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The Sensory Basis for Ecological Paradigms on Wave-Swept Shores

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The Sensory Basis for Ecological Paradigms on Wave-Swept Shores THE UNIVERSITY OF CALIFORNIA Los Angeles The Sensory Basis for Ecological Paradigms on Wave-Swept Shores A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Biology by Graham Andrew Ferrier 2010 UMI Number: 3452132 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. UMI' Dissertation Publishing UMI 3452132 Copyright 2011 by ProQuest LLC. All rights reserved. This edition of the work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 © copyright by Graham Andrew Ferrier 2010 The dissertation of Graham Andrew Ferrier is approved. ~~) V <L K x Paul Barber hfr-i~^/cz\ (hy^^ Steven D. Gaines OAjjut^ (juxs^-l^-s Cheryl Ann Zimmer, Committee Co-chair ^n^\; Richard K. Zimmer, Committee Co-chair University of California, Los Angeles 2010 DEDICATION To Carrie, Nayla, Mom, and Dad, for your unwavering support and belief in me for all these years, it has been a long time. TABLE OF CONTENTS List of Figure v List of Tables vii Acknowledgments viii Vita xi Abstract xiii Chapter 1 Whelk-Barnacle Interactions, the Energetics of Prey Choice, and the Sensory Basis for an Ecological Paradigm 1 Literature Cited 63 Chapter 2 Barnacle Glycoproteins: a Keystone Molecule that Structures Natural Communities 73 Literature Cited 112 Chapter 3 Barnacle MULTIFUNCin: a Multifunctional Barnacle Protein at the Core of Community Dynamics 126 Literature Cited 158 IV LIST OF FIGURES Chapter 1 Figure 1-1 Relative abundance of prey species at each field site 47 Figure 1-2 Size of barnacles consumed and the frequency of size classes 48 Figure 1-3 Size of mussels consumed and the frequency of size classes 49 Figure 1-4 Size of turban snails consumed and the frequency of size classes 51 Figure 1-6 Energy gained per unit time handled for three prey types 52 Figure 1-7 Barnacle size frequency, whelk size choice, electivity, and energy 53 Figure 1-8 Whelk prey selection in choice experiments 54 Figure 1-9 Whelk response to waterborne cues at Broad Beach 55 Figure 1-10 Prey mimics eaten embedded with crude protein extractions 56 Figure 1-11 Prey mimics eaten embedded with protein precipitates 57 Figure 1-12 Prey mimics eaten embedded with Pro teinase-K digested proteins 58 Chapter 2 Figure 2-1 Feeding and settlement responses to crude protein 102 Figure 2-2 Feeding and settlement responses to active (NH^SC^ cut 103 Figure 2-3 M.W. distribution, and feeding and settlement response to each 104 Figure 2-4 Glycoprotein separation, and feeding and settlement response 105 Figure 2-5 Comparison of all active purification steps 106 Figure 2-6 Reducing SDS-P AGE gel of all active purifications steps 107 Figure 2-7 Reducing SDS-PAGE gel of LCA-purified barnacle tissues 108 Chapter 3 Figure 3-1 SDS-P AGE of purified glycoprotein and isolated subunits 149 Figure 3-2 ESI-GEMMA spectrum of native and denatured glycoproteins 150 Figure 3-3 MALDI-ToF spectrum of active isolated subunits 151 Figure 3-4 Settlement and feeding response to isolated glycoprotein subunits 152 Figure 3-5 Settlement and feeding response compared between purifications 153 Figure 3-6 Inferred evolutionary history of the active protein 154 vi LIST OF TABLES Chapter 1 Table 1-1 Feeding responses following ingestive conditioning 46 Chapter 3 Table 3-1 Peptide sequences for degenerate primers obtained in LC MS/MS 148 vn ACKNOWLEDGEMENTS The findings of this dissertation are not the single accomplishments of one person, but rather the product of numerous minds coming together to solve a problem. I would like to recognize those people who have contributed to this work over the years and who are partly responsible for its findings. Furthermore, I would like to thank those individuals who helped me through this long journey in science. First, I would like to acknowledge my family. It was not long ago that I struggled just to stay in school. Through it all my mother and father never lost hope in me and knew all along that a day would come for me to find my own path. Moreover, a lot of my interest in the marine environment stems from my early days sailing with my grandfather, mother, and father in New England. Those days obviously influenced me and I am very grateful to have had such an introduction. Second, I would like acknowledge my wonderful wife, Carrie Schneider Ferrier, whose love and support in even the toughest times keeps me going. She has put up with a level of work and near-poverty for 5 years that many others would have run from. Carrie is my rock, and my constant inspiration that life is too short to not follow something you are passionate about, thank you Carrie. Finally, I must recognize my intrepid dog, Nayla, who follows me where ever I go, even in the roughest of intertidal conditions. She helped collect countless organisms and endured numerous hours in rough intertidal water retrieving settlement plates at all hours of the day. Your webbed feet came in handy on more than one occasion. vin Members of the Zimmer lab, Ryan Ferrer, Julie Himes, and Sammi Ali contributed valuable insights and generated thoughtful discussion with respect to research of all sorts. Kevin Peng, Riley Jondle, Ian Roberts, Aleskey Korolyov, Jenny Wang, Michelle Li, Noelle Bridigainberry, Heather Johnston, Patrick Green, Leo Varzi, and Emily Admanson tirelessly conducted field surveys, produced crude extracts and ran bioassays. Don Conestro of the UC Rancho San Marino Reserve was always available and numerously provided a warm meal and good conversation while working the Central California coast. My committee members, Drs. Joe Loo, Steve Gaines, Paul Barber, and Steve Kim provided expert guidance, comments, and advice throughout the course of my dissertation. Steve Kim took the time to work directly with me in the lab teaching the fundamentals of biochemistry. With his support I learned more biochemistry in two short years than many learn with a Bachelors degree. Joe Loo took the time to teach proteomics and mass spectrometry in a way that could be easily incorporated into ecology. Paul Barber, and the Barber lab, allowed me to use their space and equipment and were always there to answer the questions of a sequencing- and phylogenetics- novice. Finally, Steve Gaines provided critical ecological insights which were instrumental in tying sensory biology, proteomics, and ecology together into a compelling story. Finally, I am indebted to the support Drs. Dick and Cheryl Ann Zimmer have provided. They gave time, energy, expertise, money, and most importantly an opportunity for me to explore science, and for that I am eternally grateful. Dick "Z" ix Zimmer coaxed from me a level of work that I believed I could not do myself and constantly pushed for more. Although he set his bar quite high, his guidance always managed to get me over it. His insight has allowed me to broaden my scientific horizons and from them my mind typically follows ideas from the level of proteins up through their impacts on community dynamics. I owe him much more than I can write here. From Cheryl Ann I learned the critical, but often neglected, importance of scaling in experiments, a lesson I will take with me everywhere. Here ability to convey concepts and messages with enthusiasm is a skill I hope to match when I teach and during times when I felt stuck with courses I often thought of her style and I managed to get through them. Furthermore, Cheryl Ann took the time to assist me with writing. She has patiently gone through countless revisions and taught me how to communicate as a scientist, a skill I lacked before my valuable interactions with her. From Dick and Cheryl Ann's guidance I feel I have accomplished something scientifically meaningful I can not thank them enough for this. x VITA September 11, 1980 Born, Morristown, New Jersey 2002 Bachelor of Science, Marine Resources and Development, University of Rhode Island Kingston, RI 2005 M. S., Biology, California State University Northridge. Northridge, CA 2005-2010 Teaching Assistant University of California, Los Angeles Los Angeles, CA 2007 Mia Tegner Award in Ecology Western Society of Naturalists 88th Annual Meeting 2010 Division of Ecology and Evolutionary Best Student Research Award Society for Integrative and Comparative Biology Annual Meeting PUBLICATIONS AND PRESENTATIONS Ferrier, G.F., and R.C. Carpenter. 2009. Subtidal benthic heterogeneity: Impacts on the flow environment, and marine algal community structure and morphology. Biological Bulletin 217:115-129. Ferrier, G.A., C.A. Zimmer, and R.K. Zimmer. Chemical Cues and the Keystone Species Hypothesis. Talk presented at the 2007 Western Society of Naturalists Meetings. Ferrier, G.A., C.A. Zimmer, and R.K. Zimmer. The Sensory Basis for and Ecological Paradigm: Predator-Prey Interactions on the Rocky Intertidal. Talk presented at the 2007 Benthic Ecology Meetings. xi Ferrier, G.A., C.A. Zimmer, S.J. Kim, and R.K. Zimmer. Chemical signaling in turbulent environments. Talk presented at the 2008 AChemS International Symposium on Olfaction and Taste. Ferrier, G.A., C.A. Zimmer, and R.K. Zimmer. Keystone Molecules and the signals that structure natural communities. Talk presented at the 2010 annual Society for the integrative and comparative biology.
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