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Anatomy and Physiology of the Elasmobrach Olfactory System

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Anatomy and Physiology of the Elasmobrach Olfactory System ANATOMY AND PHYSIOLOGY OF THE ELASMOBRACH OLFACTORY SYSTEM by Tricia L. Meredith 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 December 2011 ACKNOWLEGMENTS This work would not have been possible without financial support from several private donors and scientific organizations including: Gordon Gilbert Scholarship, Captain Al Nathan Memorial Scholarship, Edward Shoaf Scholarship, Marsh Scholarship in Marine Biology, Donald R. Nelson Behavior Research Award, Helen O‟Leary Scholarship, Dr. Vincent R. Saurino Fellowship, American Elasmobranch Society Student Research Award, Lerner-Gray Grant for Marine Research, and Sigma Xi Grants-in-Aid of Research. Additionally, internal support from Florida Atlantic University (FAU) included the FAU Graduate Fellowship for Academic Excellence, FAU Memorial Scholarship, FAU Student Government Scholarship for Undergraduates and Graduates, FAU Alumni Association Scholarship, and a teaching assistantship each semester. While the many funding sources provided the means, several people provided the guidance along this amazing journey. I must first thank my advisor, Dr. Stephen Kajiura. He introduced me to the world of olfaction research during a research trip to Hawaii where I learned everything from shark fishing to EOG electrode construction. From there he mentored me through my Ph.D., providing invaluable advice, edits, and most importantly the basic tools necessary to figure things out for myself in almost any situation. The other members of my dissertation committee, Dr. Kathleen Guthrie, Dr. John Baldwin, Dr. Sarah Milton, Dr. John Caprio (LSU), were also very supportive throughout this process. I cannot express enough gratitude toward John Caprio in particular. He took me under his wing during a time when I was in need of guidance and another perspective, helped me carve a definitive path to obtaining my doctoral degree, and has been there for me every single step of the way. Dr. Tricas allowed me to invade his lab on Coconut Island in Oahu, HI twice to learn electro-physiological techniques and participate in interesting projects. The Gumbo Limbo Environmental Complex in Boca Raton, Fl provided me with use of iii their facility, and the staff, including Kirt Rusenko and Neal Tempel, was always available to help troubleshoot any issues that arose. Bob Hueter, Jack Morris, Carl Luer, and Jayne Gardiner, at Mote Marine Laboratory in Sarasota, Fl, also supplied me with animals, tank space, and lab space. Doug Adams, Joy Young, and colleagues at the Florida Fish and Wildlife Conservation Commission were instrumental in helping me obtain many of my experimental specimens. Dr. Anne Hansen not only welcomed me into her lab at the University of Colorado Denver (and her home) twice, but also was an invaluable mentor. I thank Dr. Rod Murphey, Dr. Evelyn Frazier, Dr. Ken Dawson-Scully, Geri Mayer, and Jenny Govender from the FAU Biological Sciences Department for all of the assistance and opportunities they provided. I also could not have survived graduate school without my labmates and fellow graduate students. Thanks to Dr. M. Porter, M. Smith, L. Dirk, A. Cornett, L. Macesic, M. McComb, D. McGowan, C. Bedore, L. Harris, K. Smith, S. McCutcheon, and the many volunteers that donated their time to my research. Through all of the coffee breaks, edits, happy hours, lab meetings, field trips, and classes, you helped keep me sane. Finally, I thank my family for all of their love and support. Mom, Dad, Grandma Greathouse, Grandma and Grandpa Meredith, thank you for teaching me at an early age that I can do whatever I want in my life as long as I work hard to achieve it. Even if it‟s playing in the ocean for a living! I also thank my sisters who inspire me to be a worthy role model and my amazing fiancé, Dave, who has been nothing but supportive from beginning to end. iv ABSTRACT Author: Tricia L. Meredith Title: Anatomy and Physiology of the Elasmobranch Olfactory System Institution: Florida Atlantic University Dissertation Advisor: Dr. Stephen M. Kajiura Degree: Doctor of Philosophy Year: 2011 The olfactory system is the most highly developed system for molecular sensing in vertebrates. Despite their reputation for being particularly olfactory driven, little is known about how this sense functions in elasmobranch fishes. The goal of this dissertation was to examine the morphology and physiology of elasmobranchs to compare their olfactory system with teleost fishes and more derived vertebrates. To test the hypotheses that elasmobranchs possess greater olfactory sensitivities than teleosts and that lamellar surface area is correlated to sensitivity, I compared the surface area of the olfactory lamellae and the olfactory sensitivities of five phylogenetically diverse elasmobranch species. The olfactory thresholds reported here (10–9 to 10–6 M) were comparable to those previously reported for teleosts and did not correlate with lamellar surface area. Since aquatic species are subject to similar environmental amino acid levels, they appear to have converged upon similar amino acid sensitivities. To test the hypothesis that elasmobranchs are able to detect bile salt odorants despite lacking ciliated olfactory receptor neurons (ORNs), the type of ORN that mediates bile salt detection in the teleosts, I quantified the olfactory specificity and sensitivity of two elasmobranch species to four, teleost-produced C24 bile salts. Both species responded to all four bile salts, but demonstrated v smaller relative responses and less sensitivity compared to teleosts and agnathans. This may indicate that elasmobranchs don‟t rely on bile salts to detect teleost prey. Also, the olfactory system of elasmobranchs contains molecular olfactory receptors for bile salts independent of those that detect amino acids, similar to teleosts. In some elasmobranch species, each olfactory bulb (OB) is physically partitioned into two hemi-bulbs; however, the functional significance of this morphology is not fully understood. The organization of the OBs in three species with varying OB morphologies was examined to test the hypothesis that the elasmobranch OB is somatotopically arranged. Glomeruli in the OB received projections from ORNs in 3-4 olfactory lamellae situated immediately anterior. These results indicate a somatotopic arrangement of the elasmobranch OB, which may be unique among vertebrate olfactory systems and potentially led to the hemi-OB morphology. vi ANATOMY AND PHYSIOLOGY OF THE ELASMOBRANCH OLFACTORY SYSTEM LIST OF TABLES ............................................................................................................................. x LIST OF FIGURES .......................................................................................................................... xi CHAPTER 1 ..................................................................................................................................... 1 CHEMORECEPTION ................................................................................................................... 1 CONSERVED FEATURES IN VERTEBRATE OLFACTION ....................................................... 2 OLFACTION IN FISHES .............................................................................................................. 3 Morphology of the teleost olfactory system .............................................................................. 4 Morphology of the elasmobranch olfactory system ................................................................. 7 Physiology of the teleost olfactory system ............................................................................. 11 Physiology of the elasmobranch olfactory system ................................................................. 14 REFERENCES ........................................................................................................................... 17 CHAPTER 2 ................................................................................................................................... 29 ABSTRACT ................................................................................................................................ 29 INTRODUCTION ........................................................................................................................ 29 MATERIALS AND METHODS ................................................................................................... 31 Animal Collection ................................................................................................................... 31 Morphology............................................................................................................................. 31 Electrophysiology: Experimental Protocol .............................................................................. 33 Analysis .................................................................................................................................. 35 RESULTS ................................................................................................................................... 36 Morphology............................................................................................................................. 36 vii Electrophysiology: Relative effectiveness of amino acids ....................................................
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