Insect overwintering is a fascinating process involving many physiological, epidemiological, biochemical and behavioural changes. The study of the overwintering process can offer an insight into the development of insects, as well as help us to predict the patterns of disease epidemic and crop destruction caused by some species. This book provides a comprehensive account of the various forms of insect overwintering that highlights important areas of economic interest. It will be essential reading for advanced students and researchers in the fields of zoology, agriculture, forestry and ecology. THE ECOLOGY OF INSECT OVERWINTERING THE ECOLOGY OF INSECT OVERWINTERING S. R. LEATHER Lecturer in Pest Management, Department of Biology, Imperial College K. F. A. WALTERS Principal Scientific Officer, Central Science Laboratory, MAFF, Harpenden and j. s. BALE Professor of Environmental Biology, Birmingham University CAMBRIDGE UNIVERSITY PRESS CAMBRIDGE UNIVERSITY PRESS Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao Paulo Cambridge University Press The Edinburgh Building, Cambridge CB2 2RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9780521417587 © Cambridge University Press 1993 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 1993 Reprinted 1995 First paperback edition 1995 A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Leather, S. R. (Simon R.) The ecology of insect overwintering / Simon R. Leather, Keith F. A. Walters, and Jeffrey S. Bale. p. cm. Includes bibliographical references (p. ) and index. ISBN 0-521-41758-9 (he) 1. Insects - Ecology. 2. Insects - Physiology. I. Walters, Keith F. A. II. Bale, Jeffrey S. III. Title. QL463.L43 1993 595.7'0543 - dc20 91-43260 CIP ISBN-13 978-0-521-41758-7 hardback ISBN-10 0-521-41758-9 hardback ISBN-13 978-0-521-55670-5 paperback ISBN-10 0-521-55670-8 paperback Transferred to digital printing 2006 Contents Foreword Page ix 1 Introduction 1 Why study overwintering? 1 What is overwintering? 2 Advantages and disadvantages of overwintering 3 2 The overwintering locale - suitability and selection 5 Introduction 5 The winter habitat - regional climate 5 Terrain and overwintering success 7 Effects of local habitat 10 Selection of the overwintering site 20 3 The stimuli controlling diapause and overwintering 25 Introduction 25 The induction of the overwintering state 26 Maintenance and termination of the overwintering state 42 Re-entry into a second period of winter diapause 59 Sex and the response to overwintering cues 60 Overwintering cues and parasitoid-host interactions 62 Overwintering cues for social insects 65 Varying responses to overwintering cues in different geographical areas 67 Synchronisation of overwintering stage with season 71 4 Insect cold-hardiness 75 Introduction 75 Concepts and definitions 76 Strategies of insect cold-hardiness 77 Ecophysiological approaches to insect cold-hardiness 143 vn Vlll Contents 5 Costs and benefits of overwintering 148 Introduction 148 Developmental stage and overwintering success 148 Winter inactive insects 149 Winter active insects 156 Winter avoidance 158 The costs of overwintering 161 Spreading the risk 163 Physical costs 165 Metabolic costs 166 Reproductive costs 172 Insect colour and overwintering costs 173 Conclusions 176 6 Prediction and control 177 Introduction 177 Systems in use 178 Systems in development 192 Systems still to be developed 196 Control 200 Conclusion 204 Bibliography 206 Index 240 Foreword The study of insect overwintering has largely concentrated on a few well defined areas of study. Whether this has been the result of the under- standable reluctance of entomologists to expose themselves to the rigours of the great outdoors during what is one of the more taxing times of the year or to the fact that the importance of the overwintering stage in relation to the population dynamics of a particular species has been underestimated, is a moot point. Be that as it may, it is a fact that a large proportion of a temperate or polar insect's life cycle is spent in the overwintering stage and recent work within allied groups, e.g. red spider mite, and within insect groups such as the Aphidoidea, has highlighted the advantages, in terms of control and prediction, to be gained from a detailed knowledge of insect overwintering habits. The contents in each chapter of this book have been largely determined by the availability of published work and by what we have considered to be the more important aspects of this subject. However, we have included previously unpublished material in an attempt to make this a comprehensive and enlightening addition to the field. The over- wintering habits of some insect groups have been largely ignored by the entomological world and we have tried, where possible, to point out areas where future research would be profitable. One of the great problems that has hampered the study of overwintering in insects has been as Danks (1978) points out, the tendency of researchers to consider ecology and physiology as two separate and unrelated disciplines. We have tried wherever possible to adopt an ecological and physiological approach to the problem and feel that by so doing, we have thrown new light on this subject. We hope that this book, by emphasising the importance of insect overwintering, will induce other entomologists to pay more attention ix x Foreword to this fascinating phase of the insect life cycle. We have thus aimed the contents of the book at postgraduate entomologists in all stages of their careers. However, we hope that this will not deter the more advanced undergraduate from finding something of interest within these pages. S. R. Leather K. F. A. Walters J. S. Bale 1992 1 Introduction Although most insects in temperate climates spend a large proportion of their life in an overwintering stage (the small willow aphid, Aphis farinosa (Gmelin) (Homoptera: Aphididae), for example, spends 75 per cent of the year as an egg) the study of insect overwintering has, in many cases, been surprisingly neglected. Perhaps this is a reflection of the fact that many entomologists, like the majority of the insects they study, spend the long cold winter months carefully insulated from the outside world! Why study overwintering? The vast majority of the prodigious amount of literature concerning insects, and particularly the literature concerning those insects of econo- mic importance (with which this book is mainly concerned) details investigations of the summer stages of the life cycle. This is, of course, understandable - the insects are present in large numbers during the summer (generally in the multiplicative stage of the life cycle) and this is, in general, the time when the damage to the crop becomes apparent. In addition, the majority of control measures are applied at or just before this time of the year. However, it is a sometimes forgotten fact that the size of the insect populations entering the overwintering stages, and the subsequent survival of these stages, play a major part in determining the population levels encountered in the following spring and summer. Although it has been stated that the literature on overwintering is extensive (Danks 1978), it has too often been of a superficial nature or confined to one specific area, generally that of cold-hardiness. Further, relatively few attempts have been made to correlate the ecological information gained from field studies with the results of physiological and 2 Introduction biochemical investigations normally conducted in the laboratory. This is a serious fault and should be remedied. Recent work within allied groups, e.g. red spider mite, and within insect groups such as the Aphidoidea, has highlighted the advantages, in terms of control and prediction, to be gained from a detailed knowledge of overwintering habits. For example, the number of overwintering eggs of the aphids Aphis fabae Scopoli. and Rhopalosiphum padi (L.) (Homop- tera: Aphididae) can be used to forecast the summer populations of these species developing on field beans in England and on cereals in Finland, respectively (Way et al. 1981; Leather 1983). In addition, the spread of potato leaf roll virus can be predicted from a knowledge of the over- wintering habits of its aphid vectors (Turl 1983). In the field of forest entomology, the numbers of overwintering pupae of the pine beauty moth, Panolis flammea (D & S) (Lepidoptera: Noctuidae), and the pine looper moth, Bupalus piniaria (L.) (Lepidoptera: Geometridae), can be used to predict the need for control measures in the coming season (Stoakley 1977; Bevan and Brown 1978). There are many other similar examples, and these will be dealt with in greater detail later (see Chapter 6). There are also many examples where a knowledge of the overwintering biology of an insect would be advantageous, and some of these are pointed out. The study of insect overwintering habits is thus of great importance to entomologists. What is overwintering? This may at first seem a relatively simplistic question to pose, and one that may be answered just as simplistically as 'the way that an organism passes the winter'. However, this does not get us very far. Many different definitions of overwintering have been suggested, illustrating the com- plexity of the subject. Mansingh (1971) considers overwintering in his discussion of dormancy under the heading of hibernation. He defines insect hibernation as 'a physiological condition of growth retardation or arrest, primarily designed to overcome lower than optimum temperatures during winter or summer'. He goes on to point out that overwintering insects also have to contend with the other adversities associated with winter conditions. The main difference between hibernating insects and active ones is that the optimum body temperatures of the former are lower, which leads to torpidity and other metabolic changes.