The discovery of a visual system: the honeybee

293 Pages·2019·6.642 MB·English

by  Horridge, G. Adrian

The Discovery of a Visual System: the Honeybee
The author with coloured patterns on square targets of standard size.
The Discovery of a Visual System:
the Honeybee
Light guides, optics, visual cues,
optic flow, route finding
Adrian Horridge
The views and opinions expressed in this book are those of the author
and do not necessarily reflect the official policy or position
of CAB International.
CABI is a trading name of CAB International
CABI CABI
Nosworthy Way 745 Atlantic Avenue
Wallingford 8th Floor
Oxfordshire OX10 8DE Boston, MA 02111
UK USA
Tel: [phone] Tel: [phone]
Fax: [phone] E-mail: [email protected]
E-mail: [email protected]
Website: www.cabi.org
© Adrian Horridge 2019. All rights reserved. No part of this publication
may be reproduced in any form or by any means, electronically, mechanically,
by photocopying, recording or otherwise, without the prior permission of
the copyright owners.
A catalogue record for this book is available from the British Library, London,
UK.
Library of Congress Cataloging-in-Publication Data
Names: Horridge, G. Adrian, author.
Title: The discovery of a visual system : the honeybee / Adrian Horridge.
Description: Boston, MA : CABI, [2019] | Includes bibliographical
references and index.
Identifiers: LCCN 2018049622 (print) | LCCN 2018055072 (ebook) |
ISBN 9781789240900 (ePDF) | ISBN 9781789240917 (ePub) |
ISBN 9781789240894 (hbk : alk. paper)
Subjects: LCSH: Honeybee--Physiology. | Vision--Research.
Classification: LCC QL568.A6 (ebook) | LCC QL568.A6 H57 2019 (print)
| DDC 595.79/9--dc23
LC record available at https://lccn.loc.gov/2018049622
ISBN-13: 978 1 78924 089 4 (hardback)
978 1 78924 090 0 (ePDF)
978 1 78924 091 7 (ePub)
Commissioning Editor: Ward Cooper
Editorial Assistant: Emma McCann
Production Editor: Shankari Wilford
Typeset by SPi, Pondicherry, India
Printed and bound in the UK by Severn, Gloucester
Contents
About the author vii
Preface ix
Introduction xi
1 The Difficult Birth of Honeybee Colour Vision 1
2 No Way to Untie the Spell 12
3 Innovation, Deep Thought and Hard Work 28
4 The Fundamentals of the Insect Compound Eye 44
5 How Bees Distinguish Colours and Modulation 89
6 Feature Detectors, Cues, Resolution, Preferences and Coincidences 106
7 Symmetry and Asymmetry: Signposts in Route Finding 135
8 Bee Vision is Not Adapted for Pattern or Shape 150
9 The Visual Control of Flight 173
10 The Route to the Goal and Back Again 197
11 What Was Not Mentioned 222
12 What We Learned 231
Appendix Training and Testing Bees 253
Author Index 259
Subject Index 263
v

About the Author
Born in 1927, after wartime teenage years
Adrian Horridge was admitted as a scholar
of St John’s College, Cambridge in 1945, and
passed the Natural Sciences Tripos with
first class. He joined the Department of Zo-
ology, completed a PhD on electrophysi-
ology of primitive nervous systems, won a
Senior Award from the Commissioners from
the Great Exhibition of 1851, and a Research
Fellowship at St John’s College. In 1956, he
became a lecturer in Zoology at University
of St Andrews, Scotland. Most of his early
work was on marine animals found there
and at Millport (west coast), Naples, Ply-
mouth and on reefs of the Red Sea. In 1959,
he was a Fellow of the Center for Advanced
Studies in the Behavioral Sciences at Palo
Alto, California, where Ted Bullock and Ad-
rian wrote most of The Structure and Function of the Nervous Systems Of Invertebrates
(1965). He returned as Director of the Gatty Marine Laboratory at St Andrews in 1961. After
a period of intense research on invertebrate nervous systems, mainly on eyes of insects and
Crustacea, he was elected to the Royal Society in 1969.
In the same year, he moved to the Australian National University as one of four foun-
der professors of the new graduate Research School of Biological Sciences. There, his re-
search and training of others focused on insect vision. He supervised 51 PhD students al-
together, 37 of whom became professors in 14 different countries. Three of his students,
Meyer-Rochow, Simmons and Warrant, won three separate Ignoble Prizes: this must be
unique. Eight of his students or post-docs have been elected to the Royal Society, and one
to the Royal Society of Canada, four of them retired as Cambridge professors. Up to 2018,
Adrian published 260 papers on neurobiology. This output, together with the two volumes
with Ted Bullock, Structure and Function of the Nervous Systems of the Invertebrates (Bul-
lock and Horridge, 1965), followed by another, Interneurons (Horridge, 1968), makes him
one of the fathers of neurobiology of invertebrates. The books are still prized.
vii
viii About the Author
Adrian has also researched and written three books, several monographs and 12 pa-
pers on the sail trading fleets, fishing vessels and outrigger canoes of Indonesia and their
history, functions, rigs and structures. These are the major reference source for Indonesian
maritime ethnography and have recently become expensive collector’s items. In 2016, a
version was published in the local language, Bahasa Indonesia.
In sabbatical years, Adrian has twice been an Overseas Fellow of Churchill College
Cambridge, and a Colonial Fellow of Balliol College, Oxford. He made many research visits
to marine laboratories, and has dived on coral in all parts of the world. His son Mark and
grandson Tor Lattimore are professors of mathematics.
Remarkable practical innovations emerged unexpectedly from the research on insect
vision in Canberra. By studying the light path in flies’ eyes, Allan Snyder (1972) realized
how light signals entered most efficiently into light guides and travel long distances along
them. This new understanding led directly to the World Wide Web of optical fibre. In 1985,
Adrian realized that range to nearby objects was measured by the relative motion induced
in the compound eyes by walking or flying insects (Horridge, 1987). With this measure-
ment of range to nearby contrasting edges, insects have no need to distinguish every separ-
ate object. His group showed that bees use this optic flow to give them a third dimension
(Srinivasan et al., 1989a, b). They carried it through to guidance principles for vehicles and
put insect-style vision on drone aeroplanes and helicopters with a computer on board. Both
Snyder and Srinivasan won the Australian Prime Minister’s Prize for Science and were
elected to the Royal Society for these discoveries.
At the age of 91, Adrian is still researching the vision of the honeybee as a guide to vi-
sion of arthropods in general, and as a model for reverse engineering of simple visual sys-
tems for robot tasks.
Adrian Horridge was married for 59 years to Audrey (1930–2013), née Lightburne, a
Cambridge and Oxford graduate. In her final job, Audrey was in charge of welfare of all
36,000 government-supported overseas students, with an office in every university in Australia.
His son, Mark, also a Johnian, is a professor of macroeconomics and its computing tech-
niques, based in Melbourne. Daughter Alison is an artist who home-schooled her family;
Naomi juggles motherhood with writing, lecturing and museum curating. His youngest
daughter, Meret, also a Johnian, is a published poet and teaches molecular biology in Zürich.
Rebecca is a roaming radio journalist, specializing on environmental and social issues in
Australia. His granddaughter, Dr Finnian Lattimore works in computer technology in the
Australian National University. His grandson Tor Lattimore is a professor of analyticals,
working on Deep Mind at Google, London. Two great-grandchildren look quite promising.
Adrian Horridge
Adrian-Horridge.org
Preface
When I retired in 1992, a research topic with little expense was essential, so for 15 years every
spring and autumn I continued training bees in my old ‘shed of discovery’ in the grounds of
the Australian National University (ANU). I would start work at 8 a.m. for 2 h training them,
then prepare tests. My assistant would turn up at 10 a.m. and, between regular periods of con-
tinued training we would test them. We took turns to have lunch, shut shop at 4 p.m., 5 days
a week during October to December, and March to May. The other months were either too hot
or too cold for the bees. Usually, we started with a new group of bees each Monday morning
and finished the experiment on Friday afternoon. I fed the bees early each morning at the
weekend so that they kept their habit of coming for sugar. My aim was to train bees to every
kind of display and test them to reveal exactly what they had detected and learned.
My retirement saved a lot of money for ANU, but funding was never a problem for me.
First, to pay for a part-time assistant, I had a grant as an Emeritus Fellow of ANU, then a
series of grants from the Royal Society that came by a remarkable route. I asked the Secretary
of the Royal Society if there were funds to hire an assistant. The reply was initially un-
favourable, because UK government funds were for work based in the UK. Then it was sug-
gested that I should apply to a fund ‘for the assistance of fellows’ that had been established
200 years ago to assist fellows who fell into poverty. The fund had accumulated ‘a large sum’.
I certainly needed assistance, and my case fitted the rules, so I applied and was asked to re-
veal my income. By good fortune, all my retirement funds were in a portfolio of mining com-
panies, which paid few dividends, and my wife Audrey had a separate income. So, I sent
them a copy of my tax return, which indeed revealed a very small income, and they sent me
£10,000 to pay for a part-time assistant. There was no shortage of interesting school leavers
and backpackers, who had to be not allergic to bees, and who had never expected to learn
how to train them.
All funds that came from overseas to support research in Australia were subject to 10%
tax unless the product was re-exported. So, I was obliged to publish the results in overseas
journals. The grant was continued for a time, but one day a letter arrived to say that all the
available funds had been spent on the refurbishment of the staircase in Carlton House.
Research prospered and eventually ANU E Press published my book on black/white vi-
sion of the honeybee in 2009, while I was fully occupied caring for Audrey, my wife. It lacked
chapters about colour because the new results were not yet comprehensible, and an attack of
the shingles forced me to send the book to press although unfinished. Also, on the question
of colour vision of bees, I had not been sufficiently provoked. To write anything, I needed first
ix