrosensory system by schooling conspecifics. Although it is unlikely that cownose rays use their electrosensory systems to maintain position within a school as hypothesized, their visual adaptations suggest tracking of schoolmates may be primarily visual. Cownose rays had a faster temporal resolution than yellow stingrays, which would support this hypothesis. Color vision adaptations also correlated to the photic environment of each species; cownose rays inhabit turbid, green-dominated waters and had two cone visual pigments that maximize contrast of objects against the green background. Yellow stingrays were trichromatic and likely possess the ability to discriminate colors in their clear, reef and seagrass habitats, which are spectrally rich. Both species showed evidence of ultraviolet sensitivity, which may aid in predator and conspecific detection as an enhanced communication channel. Future studies should investigate the integration of sensory input and sensory involvement in intraspecific communication to gain more insight into ecological adaptations. viii DEDICATION For Dad, Katie, Layne, and Bruce. You have inspired me to achieve my dreams, no matter how outrageous they are, and to always reach for the stars, no matter how far away they are. Thank you for your endless support and encouragement. ix VISUAL AND ELECTROSENSORY ECOLOGY OF BATOID ELASMOBRANCHS LIST OF TABLES ........................................................................................................ xiii LIST OF FIGURES ....................................................................................................... xiv CHAPTER 1: INTRODUCTION .................................................................................... 1 ELECTRORECEPTION .............................................................................................. 2 VISION ........................................................................................................................ 7 RESEARCH GOALS ................................................................................................... 9 CHAPTER 2: BIOELECTRIC FIELDS OF MARINE ORGANSISMS: VOLTAGE AND FREQUENCY CONTRIBUTIONS TO DETECTABILITY BY ELECTRORECEPTIVE PREDATORS ........................................................................ 11 ABSTRACT ............................................................................................................... 11 INTRODUCTION ...................................................................................................... 12 MATERIALS AND METHODS ............................................................................... 15 Animal collection ................................................................................................... 15 Experimental apparatus .......................................................................................... 15 Electrophysiology protocol .................................................................................... 16 Bioelectric field generator electric potential .......................................................... 19 RESULTS ................................................................................................................... 20 Bioelectric field stimulus generator electric potential ............................................ 22 ix DISCUSSION ............................................................................................................ 23 Frequency measurements ....................................................................................... 24 Voltage amplitude .................................................................................................. 25 Voltage decay and
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