The effects of nectar-robbing on a plant- pollinator mutualism and the evolution of nectar-robbing and sociality in bees Item Type text; Dissertation-Reproduction (electronic) Authors Richardson, Sarah Claire 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 05/10/2021 07:26:04 Link to Item http://hdl.handle.net/10150/290257 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. 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Ml 48106-1346 USA 800-521-0600 THE EFFECTS OF NECTAR-ROBBING ON A PLANT-POLLINATOR MUTUALISM AND THE EVOLUTION OF NECTAR-ROBBING AND SOCIALITY IN BEES by Sarah Claire Richardson A Dissertation Submitted to the Faoxlty of the DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2001 UMI Number: 3016495 UMI ® UMI Microform 3016495 Copyright 2001 by Bell & Howell Information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. Bell & Howell Information and Leaming Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346 2 THE UNIVERSITY OF ARIZONA ® GRADUATE COLLEGE As members of the Final Examination Committee, we certify that we have read the dissertation prepared by Sarah niairp Richard'^nn entitled The Effects of Nectar-Robbino on a PIant-Pnllinatnr Mutualism and the Evolution of Nectar-Robbino and Sociality in Bees and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy ri Tlan 3i, 2QQ1 BronsteiJ Date QO / UaTniel R. Papaj Date ^ ^CO ^ Nancy A. Nora^ Lucinaa Date ucnmann 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 that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. CUi/tlth. / ^/ny!/2tSAy<?i) Tan .^l,?Oni Dissertation Director Date Judith L. Bronstein 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is deposited in the Uruversity Library to be made available to borrowers imder niles 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 extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. 4 ACKNOWLEDGMENTS I am grateful to Dr. Judith Bronstein, Dr. Lucinda McDade, Dr. Daniel Papaj, Dr. Nancy Moran, Dr. Stephen Buchmarm, Dr. Francisco Omelas, and Dr. Richard Hudson for their time and their valuable suggestions for improving this dissertation. I would especially like to thank Dr. Judith Bronstein for helpful discussions of experimental design, stimulating discussions of cheating in mutualisms, and precise comments on drafts of all chapters in this dissertation. Dr. Stephen Buchmaim generously provided instruments, dye, greenhouse space, and advice on techniques for this research. Nicole Plotkin and Joyesha Chesnick were valuable field assistants; both had incredible stamina in the desert heat and useful suggestions for research. Sandy Adondakis, Eric Dyreson, and Maria Clauss gave suggestions on statistical analysis. Amy Faivre and Jill Miller gave advice on techniques for photography of pollen and pollen tubes. Sandy McGraw, Peter Murphy, David Banks, Nancy Compton, Kevin Toal, Katherina Spoms, Aaron Gove, and Mary Brown, who were volimteers from the Southwestern Research Station, helped with fieldwork investigating the effects of nectar-robbing bees. Fieldwork was supported by two grants from the Theodore Roosevelt Memorial Fimd of the American Musevim of Natural History, by the 1994 Cranwell Smith Pollination Award from the University of Arizona, by the Southwestern Research Station Student Support Fund, and by grants from the Department of Ecology and Evolutionary Biology at the University of Arizona. A fellowship that gave me time to conduct phylogenetic research was generously provided by the Biological Diversification Research Trairiing Grant from the University of Arizona. The Knight family of Paradise, AZ, the Ritchins families of Cotton City, N. M. and Animas, N. M., John Caron of Crown Dancer Estates, Myrtle BCraft of Portal, and Ann and John Dominic of Portal were kind in allowing research to be conducted on their land and in inviting me into their homes. 5 DEDICATION I dedicate this dissertation to three scientists who showed me the joy of being a biologist. Dr. Myra Niemeier began our first day together by asking me what I wanted to leam; the list is still growing. Dr. Paul Johnsgard took me to see the mating dances of prairie chickens and whooping cranes, two of the most memorable sights in my life. Dr. John Janovy, Jr. gave me a net and let me discover the most beautiful parasites in the world for myself. Finally, I dedicate this dissertation to my parents, Mr. and Mrs. Wallace and Martha Richardson, who have always encouraged me. 6 TABLE OF CONTENTS ABSTRACT 7 CHAPTER 1: INTRODUCTION 9 Effects of Nectar-Robbing on Pollinator Behavior and Plant Reproduction 11 Comparison of Costs and Benefits from Mutualists and Antagonists 12 Evolution of Sociality, Nectar-robbing, and Diet Breadth in Bees 12 CHAPTER 2: PRESENT STUDY 15 APPENDIX A: TEMPORAL VARIATION IN POLLINATOR ABUNDANCE AND POLLINATOR FORAGING BEHAVIOR IN RESPONSE TO ROBBED FLOWERS 20 APPENDIX B: BENEFITS AND COSTS OF FLORAL VISITORS TO CHILOPSIS LINEARIS: POLLEN DEPOSTHON AND STIGMA CLOSURE 38 APPENDIX C: THE EFFECTS OF NECTAR-ROBBERS ON MUTUALISTS-COSTLY OR BENEHCLAL? 73 APPENDIX D: WERE DIET BREADTH AND NECTAR-ROBBEMG FACTORS IN THE EVOLUTION OF SOCIALITY IN BEES? 114 APPENDIX E: SUMMARY OF LEVEL OF SOCIALITY AND LEVEL OF NECTAR-ROBBING FOR GENERA OF SHORT-TONGUED AND LONG- TONGUED BEES 164 7 ABSTRACT How will the intrusion of other species that remove rewards without providing reciprocal services affect the interaction between mutualists? How do costs and benefits from these "cheaters" compare to costs and benefits from potentially mutualistic visitors? Finally, did nectar-robbing, one kind of cheating, promote the evolution of complex levels of sociaKty by allowing bees access to a wider range of resources? I investigated these questions in the research described below. I found that pollinators visiting Chilopsis linearis (Bignoniaceae) spent less time visiting robbed flowers than visiting unrobbed flowers, and did not visit them as often as expected. Thus, robbing appeared to have a negative effect on pollinators visiting Chilopsis linearis. I compared costs and benefits of floral visitors to Chilopsis linearis (desert willow). Chilopsis had serrsitive stigmas that closed immediately upon touch and may have reopened later. I foimd that the probability of stigma reopening depended on the source and number of pollen grairis deposited. I compared visitors by number of pollen grains deposited, viability of pollen that they deposited, and their effect on stigmas. Nectar-robbers did not benefit plants by pollen deposition, but they also did not cost plants by causing stigmas to close without adequate pollen having been deposited. I investigated the effects of robbing on poUinator behavior and plant reproductive success. Nectar volumes were lower in robbed flowers than in unrobbed flowers. However, the most effective pollinators, bumblebees, did not avoid robbed flowers. In investigating male reproductive success, I foimd 8 that on some days, dye mimicking pollen traveled farther from robbed flowers, indicating that robbing may sometimes be beneficial to plants. In investigating female reproductive success, I found that there was no difference in pollen tube number between robbed and unrobbed flowers. Thus, a negative effect on one mutualist may not affect the other mutualist. I hypothesized that the evolution of robbing in bees was associated with a broad diet breadth and the evolution of complex sociality. Using phylogenetically independent contrasts for taxa within three geographical regions, I found that in some cases, a broad diet breadth was associated with sociality and robbing. 9 CHAPTER 1 INTRODUCTION Recently, researchers have become interested in the balance between conflict and cooperation in mutualisms.