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Insect–Plant Biology This page intentionally left blank Insect–Plant Biology Second Edition Louis M. Schoonhoven Joop J.A. van Loon Marcel Dicke Laboratory of Entomology, Wageningen University, The Netherlands 1 AC Great Clarendon Street, Oxford OX2 6DP Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York # Oxford University Press 2005 The moral rights of the author have been asserted Database right Oxford University Press (maker) First edition first published 1998 by Chapman & Hall Second edition first published 2005 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, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Schoonhoven, L.M. Insect-plant biology / Louis M. Schoonhoven, Joop J.A. van Loon, Marcel Dicke. — 2nd ed. p. cm. ISBN 0–19–852595–8 (alk. paper) — ISBN 0–19–852594–X (alk. paper) 1. Insects—Food. 2. Insect-plant relationships. I. Loon, J.J.A. van. II. Dicke, Marcel. III. Title. QL496.S38 2005 595.717085—dc22 2005019634 Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India Printed in Great Britain on acid-free paper by Ashford Colour Press, Hampshire ISBN 0–19–852594–X 978–0–19–852594–3 ISBN 0–19–852595–8 (Pbk.) 978–0–19–852595–0 (Pbk.) 13579108642 This book is dedicated to Vincent G. Dethier, Tibor Jermy, John S. Kennedy, and Jan de Wilde, whose pioneering contributions paved the way of modern research in the biology of insect–plant interactions This page intentionally left blank Foreword to the second edition It is widely known that plants and insects make up pressures elicited in either or both directions. We approximately half of all known species of multi- know that ecological as well as physiological fac- cellular organisms. They have been evolving tors influence diet breadth. We know that an insect together for over one hundred million years, with population restricted to a plant species may varying levels of interaction leading to the selection become genetically isolated in the first step of a of characters that are studied today in every branch speciation event. We recognize that while insect of biology, from biochemistry and genetics to evolution follows plant evolution the reciprocity of behaviour and ecology. close co-evolution is not necessarily present. The interactions between insects and plants may This book amply demonstrates the breadth of the be mutualistic, as with some specialized flower- field, with the three authors bringing their com- pollinator pairs, and the overall importance of bined expertise and experience to all aspects of insects as pollinators gave rise to the earliest detailed Insect–Plant Biology. From the vast literature on studies of plant-insect relationships two hundred the topic the authors have selected examples of years ago. Antagonistic interactions, in particular experiment and theory to produce a book that is a between crops and herbivorous insects, have pro- comprehensive guide for students and researchers vided the inspiration for many studies in the past alike. From an overview of the patterns found in hundred years, leading to greater understanding of nature, they move logically to plant structure and plant chemistry, insect physiology and behaviour chemistry, host finding and host choice, including and ecology. The ability to establish molecular variation and insect physiology. The later chapters phylogenies has led to renewed interest in the degree include coverage of ecology and evolution, insect of co-evolution of plants with insects. In these and flower interactions, and last, to applications of studies, complexities revealed themselves in the knowledge in insect-plant interactions. form of multiple interactions—with microorgan- Since 1998, when the first edition of this book was isms, fungi, predators and parasitoids of insects—all published, advances have been made particularly in impacting how interactions between plants and plant biochemistry and evolution. Molecular tech- insects develop, vary, and evolve. By contrast, many niques have elucidated details in these and other examples of herbivores being inconsequential in the areas, and the understanding of insect-plant biology lives of plants have also been found. has broadened. With the inclusion of Marcel Dicke Today, the field of plant-insect interactions among the authors, some of the newer work as well encompasses the whole gamut of relationships, as the topic of co-evolution get a somewhat different across the complete range of biological disciplines. treatment, and throughout the book, there are We think, not just of an insect herbivore choosing to additions and updates. For anyone with an interest eat an undefended plant, but of the many historical in any aspect of plant and insect interactions, this factors that influence the choice made, the pheno- text will be a firm and reliable resource. typic plasticity of behaviour, the different trophic levels playing a part in the response, the sensory Elizabeth A. Bernays and neural determinants of the choice, the con- University of Arizona sequences of it for the herbivore, the plant genes Tucson activated in their turn and the potential selection May 2005 vii This page intentionally left blank Preface to the second edition Apart from offering an update motivated by the hospitable and inspiring environment when rapidly expanding literature of the past seven working on this second edition. years, this second edition differs in two respects We are especially grateful to everyone at the from the previous one. First, Dr. Tibor Jermy, one of Production Department of Oxford University Press the founders of the field of insect-plant relations for their stimulation and help with turning our text and co-author of the first edition, bears no into what we hope will be a useful and stimulating responsibility for the present book. Yet his extens- book. ive knowledge and views on the subject can be traced back in the present edition. It is with pleas- Wageningen, Summer 2005 L.M. S. ure that we dedicate this volume to Tibor Jermy, to J.J.A. v. L. express our respect for his deep insights and long- M. D. lasting contributions to the development of insect- plant biology. The second difference with the first edition relates to recent changes in the scientific approach of the multifaceted way in which insects and plants interact with each other and with their environ- ment. New insights into, among others, the molecular biology of chemoreception and induced plant defences and their effects on higher trophic levels allow a more comprehensive approach of the theme of this book than could be envisaged only a few years ago. Studying insect-plant interactions at the molecular level adds an exciting dimension to our understanding. We are indebted to several colleagues, who have read and commented on chapters, including Tibor Jermy, Peter de Jong, Erich Sta¨dler, and Freddy Tjallingii. We thank them for their encouragement and help. Hans Smid produced some marvellous new photographs and several other colleagues have allowed us to reproduce some of their finest micrographs. M.D. gratefully acknowledges the NERC Centre for Population Biology of Imperial College at Silwood Park (UK) and its director Charles Godfray, as well as Maarten and Elly Koornneef (Cologne, Germany) for providing a ix Preface to the first edition Green plants cover most of the terra firma on planet We wish to dedicate this book to the memory of Earth. Insects are dominant among plant con- three great men who have deeply influenced our sumers. The interactions between plants trying to thoughts on this subject and who can be considered avoid consumption, and insects trying to optimize as founding fathers of the field: Jan de Wilde, food exploitation, are the subject of this book. It is a Vincent G. Dethier, and John S. Kennedy. Without rich subject: the primary literature has grown dur- their foresight, their stimulating enthusiasm, and ing the past 25 years at an exponential rate. It is also their perceptiveness of basic mechanisms operative an intellectually challenging subject since, in spite in nature the field of insect–plant relationships of the wealth of facts, the principles underlying would not have reached its present prominence. insect–plant interactions are still largely unknown. Many people have provided generous assistance This book aims to categorize the multitude of facts in a variety of ways—stimulating discussions, derived from studies in natural surroundings as frank criticism, the provision of material for illus- well as agricultural environments, and attempts to trations, and permission to use published diagrams indicate emerging lines of understanding. Hope- and information. We should especially like to fully it will serve as an introduction to students of mention those who have read parts of the manu- this area of biology and will highlight to general script and made useful suggestions for improve- biologists the complexity of interactions between ment: T.A.

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