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Numerical Cognition in Honeybees: Rule Learning Enables Quantity Discrimination, Zero Comprehension, Simple Arithmetic, and Symbol Use by an Insect

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Numerical Cognition in Honeybees: Rule Learning Enables Quantity Discrimination, Zero Comprehension, Simple Arithmetic, and Symbol Use by an Insect Numerical cognition in honeybees: rule learning enables quantity discrimination, zero comprehension, simple arithmetic, and symbol use by an insect A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Scarlett R Howard M.Sc. (Zoology) at University of Melbourne; B.Sc. (Zoology) at University of Melbourne School of Media and Communication College of Design and Social Context RMIT University October 2018 Declaration I certify that except where due acknowledgement has been made, the work is that of the author alone; the work has not been submitted previously, in whole or in part, to qualify for any other academic award; the content of the thesis is the result of work which has been carried out since the official commencement date of the approved research program; any editorial work, paid or unpaid, carried out by a third party is acknowledged; and, ethics procedures and guidelines have been followed. I acknowledge the support I have received for my research through the provision of an Australian Government Research Training Program Scholarship. Scarlett R Howard 25.09.2018 ii Preface The work presented here was completed for this thesis and is predominantly my own. It was conducted under the supervision of Associate Professor Adrian Dyer (School Media and Communication, RMIT University), Professor Andrew Greentree (School of Science, RMIT University), Dr Jair Garcia (School Media and Communication, RMIT University), and Dr Aurore Avarguès-Weber (Centre de Biologie Intégrative (CBI), Université de Toulouse). Some of the work in this thesis has been published and some of it is in review, thus the journal formatting is retained throughout the thesis and figure titles are specific to the chapters they appear in. Each chapter only refers to figures within the same chapter. Publications and contributions from others are detailed below. Chapter Two has been submitted: Howard, S.R., Avarguès-Weber, A., Garcia, J.E., Greentree, A.D. and Dyer, A.G., (Submitted). Surpassing the subitizing threshold: Appetitive-aversive conditioning improves quantity discrimination in honeybees. All authors contributed to experimental design, interpretation of the data, and editing of the manuscript. SRH predominantly designed the experiments, collected and analysed the data, and wrote the manuscript. All authors gave final approval for submission. Chapter Two has also been presented at the international conference International Congress of Neuroethology 2018. Chapter Three is a published paper: Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2018) Numerical ordering of zero in honey bees. Science. 360: 1124-1126. SRH, AAW, JEG, ADG, and AGD were involved in the design of the experiment, data interpretation, and drafting of the manuscript. SRH, JEG, AGD, ADG, and AGD analysed data. SRH collected data and wrote the manuscript. All authors gave final approval for iii submission. Chapter Three has also been presented at the international conferences Behaviour 2017 and the International Congress of Neuroethology 2018. Chapter Four has been accepted in Scientific Advances and will be published on February 8th 2019: Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (2019) Numerical cognition in honeybees enables addition and subtraction. Scientific Advances. SRH, AAW, JEG, and AGD designed the experiment. SRH performed data collection and wrote the manuscript. SRH, JEG, and ADG analysed data. All authors were involved in the interpretation of results and drafting of the manuscript. Chapter Five is a draft paper: Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG (Submitted) Symbolic representation of number in the honeybee (Apis Mellifera). SRH, AAW and AGD designed the experiment. SRH collected and analysed the data, and wrote the manuscript. Scarlett R Howard is supported by an Australian Postgraduate Award, and has also received funding from the Company of Biologists (JEB Travelling Fellowship), International Commission for Plant-Pollinator Relationships (Young Scientist Scholarship), International Society for Neuroethology (Heiligenberg Student Travel Award), and RMIT University. Other publications during candidature (included in the appendices): Dyer AG, Howard SR, Garcia JE (2016) Through the Eyes of a Bee: Seeing the World as a Whole. Animal Studies Journal 5: 97-109. See appendix 2 Howard SR, Avarguès-Weber A, Garcia JE, Dyer AG. (2017). Free-flying honeybees extrapolate relational size rules to sort successively visited artificial flowers in a realistic foraging situation, Animal Cognition 20: 627-638. See appendix 3 iv Howard SR, Avarguès-Weber A, Garcia JE, Stuart-Fox D, Dyer AG. (2017). Perception of contextual size illusions by honeybees in restricted and unrestricted viewing conditions, Proceedings of Royal Society B 284: 20172278. See appendix 4 Guntarik O, Garcia JE, Howard SR, Dyer AG. (2018). TRACES: Mobile Eye Tracking Captures User Sensory Experience in an Outdoor Walking Tour Environment, Leonardo 51: 163-164. See appendix 5 Howard SR, Avarguès-Weber A, Garcia JE, Greentree AD, Dyer AG. (2018). Honeybees prefer novel insect-pollinated flower shapes over bird-pollinated flower shapes, Current Zoology. See appendix 6 Garcia JE, Shrestha M, Howard SR, Petersen P, Dyer AG. (2018). Signal or cue: the role of structural colours in flower pollination, Current Zoology. See appendix 7 Shrestha M, Garcia JE, Chua JHJ, Howard SR, Tscheulin T, Dorin A, Nielsen A, Dyer AG. (2019). Fluorescent pan traps affect the capture rate of insect orders in different ways, Insects. See appendix 8 v Acknowledgements I can honestly say these years have been the best of my life. For that reason, I have many people to thank. To my primary supervisor, Adrian Dyer, I owe my knowledge, my way of thinking, and my love of research. Adrian has guided me through my postgraduate research and instilled many important life and professional lessons along the way using his unconventional ‘analogies’ and story-telling. He has become a good friend and great mentor throughout this process. Thank you for the hot chocolates, train rides, and dinners with your family. Andrew Greentree has been an incredible supervisor and cheerleader throughout my doctorate. He has taught me not to underestimate myself, or my research, and to follow through with my work and overcome my fears. I thank him for his input from a physics perspective and his support for these past years. To my colleague, friend, and supervisor, Jair Garcia, you have taught me all I know about statistics and modelling. I quite disliked the topic before I met you, but somehow you have managed to make me love it and want to understand it – I’m not sure how you achieved this but thank you for your time and patience. Aurore Avarguès-Weber has not only been a fantastic supervisor but also a great support and friend during my research overseas in her laboratory. She has become a mentor and I hope that in a few years I can achieve the level of success she has managed to reach in the years following her doctorate. I look forward to joining your lab next year. I would also like to acknowledge my collaborators and colleagues including Dr Mani Shrestha, Dr Juergen Schramme, Prof Martin Giurfa, Dr Olivia Guntarik, Leslie Ng, Justin vi Chua, and Stuart McFarlane. You have all made my research possible by providing your knowledge, aid, resources, time, and friendship. I thank my two examiners for their insightful comments and suggestions on my thesis work. I was inspired by your research and thrilled to have my thesis examined by such experts. To my many friends and loved ones, there are too many to name, but thank you for all your support throughout the years and thank you for never complaining about how much I talk about bees. I wish to thank Stephen White. Your support throughout my doctorate has been unwavering. Whether it be reading my manuscripts, listening to me prattle on endlessly about statistics and results, or agreeing to move overseas with me to continue my research, you have always believed in me and my work. Thank you for joining me in this adventure and I hope our next one is just as great. To my family, Rosemary, Steven, Rhys, and Zoe, thank you for your immense support and love. I could not have achieved anything without you all. Thank you for listening to my practice talks, reading my manuscripts, giving me career advice, and pretending to be interested in honeybees for five years. I would like to dedicate my thesis to my parents, Rosemary and Steven, whom have always supported my choices and whom I have to thank for all that I have and all I have achieved. Finally, thank you to all the honeybees involved. I appreciate your time and participation. I will continue to show the world your value and intelligence. vii “The bee's life is like a magic well: the more you draw from it, the more it fills with water” Karl Von Frisch (1886 – 1982) viii Thesis abstract Many non-human animals demonstrate some level of numerical ability which includes an understanding of complex numerical concepts such as arithmetic, sequential ordering of numbers, or an understanding the concept of zero. Although very little research has been done on numerical ability in invertebrates, honeybees and several other insects have been shown to possess some numerical capabilities. In my thesis, I have assessed the capacity of bees to exhibit complex numeric skills such as number categorisation, extrapolation, and simple arithmetic. I show that the use of appetitive-aversive differential conditioning improves the honeybees’ ability to discriminate between quantities above the subitizing range compared to appetitive-differential conditioning. Honeybees have demonstrated an understanding of the quantitative value of nothing and placed an empty set in the correct position along a line of sequential numbers, learnt to categorise numbers as greater or lesser in context, acquired abstract colour-based rules to solve elementary incremental and decremental problems, and demonstrated an ability to match symbols with specific quantities.
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