Mechanisms of Floral Specialization by Pollen-Foraging Bumble Bees Item Type text; Electronic Dissertation Authors Russell, Avery Leigh 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 03/10/2021 19:37:16 Link to Item http://hdl.handle.net/10150/621876 MECHANISMS OF FLORAL SPECIALIZATION BY POLLEN-FORAGING BUMBLE BEES by Avery Leigh Russell __________________________ Copyright © Avery Leigh Russell 2016 A Dissertation Submitted to the Faculty of the GRADUATE INTERDISCIPLINARY PROGRAM IN ENTOMOLOGY & INSECT SCIENCE In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2016 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Avery Russell, titled Mechanisms of Floral Specialization by Pollen- Foraging Bumble Bees and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. _______________________________________________________________________ Date: (11/21/2016) Daniel R. Papaj _______________________________________________________________________ Date: (11/21/2016) Wulfila Gronenberg _______________________________________________________________________ Date: (11/21/2016) Judith L. Bronstein _______________________________________________________________________ Date: (11/21/2016) Stephen L. Buchmann _______________________________________________________________________ Date: (11/21/2016) Anne S. Leonard Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies 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. ________________________________________________ Date: (12/4/2016) Dissertation Director: Daniel R. Papaj 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of the 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 an accurate acknowledgement of the 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 copyright holder. SIGNED: _________________________ Avery L. Russell 4 ACKNOWLEDGEMENTS This doctoral dissertation reflects the combined efforts of a great number of intelligent and considerate people. First, I thank my advisor, Dan Papaj, who welcomed me into his lab, introduced me to the incredible world of animal behavior, and gave me a great many opportunities that I will always be grateful for. Dan has been instrumental in teaching me how to think, write, and communicate clearly and I am most appreciative of his continued mentorship and support. Judie Bronstein has been a powerful role model and I thank her for the hours of advice, encouragement, and advice she has given me. I thank Steve Buchmann for his friendship, his encyclopedic knowledge and passion for bee research, and for taking us on many excursions to see what animals actually do outside of the lab. I thank Wulfila Gronenberg for his tremendous hospitality, for grounding my graduate career, for teaching me many valuable skills, and for allowing me to occasionally monopolize his microscopes. I thank Annie Leonard for her knowledge, support, and for reading over countless manuscript drafts. The dissertation committee and the Bronstein, Gronenberg, Leonard, and Papaj labs have been key and tremendous sources of support and friendship. Many people conducted these experiments and they deserve plentiful praise. I could not have asked for a finer group of research assistants, whose enthusiasm, hard work, compassion, and friendship made mentoring a joy. Of the many students who have worked with me, my thanks especially to (alphabetized) Heather Gillette, Bekah Golden, Tara Hall, Kevin Mauerman, Mary McIntosh, Eleni Moschonas, China Rae Newman, Cynthia Trefois, and Sarah White. I would also like to thank the EEB, CIS, and EIS staff, especially Sky Dominguez, Lauren Harrison, Marilyn Kalthoff, Teresa Kudrna, Rachael Mattull, Kristina Souders, and Pat Waters, for diligently documenting all my weirdly wonderful shipments and for taking care of the huge amount of paperwork and scheduling necessary to keep a dissertation going. This work would likewise have been impossible without the greenhouse assistance of Abreeza Zegeer, who taught me many valuable horticultural tricks. For making me feel at home in EEB, EIS, and Neuroscience, in addition to those mentioned previously I must also thank, in alphabetical order: Yves Carrière, Goggy Davidowitz, Katrina Dlugosch, Kirsten Grabo, Molly Hunter, Wendy Moore, Lynne Oland, Nick Strausfeld, Bruce Tabashnik, Kathleen Walker, and Konrad Zinsmaier. I also thank the numerous graduate students and postdocs who contributed brains, companionship, coffee, and beer to keep me functional – and for not running away from an unending stream of puns. In alphabetical order, these wonderful people include, but are not limited to Sarah Bengston, Kathryn Busby, Tuan Cao, Bodil Cass, Dan Charbonneau, Carla Essenberg, Garrett Hughes, Eileen Jeffrey, Elinor Lichtenberg, Chan Lin, Brianna McTeague, Chandreyee Mitra, Sarah Morrison, Felicity Muth, Matt Nielsen, Robert Orpet, John Palting, Sarah Richman, Andre Riveros, Pedro Rodrigues, Eric Shuman, Gordon Smith, Andy Stiegler, Corinne Stouthamer, Jessica Vogt, Lisa Wang, Kara Welch, and Gabby Wolff. And the list goes on... Lastly, I thank the spiny plants and the stinging bees for cooperating most of the time, and for ibuprofen and Epipens when they did not. 5 This research was funded by grants from the Center for Insect Science (UA), NSF (Award Nos. IOS-0921280 and IOS-1257762), the Graduate and Professional Student Council (UA), the Entomology and Insect Science Program (UA), and the Department of Entomology (UA). 6 DEDICATION To my family, teachers, and mentors. I would especially like to thank John & Yvi Russell, who have always supported me and encouraged a love of the natural world and the humanities; and my partner-in-crime: the intelligent and amazing Sarah Morrison. 7 TABLE OF CONTENTS ABSTRACT……………………………………………………………………………….8 INTRODUCTION……………………………………………………………………….10 PRESENT STUDY………………………………………………………………………16 REFERENCES…………………………………………………………………………..20 APPENDIX A: ..................................................................................................................23 PATTERNS OF POLLEN AND NECTAR FORAGING SPECIALIZATION BY BUMBLEBEES OVER MULTIPLE TIMESCALES USING RFID APPENDIX B: …………………………………………………………………………..75 BEES LEARN PREFERENCES FOR PLANT SPECIES THAT OFFER ONLY POLLEN AS A REWARD APPENDIX C: …………………………………………………………………………129 SYNERGY BETWEEN VISUAL AND OLFACTORY CUES IN ASSESSMENT OF CONCEALED POLLEN REWARDS BY BUMBLE BEES APPENDIX D…………………………………………………………………………..178 CONCEALED FLORAL REWARDS AND THE ROLE OF EXPERIENCE IN FLORAL SONICATION BY BEES APPENDIX E: ……………………................................................................................226 HOW A GENERALIST BEE ACHIEVES HIGH EFFICIENCY OF POLLEN COLLECTION ON DIVERSE FLORAL RESOURCES 8 ABSTRACT A fundamental question in biology is how animals efficiently locate and use diverse resources. Pollinators foraging on flowers are one of our most thoroughly studied examples of generalist foraging behavior and cognition. Individual pollinators typically specialize on a subset of flowering species available to them. Specialization by nectar- foraging pollinators is often the consequence of learned or innate preferences for floral display traits such as color, pattern, and scent. Pollinators must also typically learn to extract nectar from each floral type. By specializing, pollinators reduce costs associated with learning and forgetting nectar extraction routines. Specialization also benefits the plant by enhancing conspecific pollen transfer. Yet nectar is not the only floral reward. The pollen of hundreds of thousands of plant species is collected by pollinators such as bees, beetles, and flies. In fact, solitary and social bees must collect both pollen and nectar to survive. However, much of the vast literature on bee foraging behavior concerns the collection of nectar. This research investigated mechanisms by which generalist bumblebees (Bombus impatiens) specialize on diverse floral resources. Most foragers in a colony were reward generalists over their lifetime, but specialized daily on either pollen or nectar collection. Lifetime patterns of pollen collection were associated with interindividual differences in sensory morphology. Pollen-foraging bumblebees had weak innate preferences, but learned strong preferences for pollen-only plant species, with preferences mediated primarily by anther properties. The anthers provided indirect cues of concealed pollen, and bees learned to prefer properties of the anthers to select potentially rewarding flowers.