Biology of Insect Eggs IN THREE VOLUMES H. E. HINTON, F.R.S. Late Professor and Head of the Department of Zoology, University of Bristol Volume I PERGAMON PRESS OXFORD · NEW YORK · TORONTO · SYDNEY · PARIS · FRANKFURT U.K. Perganion Press Ltd., Headington Hill Hall, Oxford OX3 OB W, England U.S.A. Perganion Press Inc., Maxwell House, Fairview Park, Elmsford, New York 10523, U.S.A. CANADA Pergamon of Canada, Suite 104, 150 Consumers Road, Willowdale, Ontario M2J 1P9, Canada AUSTRALIA Perganion Press (Aust.) Pty. Ltd., P.O. Box 544, Potts Point, N.S.W. 2011, Australia FRANCE Perganion Press SARL, 24 rue des Ecoles, 75240 Paris, Cedex 05, France FEDERAL REPUBLIC Pergainon Press GmbH, 6242 Kronberg-Taunus, OF GERMANY Hamnierweg 6, Federal Republic of Germany Copyright 0 1981 Pergamon Press Ltd. All R<@s Reserved. No part of this piddication way 6e reprodirced, stored in a retrieval system or transnritted in anyform or by any means: electronic, electrostatic, tnagtretic tape, tnerlranical, photocopying, recording or otkeriuise, tvitlioiit perinission in writing front the pii6lishers First edition 1981 British Library Cataloguing in Publication Data Hinton, Howard Everest Biology of insect eggs. 1. Insects - Eggs I. Title 595.7’03’34 QL495.5 77-30390 ISBN 0-08-021539-4 Prirrtrd in Great Britain by A. Wheatrun G Cu. Ltd, Exeter Introductory Note HOWARD HINTON died soon after he had received the first proofs of Volume I of Biology of Insect Eggs. During his final illness I agreed that, should he not be able to see the book to publication, I would take on the job. The task has only been made possible through the knowledge, skills, and unstinting efforts of Mrs. Joyce Ablett, who worked as his assistant for many years. It is to her that we, his colleagues, friends, and fellow scientists, owe an immense debt of gratitude. I hope that our efforts will have done justice to Howard Hinton's last and greatest publication—a work which I am sure will be a fitting memorial to the life and work of one of the world's most eminent entomologists. COLIN MAPES v Appreciation Professor Howard Everest Hinton, F.R.S. (1912-77) PRODIGIOUS is an adjective that comes readily to mind in association with Howard Hinton: for it aptly describes his knowledge of entomology, the energy he displayed in his en­ tomological work, and his output of publications. His death on the eve of his retirement has undoubtedly robbed us of many contributions. His familiarity with insects was such that he could range over the whole field : one never knew where he would strike next and, like lightning again, he was always illuminating, even if he sometimes scorched those nearby ! Born in Mexico, on 24th August 1912, where his father was a mining engineer and a competent amateur botanist, he attended the Berkeley campus of the University of California, graduating in 1934. Every summer vacation was devoted to entomological expeditions: in 1930 and 1931 to the Rocky Mountains and in 1932, 1933, and 1934 to Central Mexico. The late R. L. ("Bob") Usinger was a contemporary at Berkeley and in his autobiography (Mem. Pacific Coast. Ent. Soc. 4) recalls how Hinton invited him to join the 1933 expedition. With a total budget of $110 every economy was necessary, including riding on freight trains where robbery was an ever-present danger. "However," Usinger wrote, "Howard Hinton had been a boxer at Modesto Junior College so he seemed quite confident of his ability to defend us in case of need." The thousands of insects collected on these expedi­ tions led to a flood of papers on the taxonomy of Coleoptera : some seventeen had been published by the end of his graduation year. Moving to Cambridge, where he sub­ sequently held the Junior Curatorship in the Museum of Zoology, Hinton continued his studies on the Coleoptera, and utilized internal anatomy along with more traditional evidence in his study of the classification of the Dryopoidea (for which he was awarded his Ph.D. in 1939). Characteristically he had not remained continuously working in the Museum at Cambridge, but during this time had participated in expeditions to the Caribbean and to Latin America, including the Titicaca Expedition, where his fluent Spanish enabled him to serve as interpreter. When discussing entomological problems with Howard Hinton one was continually made aware of the impact on him of this intense exposure to the rich neotropical fauna. His thinking always stressed evolutionary adaptation and he strove to find the selective pressures for the bizarre forms, behaviour, and diversity that he had seen himself in nature. Field work, to be useful, demands sound taxonomy and, as Hinton himself always stressed, this is dependent on a proper understanding of functional morphology. In his wartime studies on stored products pests, whilst on the staff of the British Museum (Natural History), he brought morphology to the solution of practical problems in the identification of the vu Vili APPRECIATION stored products pests : the larvae of Lepidoptera and the Coleoptera. The continued utility of his system of chaetotaxy for larval Lepidoptera, of his book A Monograph of Beetles Associated with Stored Products (1945) (of which, sadly, only Vol. I was published), and of his booklets on stored products pests (some of which have been translated into Chinese) are evidence of the thoroughness of this work. The next phase of his entomological activity was heralded in 1946 by a letter in Nature, "Concealed phases in the metamorphosis of Insects", pointing out that the outer covering was not a true guide to the stage of the insect: a new cuticle was formed on the epidermis at "apolysis" with the result that, for example, the "pharate" adult was hidden within the pupa. These studies led Hinton to develop a formidable knowledge of insect physiology and into controversy, both overtly (e.g. Trans. Soc. Brit. Ent. 13:19 andj. Ent. [A] 48: 57-68) and through editorial strictures on contributors to the Journal of Insect Physiology. One might say that although the "apolysis" of this phase of Hinton's work was in 1946, his "ecdysis" was not until 1949 when he joined the Zoology Department at Bristol Uni­ versity. Here his studies could range freely throughout the problems of entomology ; he was promoted Reader in 1951 and Professor in 1964. Field observations on habits and laboratory observations on structure (recently made at all hours of the day and night on the scanning electron microscope) caused him to question and probe the relations of structure and function and so contributed fundamental work on dormancy, respiratory mechanisms, protective devices, especially coloration, and eggs. The present volumes exemplify his work and bring together an encyclopaedic treatment of the diversity and detail of this hitherto largely neglected stage, with Hinton's original insights on functional significance. His work in all these topics has been a powerful stimulus to others ; the novelty of many of his ideas, together with their trenchant presentation, have been as arresting and refreshing as the titles of some of his papers, e.g. "How some insects, especially egg stages, avoid drowning when it rains". Howard Hinton never minded taking on the "Establishment"; in fact, he appeared to enjoy it. When he and his work became part of the "accepted view", he seemed to find it difficult to adjust: he had no patience with those who accepted his views uncritically. However, unknown to most, he would spend much time "behind the scenes" seeking to help a young entomologist. He was formidable in scientific polemics, but was liable to be right. For instance, in 1951 he claimed, at a meeting of the Royal Entomological Society, that his studies on Elmid and Dryopid beetles showed that continental drift must have occurred: he was followed by the then President of the Geological Society, who said that the geological consequences of assuming this were "quite untenable"! With his wide knowledge of the "unusual" structure or habit, Hinton's observations were of interest to all entomologists ; in the immediate post-war years few meetings of either the Royal or the "South London" (now the British) Entomological Societies passed without him exhibiting and commenting upon some fascinating specimen. He served both Societies as their President; the R.E.S. in 1969-70 and the "British" in its centenary year, 1972. He was elected a Fellow of the Royal Society in 1961. Howard Hinton as a man had as many and varied facets as his knowledge of entomology. He and his wife Margaret always made colleagues welcome at their home; there he would show them his miniature zoo of small mammals and reptiles, about which he would speak with great enthusiasm and knowledge. The inmates of the zoo would sometimes accompany him on his journeys and, at formal dinners, he delighted in producing from his pocket a APPRECIATION ix sock, out of which crawled a "horned toad"! With A. M. S. Dunn he wrote a definitive work on Mongooses. The active contributions of Howard Hinton to entomology have been brought to an untimely end with his death on 2nd August 1977, but we may be sure that his work, ideas, and example will continue to illuminate many aspects of the subject for decades ahead. T. R. E. SOUTHWOOD Acknowledgements THESE three volumes on the biology of insect eggs could not have been written without the help of a great many people. Mrs. Joyce Ablett did much of the printing of the scanning electron micrographs that I took to make the 155 plates. The Species Index in the third volume has been almost entirely done by Mrs. Ablett. Most of my specimens for the SEM were coated by Dr. J. W. Heavens and Mr. G. Parton. I am particularly grateful to Dr. Heavens who taught me how to change the filament and do minor repairs to the instru­ ment, which for several years enabled me to work during the night when I was free of other duties. Some of my negatives were printed by Mr. J. K. Wood. Many have assisted with typing the volumes, and I would especially thank Mrs. C. Tilley and Miss S. Eden. Eggs have been given or lent to me by the following: Mr. R. S. Baiter, Mr. E. B. Basden, Dr. P. B. Carne, Prof. F. M. Carpenter, Dr. J. Chemsak, Dr. R. H. Cobben, Mr. E. A. J. Duffy, Mr. E. C. Dyte, Dr. J. W. Evans, Mr. E. A. Fonseca, Mr. E. A. Gardner, Prof. S. M. Hammad, Dr. J. C. Hartley, Dr. E. A. Heinrichs, Dr. D. Kendall, Dr. D. C. R. Lincoln, Mr. R. I. Lorimer, Miss M. MacKay, Dr. P. F. Mattingly, Dr. W. C. McGuffin, Dr. M. D. Murray, Dr. K. Norris, Dr. A. Peterson, Dr. R. C. Rentz, Dr. B. Russev, Dr. B. J. Selman, Dr. K. G. Smith, Prof. T. R. E. Southwood. I am grateful to Dr. Miriam Rothschild for the four micrographs on Plate 100. Dr. W. A. Rowley gave me the two micrographs of Diabrotica reproduced in the second volume. Mrs. H. Roberts produced the figures from which Table 32, Vol. II is compiled. Dr. B. Henning gave me some useful information about the structure of the shell of Haplothrips. Dr. A. C. Neville lent me many useful reprints and helped me to understand the hélicoïdal microfibrils of the chorion of Lepidoptera. Dr. N. Waloff very kindly translated a number of keys from Russian. Permission to reproduce some of their illustrations has been given to me by Dr. R. R. Askew, Dr. J. S. Berry, Dr. Ellinor Bro Larsen, Dr. R. F. Chapman, Dr. R. H. Cobben, Dr. C. Degrange, Dr. G. Halffter, Dr. J. C. Hartley, Dr. D. C. R. Lincoln, Dr. M. D. Murray, and Prof. E. O. Wilson. I wish to thank especially Dr. Cobben and Dr. Lincoln, many of whose drawings have been used in the first and second volumes. XXIV 1. Introduction IT proved unexpectedly difficult to decide what should or should not be included in a work on the biology of insect eggs, and in the event I ended by pleasing myself. Embryology was excluded because very extensive reviews of the embryology of insects have appeared fairly recently (Anderson, 1972a, b). I had intended to produce only one volume, but so much material accumulated that rather than have one enormous and cumbersome volume it was decided to have three more easily handled ones. The first volume contains matters of general interest. The second volume con­ tains a little general material—the structure of the female reproductive system, vitello- genesis, and the development of the micropylar complex—but it is chiefly an account of the eggs of each order of insects. The third volume is the index to subjects, species, and the bibliography, which contains over 4000 entries. I have been much exercised about the references. Many of them are trivial. To distinguish between the trivial and the more important ones not only seemed invidious but was often very difficult. But there is an im­ portant reason for including a large number of references. Apart from centres of learning in highly industrialized countries, workers in most parts of the world have access to only a minute fragment of the scientific literature. It therefore seemed best to give many refe­ rences to each particular topic so that a worker far from a large library might at least be able to find some relevant paper, even if perhaps not a very important one. This work was handed to the publisher when it reached such proportions that no sooner was one chapter revised than another had become out of date. In the pages that follow a number of controversial points are discussed briefly in order that the reader may understand what is being said in parts of the first and second volumes. Size of eggs The question of the size of the eggs of exopterygotes as compared with those of endo- pterygotes has unfortunately become almost inextricably entangled with a very different matter : the basic differences between the exo- and endopterygote insects. The exopterygote insects are supposed to have large eggs with much yolk and therefore develop within the shell into a form resembling that of the parents. The endopterygotes, on the other hand, are supposed to have small eggs with little yolk and therefore hatch in an undeveloped form that does not resemble that of their parents. The larvae of the endopterygotes are thought of by many as precocious embryos. The pupal stage of the endopterygotes is homologized with the so-called nymphal stage of the exopterygotes (Fig. 1). Some writers explicitly state that the nymphal stages of the 1 BIOLOGY OF INSECT EGGS 2 adult adult adult adult adult adult adult (pupa) larva larva larva > pupa larva larva larva larva larva larva larva » larva larva » larva larva ■ » larva Hemimetabola Holometabola Hemimetabola Holometabola Hemimetabola Holometabola Berlese Poyarkoff Hinton Fig. 1. Diagram showing the relationships between the theories o fBerlese & Imms, Poyarkoff, and Hinton. exopterygotes have become by a process of tachygenesis the pupal stage of the endoptery- gotes, e.g. Imms (1931, p. 59) says: "... the pupa, along with the antecedent prepupa, are the ontogenetic counterparts of the nymphal instars of the lower orders of insects. It seems that tachygenesis, or shortening of development, has resulted to the extent that the whole series of nymphal instars has become concentrated into these two stages, with the elimination of the intervening ecdysis." It may be noted that the prepupa of Imms is thepharate pupa and not a distinct instar. INTRODUCTION 3 The larvae of the exopterygotes were called nymphs (the French word for pupa) for no other reason than that people thought they were homologous with the pupa of the endo- pterygotes. And this homology was well established in the minds of many long before the time of Berlese and Imms. It is common to find writers in the middle 19th century using the phrase "nymph or pupa" when referring to the larvae of the exopterygotes. A summary of the history of this mistake has recently been given (Hinton, 1976c). As early as 1651 William Harvey said that it was the lack of food reserves in insect eggs that caused what he called their premature birth. Only 18 years later, Swammerdam (1669) in his Biblia Naturae cor­ rectly pointed out that the eggs of higher insects such as beetles, butterflies, and bees are not notably more deficient in yolk than those ofLepisma or grasshoppers. Swammerdam excused the mistake of Harvey on the grounds that insects are difficult to study "unless by persons accustomed to experiments of this kind; it is no wonder that the most happy geniuses, the immortal Harvey, for example, and many others have fallen into error." Harvey's idea is restated by Lubbock (1874, p. 8Q) as-follows: "That the occurrence of metamorphosis arises from the immaturity of the condition in which some animals quit the eggs." Writers who hold views like those of Lubbock cannot be found guilty of looking closely at the larvae of the endopterygotes : the structures of these larvae are very often extremely specialized as compared with those of the exopterygotes. The maggot of a blowfly is not an apodous larva that has hatched in an early embryonic stage from an egg with little yolk. It is, on the contrary, an extremely specialized larva that has hatched from an egg with plenty of yolk: it is secondarily and not primitively apodous. Its mouth parts are as specialized as any. The cardiostipes has become fused with the.dististipes, as in some Nematocera (e.g. Culi- cidae), and these remains of the maxilla are fused to the mandibles to form the characteristic mouthhooks of the Diptera-Cyclorrhapha (review in Hinton, 1958). Thus a maggot, as com­ pared with the larva of a cockroach, is much more highly specialized and less primitive, which is the opposite of what is generally claimed. In a broad general way, allowing for many exceptions, it is possible to distinguish three phases in the development of embryonic appendages. The appendages of the head appear first and are followed by the thoracic and a little later by the abdominal. The appearance of the abdominal appendages marks the end of the protopod and the beginning of the polypod phase. The polypod phase passes into the oligopod when the metamerie abdominal appen­ dages are absorbed. According to Berlese (1913) and Imms (1937), the forms of the chief kinds of larvae are determined by the times of hatching. They claim that the larvae of the exopterygotes, which they call nymphs, have hatched, because of the greater amount of yolk in the egg, in a post-oligopod phase, whereas the larvae of sawflies, Mecoptera, and Lepi- doptera have emerged from the egg in a polypod phase because they have less yolk in the egg. I do not think that the anti-selectionist nature of this way of looking at the evolution of insect larvae has ever been adequately exposed. Berlese and his followers, like Lubbock and William Harvey before them, claim that it is the relative amount of yolk in the egg that determines the embryonic phase in which the larva hatches. This and similar theories explicitly state that the abdominal prolegs of endo- pterygote larvae are serially homologous with the thoracic legs, a view already rejected by Deegener (1909) and many others. Prolegs are secondarily adaptive organs that have been evolved time and again in the endopterygotes (review in Hinton, 1955b) and some have more than one pair of prolegs on a single metamere. In the Diptera alone, prolegs have been independently evolved at least 27 times (Hinton, 1955b). Matsuda (1976) has revived the