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Proquest Dissertations Neotropical fungal endophytes: Diversity and ecology Item Type text; Dissertation-Reproduction (electronic) Authors Arnold, Anne Elizabeth Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 23/09/2021 13:07:27 Link to Item http://hdl.handle.net/10150/289841 INFORMATION TO USERS This manuscript has been reproduced from the microfilm master. UMI films the text directly from the original or copy submitted. Thus, some thesis and dissertation copies are in typewriter face, while others may be from any type of computer printer. The quality of this reproduction is dependent upon the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleedthrough, substandard margins, and improper alignment can adversely affect reproduction. In the unlikely event that the author did not send UMI a complete manuscript and there are missing pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note will indicate the deletion. Oversize materials (e.g., maps, drawings, charts) are reproduced by sectioning the original, beginning at the upper left-hand comer and continuing from left to right in equal sections with small overiaps. ProQuest Information and Learning 300 North Zeeb Road, Ann Arbor, Ml 48106-1346 USA 800-521-0600 NEOTROPICAL FUNGAL ENDOPHYTES: DIVERSITY AND ECOLOGY b\ A. Elizabeth Arnold Copyright cv A. Elizabeth Arnold 2002 A Dissertation Submitted to the Faculty of the DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY In Partial Fulfillment ofthe Requirements for the Degree of DOCTOR OF PHILOSOPHY in the Graduate College THE UNIVERSITY OF ARIZONA 200 2 UMI Number; 3073188 Copyright 2002 by Arnold, Anne Elizabeth All rights reserved. ® UMI UMI Microfomi 3073188 Copyright 2003 by ProQuest information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. ProQuest Infomiation and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346 THE UNIVERSITY OF ARIZONA ® GRADUATE COLLEGE As members of the Final Examination Committee, we certify that we have read the dissertation prepared by Anne Elizabeth Arnold entitled Neotropical Fungal Endophytes: Diversity and Ecology and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of DoctOr of Philosophy Lucinda A. McDade^ Date Ju^th L, Bronstein Date /4 %JkcjidUK Robert H. Robichaux Date Date Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College. I hereby certify chat I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. Dissertation Director Date STATEMENT BY AUTHOR This dissertation has been submitted in partial fultlllment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library. Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for e.xtended quotation from or reproduction of this manuscript in whole or in part may be granted by the copyright holder. SIGNED: 4 ACKNOWLEDGMENTS My heartfelt thanks go to Lucinda A. McDade. whose guidance, support, insights, and example inspired me to pursue, and to complete to m> satisfaction, the present u ork. I have had an enjoyable and enlightening career as a graduate student, which 1 attribute largely to Lucinda's influence: I am lucky to have found a mentor who so strongly exemplifies my goals as a researcher, teacher, and person, and I am thankful to have learned from Lucinda in these ways. I am also most grateful to Judie Bronstein and Rob Robichaux. w ho have contributed greatly to my development as a biologist. I thank Judie for insightful discussions, for sharing her deep knowledge regarding species interactions, and for cheerfully and carefully editing my thesis chapters. I thank Rob for setting an example of e.xcellence as both a biologist and as a teacher, and for sharing with me both the attentive quality of his editing and the good cheer of his ongoing support. I hope to emulate these strengths as I continue to grow as a researcher and instructor. The quality of my research has been impro\ ed by insights from dis erse facult> at the University of Arizona, including Carlos Martinez del Rio. Larn. Venable, Nancy Moran. and Michael Rosenzweig. I am grateful for support from Dan Papaj. Bill Birky. \Va>ne Maddison. Leticia .Aviles. Michael Nachman. Peter Reinthal. and especially John Lundberg. I thank Rick Michod and Hans van Etten for sharing laboratory space. Christina Kennedy for ad\ ising an early internship. Molly Hunter for encouragement, and Yves Carriere for statistical consulting. I especially appreciate the statistical advice and diverse insights I've received from Bob Steidl. I have benefited extensively from colleagues, mentors, and friends at other institutions, each of w hom has enhanced my training, experience, and know ledge. I especially thank Lissy Coley and Tom fCursar (University Utah) tor an introduction to tropical biology, and for their wonderful contributions to the field as mentors and biologists: Egbert G. Leigh. Jr. (STRl) for many enlightening discussions in Toad Hall; and Greg Gilbert (University of California at Santa Cruz) for training, helpful interactions, and leadership in tropical m\colog>. Allen Herre has furthered the cause of endophyte research, and 1 thank the Panama research group - especially Luis Mejia. Enith Rojas. and Zuleyka Maynard - for enjoyable collaborations. Friends at BCl whose enthusiasm for tropical biology helped fuel my own include Steve ^'anoviak. Jim Dalling. Stefan Schnitzer. Lars Rosengreen. Dave Tomblin. Spider Dave Penney. Hubi Herz. and Bettina Engelbrecht: 1 hope our paths w ill cross w ith frequency, and w ith a forest canopy overhead. To graduate students and postdocs at U.A. I am grateful for the w onderful community in which I've grown both personally and intellectually. I especially thank Jen Weeks. Dan Hahn. Amy Faivre. Rachel Levin. Margrit Mcintosh. Jill .Miller, Amy Boyd. Caleb Gordon. Maria Clauss. Goggy Davidow itz. Steve Perlman, Brian McGill, Margaret Evans. Tricia Kennedy. David Hearn. Nat Holland. .Alice Bo> le. Allen Gibbs. Mike Weiser. Wendy Moore, and Stacey Forsyth. 1 also acknowledge friends in EEB's front office, including Kate Rile>. Mark Brewer. Sue Whitworth. and Joan Zokvic. I thank Kate Riley and Cher> l Craddock for keeping me up to date on the literary world. Janet Barnard and Katy Riley for assistance in the lab. .Mago and Chili for enriching my day-to-day. and A. Guinness for entertaining Lucinda and me w ith frequency. Two final acknowledgments merit special attention. First. 1 thank my family for supporting my desire to do the work 1 love: 1 w ill always be grateful to Tom. Kimball, and Charlie .Arnold for the chance I've had to pursue my deep hean's call. Last. 1 give my deepest thanks to Julia and especially David Maddison, w hose sense of curiositv- and wonder is a bright spot of light, w hose support and patience are tremendous, and w hose joy in all things living reminds me daily of the pleasure of exploration, the elegance of diversity, and the richness of life's tapestr\ . TABLE OF CONTENTS ABSTRACT 6 CHAPTER 1: INTRODUCTION 8 An ir.traduclion to microbial endophylcs 9 Fungal endophytes 11 IVhy irupical forests'? 12 Biodiversity of foliar enduphytes: ecological factors 13 Biodiversity of foliar endophytes: taxonomic patterns 17 Endophyte-host interactions 21 Evolutionary implications of endophytism 23 The present study, and explanation of dissertation format 25 CHAPTER 2: PRESENT STUDY 29 APPENDIX A: ARE TROPICAL FUNGAL ENDOPHYTES HYPERDIVERSE? 34 APPENDIX B: FUNGAL ENDOPHYTES OF DICOTYLEDONOUS TROPICAL TREES: PATTERNS OF ABL^NDANCE AND DIVERSITY 47 APPENDIX C: EFFECTS OF CANOPY COVER AND LEAF AGE ON COLONIZATION BY TROPICAL FUNGAL ENDOPHYTES; ECOLOGICAL PATTERN AND PROCESS IN C'.-JC'.-JLXSTERCULIACEAE) 59 APPENDIX D: FACTORS INFLUENCING DEPOSITION OF FUNGAL AIR SPORA IN A NEOTROPICAL FOREST 96 APPENDIX E; UBIQUITY. ABUNDANCE. AND RICHNESS OF FOLIAR ENDOPHYTES: CONSISTENCY AMONG DIVERSE WOODY HOSTS IN A LOWL.AND TROPICAL FOREST 118 APPENDIX F: MORPHOSPECIES AS FUNCTIONAL TAXONOMIC UNITS: A CRITICAL ASSESSMENT FOR STUDIES OF ENDOPHYTE BIODIVERSITY 166 APPENDIX G: FUNGAL ENDOPHYTES INCREASE MINIMUM LEAF CONDUCTANCE IN LEAVES OF A NEOTROPICAL TREE 267 APPENDIX H: MUTUALISTIC FUNGAL ENDOPHYTES LIMIT FOLIAR PATHOGEN DAMAGE IN A TROPICAL FOREST TREE 304 REFERENCES 6 ABSTRACT Fungal endophytes associated witii leaves ot'woody plants are thought to be diverse and abundant, especially in tropical forests. However, associations of endophytes with tropical woody angiosperms have not been characterized in detail. In this dissertation. I assess: (1) the scale of endophyte biodiversity in a tropical forest: (2) ecological, temporal, and host-mediated factors influencing endophyte abundance in leaves of tropical trees:
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