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What Does the Honeybee See? and How Do We Know? WHAT DOES THE HONEYBEE SEE? AND HOW DO WE KNOW? A CRITIQUE OF SCIENTIFIC REASON WHAT DOES THE HONEYBEE SEE? AND HOW DO WE KNOW? A CRITIQUE OF SCIENTIFIC REASON ADRIAN HORRIDGE THE AUSTRALIAN NATIONAL UNIVERSITY E PRESS E PRESS Published by ANU E Press The Australian National University Canberra ACT 0200, Australia Email: [email protected] This title is also available online at: http://epress.anu.edu.au/honeybee_citation.html National Library of Australia Cataloguing-in-Publication entry Author: Horridge, G. Adrian. Title: What does the honeybee see and how do we know? : a critique of scientific reason / Adrian Horridge ISBN: 9781921536984 (pbk) 9781921536991 (pdf) Subjects: Honeybee. Bees. Insects Vision Robot vision. Dewey Number: 595.799 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying or otherwise, without the prior permission of the publisher. Cover design and layout by Teresa Prowse, www.madebyfruitcup.com Cover image: Adrian Horridge Printed by University Printing Services, ANU This edition © 2009 ANU E Press CONTENTS About the author . .vii Preface . ix Acknowledgments . xi Introduction . xiii Chapter summary . xix Glossary . xxiii 1 . Early work by the giants . 1 2 . Theories of scientific progress: help or hindrance? . 19 3 . Research techniques and ideas, 1950 on . 39 4 . Perception of pattern, from 1950 on . 63 5 . The retina, sensitivity and resolution . 85 6 . Processing and colour vision . 117 7 . Piloting: the visual control of flight . 147 8 . The route to the goal, and back again . 177 9 . Feature detectors and cues . 207 10 . Recognition of the goal . 249 11 . Do bees see shapes? . 263 12 . Generalisation and cognitive abilities in bee vision . 283 Afterthoughts . 307 Summary of the model of bees’ visual processing . 311 Bibliography . 319 v ABOUT THE AUTHOR Adrian Horridge was appointed in 1960 as Director of the Gatty Marine Laboratory, St Andrews, Scotland, while completing the two-volume work with Professor T. H. Bullock of the University of California on The Structure and Function of the Nervous Systems of Invertebrates (1965). At St Andrews, he started a research group that worked on the eyes of crustaceans and insects. In 1969, he brought this group with him to Australia, when he was appointed as one of four foundation professors of the Research School of Biological Sciences at The Australian National University. Since that time, he and his numerous students and postdoctoral collaborators have discovered much about the vision of insects. In 1969, Horridge was elected a Fellow of the Royal Society of London and in 1972 a Fellow of the Australian Academy of Sciences. vii PREFACE The unique and self-contained topic ‘The vision of the bee’ is of interest in its own right as the best-known example of what a typical medium-sized insect can detect with its eyes. It is also a topic of philosophical interest because it raises centuries-old questions about perception, consciousness, sentient beings, human uniqueness and insect-like robots. What does the bee really see? How does the small brain of the bee see so well? How does this influence our ideas about perception, automata and future practical applications? There are many ways to answer these questions. Bees assist us because they can be trained to come to objects or patterns, and trained bees will answer questions put to them in simple tests. The bee’s visual system is also open to analysis by optical, anatomical and electrophysiological methods, by tracking the bees while navigating and route finding and also by studying visual flight control as they pilot themselves between obstacles. This book includes a historical survey of how scientists have approached, experimented with and argued about insect vision for 100 years, finally rejecting anthropomorphism and solving some critical questions. One of the features is the (still-imperfect) coverage of the German contribution to the subject. Until about 1966, insect vision was scarcely mentioned in books in English. The older work was ignored, while the more recent contributions were controversial and unrelated to each other. There was little study of the topic in England and textbooks made a hash of it. This particular science is grounded in observation and logic. There is little mathematics, chemistry or physics involved or need for great learning. Bees are found worldwide and are reasonably representative of all large insects. Research on bee vision can be very cheap. The results have mostly been published but the story is not generally known or even available to the educated public. Here now is an account of what bees really detect with their eyes and how scientists found this out. The accounts of earlier experiments on this road of discovery, and how inferences were made from the data, make a fascinating account of the arguments and counterclaims of contending professors. The approach here is out-and-out support for experiment, backed by the logic of John Stuart Mill and the philosophy of scientific progress of Thomas S. Kuhn. The processes of designing the experiments and inferring the conclusions from the data make a ix WhAT DoES ThE honEyBEE SEE AnD hoW Do WE knoW? miniature picture of scientific effort in several areas of biology, physiology and comparative psychology. They illustrate how the work was really conducted— not always amicably. The basis of this study is the observation of the performance of bees. From the performance, an intuitive inference was usually made, as a stab at explaining the behaviour. Often, the inference was incorrect because the vision of bees was counter-intuitive in several ways. Explanations made by analogy with mammalian visual systems or drawn from the terminology of the cognitive sciences were usually found to be inadequate. There were many examples of excellent observations and reliable data, from which a wrong inference was made, followed by argument without new data, stubborn resistance to reinterpretation and refusal to accept advances made by others. Later, the mechanisms of the performance were analysed by extensive testing of trained bees and, after much thought, the counter-intuitive processing mechanisms of bees’ strange visual behaviour were slowly revealed. The whole subject became an exposition of the stages of visual processing. Bees do not see shapes or objects; they detect parameters and recognise places. This story is told as an example of how early intuitive inferences have given way to the results of carefully designed tests of trained bees. The book is intended for an audience who do not want a text crowded with references and every fact that exists. The aim is for it to be read more like an essay for anyone with some scientific background. It describes the process of scientific discovery on a limited theme, with two excursions into branches of the subject in more detail: the action of the retina and processing by the nerve cells (Chapters 5 and 6). For all chapters, there are sufficient names of researchers given for anybody who wishes to dig deeper, using the extensive bibliography. This book could be used by university students interested in subjects such as vision for physiologists, perception for psychologists, insects for entomologists or zoologists, robot vision for engineers looking for new ideas and scientific method for philosophers. x ACKNOWLEDGMENTS First, I acknowledge with enormous gratitude the contributions of those ancient institutions, St Johns College, Cambridge, where I was for 10 years absorbing a myriad influences from curious role models, and the University of St Andrews, where I learned to stand on my own feet, and where the work on insect vision began during 13 years at the Gatty Marine Laboratory. At Yale and the University of California, I was introduced to research financed by grants. Then at The Australian National University, I was able to expand with my research group on my own broad topic that seemed scientifically interesting: insect vision. Second, I thank the great number of colleagues, who worked with and near me, aided by technical staff, librarians and secretaries. I depended on their support. I owe a particular debt of gratitude to the numerous enthusiastic colleagues who made good use of the plentiful equipment, made scientific advances and mostly published their own work on insect vision. Their names appear throughout this book. Some, in particular, stand out: Tudor Barnard, Malcomb Burrows, John Scholes, Steve Shaw, Rick Butler, Ben Walcott, Ayis Ioannides, Ian Meinertzhagen and David Sandeman. In Canberra: Simon Laughlin, Allan Snyder, Andreas Dubs, Randolf Menzel, Gert Stange, Benno Meyer-Rochow, Ted Maddess, Fred Doujak, Peter Lillywhite, Jenny Kien, David Williams, Roger Hardy, Yasuo Tsukahara, Keiichi Mimura, Mark Leggett, Dan-Eric Nilsson, Mike Land, Stjepan Marčelja, Willi Ribi, Martin Wilson, Richard Payne, Roger Dubois, Doukele Stavenga, David O’Carroll, Tom Matic, Shi Jian, Jan Dalczynski, Peter McIntyre, Qijian Sun, Yang En-Cheng, Danny Osorio, Joe Howard, Mandyam Srinivasan, Tony Heyes, Andrew James, Zhang Shaowu, Miriam Lehrer, Eric Warrant, Mike Ibbotson and Neville Fletcher. There is especial gratitude to the assistants who worked with me, sometimes for many years—notably, Margaret Lang, Charlie Roemmele, Margaret Canny, Bob Jackson, Caroline Giddings, Miriam MacLean, Roland Jahnke, Jadviga Duniec, Ljerka Marčelja, Edyta Kucharska, Sasha Neist, Steve Lucock and Virginia Pierce—and to secretaries (before they became extinct): Veronique, Tess, Tiger Lily, Elizabeth and Margaret. Finally, I owe an infinite debt of gratitude to Audrey, the loving woman I married 55 years ago, who cared for me and four children, in a family life that was full of interest, culture and generosity. xi INTRODUCTION Small in size but high among the wonders of nature, insects delight and amaze us with their skill in flight and their obvious ability to see.
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