Bumblebees’ Bombus impatiens (Cresson) Learning: An Ecological Context by Hamida B. Mirwan A Thesis Presented to The University of Guelph In partial fulfillment of requirements for the degree of Doctor of Philosophy in School of Environmental Biology Guelph, Ontario, Canada © Hamida B. Mirwan, August, 2014 ABSTRACT BUMBLEBEES’ BOMBUS IMPATIENS (CRESSON) LEARNING: AN ECOLOGICAL CONTEXT Hamida B. Mirwan Co-Advisors: University of Guelph, 2014 Professors Peter G. Kevan & Jonathan Newman The capacities of the bumblebee, Bombus impatiens (Cresson), for learning and cognition were investigated by conditioning with increasingly complex series of single or multiple tasks to obtain the reinforcer (50% sucrose solution). Through operant conditioning, bumblebees could displace variously sized combinations of caps, rotate discs through various arcs (to 180°), and associate rotation direction with colour (white vs. yellow). They overcame various tasks through experience, presumably by shaping and scaffold learning. They showed incremental learning, if they had progressed through a series of easier tasks, single caps with increasing displacement complexity (to left, right, or up) or of balls with increasing masses, but could not complete the most difficult task de novo. They learned to discriminate the number of objects in artificial flower patches with one to three nectary flowers presented simultaneously in three compartments, and include chain responses with three other tasks: sliding doors, lifting caps, and rotating discs presented in fixed order. Pattern recognition and counting are parts of the foraging strategies of bumblebees. Multiple turn mazes, with several dead ends and minimal visual cues, were used to test the abilities of bumblebees to navigate by walking and remember routes after several days. They rapidly learned these mazes and remembered the routes even after 16 days. Bumblebees could learn from each other, socially by imitation, observation, and communication within the nest. They were slower to learn to forage with dead conspecific models than with living ones, whether nest-mate or non-nest-mate. Bees that had no opportunity for social learning were unable to forage. The array of experimental approaches I used for training bumblebees and my results have expanded the scope and understanding of the complexity of invertebrate learning and cognition in the context of comparative psychology, and have application to ecological and ethological principles of the evolution of learning and cognition. ACKNOWLEDGEMENTS I am thankful to Allah for giving me the health and the strength to finish my study. I am grateful to my country, Libya, for the scholarship granted to me to pursue doctoral studies, and the University of Guelph for the opportunity to do graduate work. My deepest thankfulness goes to my supervisor Professor Dr. Peter Kevan for accepting me and for his brilliance and knowledge from which I benefited during the past years and I have had the privilege to work with him and will forever be grateful for that. His dedication and commitment to science and education is truly inspiring and remarkable. Special thanks to the members of my graduate committee for great support and for sharing their knowledge on study techniques: Dr. Jonathan Newman; Dr. Georgia Mason for her support, and discussion of several issues, and help with the edition of the final document; Dr. Ernesto Guzman. I am grateful to have Dr. Sarah Bates of being always available for questions and help, Dr. Thomas Woodcock for his time to review some of my work, and John Charles for his help with my final work of my thesis. I also thank Joy Roberts who was the secretary of the graduate studies, and Dr. Hung Lee and Dr. Paul Sibley who were the graduate coordinator, of the School of Environmental Sciences, University of Guelph, for their help of administrative issues during my study, Dr. Francesco Leri at Psychology Department, University of Guelph for his help and comments on some of my papers, Dr. Les Shipp for giving the opportunity to work and gain Canadian experience at Agriculture and Agri-Food Canada at Harrow Research Centre, Harrow, Ontario, and Dr. Marisol Amaya Márquez at National University of Colombia. Finally, I thank all the people who work and manage the Honeybee Research Centre at the University of Guelph, iv Guelph, Ontario, especially Paul Kelly for providing the food supplements for my bees during all my experiments, and BioBest Biological System, Leamington, Ontario, Canada for providing the bees during all period of my study. Special thanks to my mother and other members of my family, who believed in and supported me through my doctoral studies. Deep thanks to Mohsin Grera who always helped, supported and encouraged me to find strength and hope. I thank other people who taught me, all my friends for their support and solidarity with me during these years for their friendship. Financial support of this work was by The Ministry of Higher Education and Scientific Research, Tripoli- Libya, NSERC, CANPOLIN, and The University of Guelph, Guelph, Ontario, Canada. v DEDICATION I dedicate this dissertation: To My father Bashir Mirwan, who always engaged and taught me that, the best kind of knowledge is that which is learned for its own sake. To My mother, who taught me that, even the largest task can be accomplished if it is done one step at a time. To My brother Najme, and my nephew Abdul Aziz. vi TABLE OF CONTENTS ACKNOWLEDGEMENTS ................................................................................................................. IV DEDICATION ........................................................................................................................................ VI LIST OF TABLES..................................................................................................................................... XI LIST OF FIGURES ............................................................................................................................. XII CHAPTER 1 INTRODUCTION ..........................................................................................................1 1.1 Introduction ............................................................................................................................................. 1 1.1.1 Learning definitions ......................................................................................................................................... 2 1.1.2 Definitions of learning found through a review of the literature ...................................................................... 3 1.1.3 The benefits and the cost of learning ................................................................................................................ 4 1.2 Innate behaviour ............................................................................................................................................. 6 1.3 Learning .......................................................................................................................................................... 6 1.3.1 Non Associative learning ................................................................................................................................. 6 1.3.2 Associative learning ......................................................................................................................................... 7 1.3.3 Cognitive learning .......................................................................................................................................... 10 1.3.3.1 Insight learning ....................................................................................................................................... 10 1.3.3.2 Problem Solving...................................................................................................................................... 10 1.3.3.3 Conditional discrimination and response chaining ................................................................................. 13 1.3.3.4 Navigation and maze navigation ............................................................................................................. 16 1.3.3.5 Social learning ........................................................................................................................................ 18 1.3.4 Objectives ....................................................................................................................................................... 21 1.3.5 Overarching Hypothesis ................................................................................................................................. 21 1.4 Glossary ........................................................................................................................................................ 22 CHAPTER 2 COMPLEX OPERANT LEARNING BY WORKER BUMBLEBEES (BOMBUS IMPATIENS CRESSON (HYMENOPTERA: APIDAE)) .................................... 25 2.1 ABSTRACT .................................................................................................................................................. 25 2.2 INTRODUCTION ........................................................................................................................................ 26 2.3 MATERIAL AND METHODS .................................................................................................................... 27 2.3.1 Experimental set up .......................................................................................................................................