The Physiology of Insecta: Volume III

THE PHYSIOLOGY OF INSECTA

Volume III

Second Edition

MORRIS ROCKSTEIN

Department of Physiology and Biophysics, University of Miami School of Medicine, Miami, Florida

Table of Contents

Cover image

Title page

CONTRIBUTORS

Copyright

LIST OF CONTRIBUTORS

PREFACE

PREFACE TO FIRST EDITION

CONTENTS OF OTHER VOLUMES

Part A: The Insect and the External Environment. II. Reaction and Interaction

Chapter 1: INSECT BEHAVIOR: FUNCTIONS AND MECHANISMS

Publisher Summary

I Introduction

II Analysis of Functions*

III Analysis of Mechanisms

IV Conclusion

Chapter 2: SOCIAL BEHAVIOR AND MUTUAL COMMUNICATION

Publisher Summary

I Introduction

II Forms of Social Life

III The Organization of Higher Social Communities of Insects

IV Mutual Communication

V Communication in the Search for Food

VI Communication by Means of Dances in the Search for A New Nesting Place

VII Evolutionary Aspects

Chapter 3: INSECT PHEROMONES

Publisher Summary

I Introduction

II Sex Pheromones

B PERCEPTION AND RESPONSE

III Aggregation Pheromones

IV Alarm Pheromones

V Trail-Marking Pheromones

VI Pheromones Controlling Sexual Maturity

VII Pheromones Controlling Queen Rearing

Part B: The Insect and the External Environment. III. Locomotion

Chapter 4: INSECT MIGRATION: ASPECTS OF ITS PHYSIOLOGY

Publisher Summary

I Introduction

II Exodus from the Breeding Site

III Migratory Flight

IV Orientation during Migration

V Migrants and Polymorphism of the Flight Apparatus

VI Conclusion

Chapter 5: LOCOMOTION: TERRESTRIAL

Publisher Summary

I Introduction

II Morphology

III Performance

VI Walking and Running

V Jumping

VI Crawling

Chapter 6: LOCOMOTION: MECHANICS AND HYDRODYNAMICS OF SWIMMING IN AQUATIC INSECTS

Publisher Summary

I Introduction

II The Body Shape of Dytiscidae and Gyrinidae

III The Rowing Mechanism of Dytiscidae, Gyrinidae, and Corixidae

C KINEMATICS

D DYNAMICS

IV The Rowing Mechanism of Other Aquatic Insects

V The Propulsion System of Narrowing Aquatic Insects

Chapter 7: LOCOMOTION: FLIGHT

Publisher Summary

I Introduction

II Structure and Mechanical Properties of the Pterothorax

III The Flight Motor

IV Flight Characteristics

V The Control of Flight

VI The Flight Muscles

Acknowledgement

AUTHOR INDEX

SUBJECT INDEX

CONTRIBUTORS

G.M. HUGHES

MARTIN JACOBSON

C.G. JOHNSON

MARTIN LINDAUER

HUBERT MARKL

P.J. MILL

WERNER NACHTIGALL

J.W.S. PRINGLE

Copyright

COPYRIGHT © 1974, BY ACADEMIC PRESS, INC.

ALL RIGHTS RESERVED.

NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER.

ACADEMIC PRESS, INC.

111 Fifth Avenue, New York, New York 10003

United Kingdom Edition published by

ACADEMIC PRESS, INC. (LONDON) LTD.

24/28 Oval Road, London NW1

Library of Congress Cataloging in Publication Data

Rockstein, Morris, ed.

The physiology of Insecta.

Includes bibliographies.

1. Insects-Physiology. I. Title.

QL495.R58 1973 595.7′01 72-9986

ISBN 0-12-591603-5 (v. 3)

PRINTED IN THE UNITED STATES OF AMERICA

LIST OF CONTRIBUTORS

Numbers in parentheses indicate the pages on which the authors’ contributions begin.

G.M. HUGHES,     (335), Research Unit for Comparative Animal Respiration, The University of Bristol, Bristol, England

MARTIN JACOBSON*,     (229), Entomology Research Division, U. S. Department of Agriculture, Beltsville, Maryland

C.G. JOHNSON,     (279), O. D. A. Lethal Yellowing Team, Coconut Industry Board, Kingston, Jamaica

MARTIN LINDAUER†,     (149), Zoologisches Institut der Universität, Frankfurt am Main, Germany

HUBERT MARKL,     (3), Fachbereich Biologie, Technische Hochschule, Darmstädt, Germany

P.J. MILL,     (335), Department of Pure and Applied Zoology, The University of Leeds, Leeds, England

WERNER NACHTIGALL,     (381), Zoologisches Institut der Universität des Saarlandes, Saarbrucken, Germany

J.W.S. PRINGLE,     (443), Department of Zoology, Oxford University, Oxford, England

*Present address: Agricultural Environmental Quality Institute, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Maryland.

†Present address: Zoologisches Institut (II) der Universität, Würzburg, Germany.

PREFACE

Since the first edition of this multivolume treatise appeared, well over eight years ago, there has been a notable expansion of scientific endeavor in each of the now numerous aspects of insect physiology. Accordingly, revising this major reference work has been a challenging undertaking both to the original authors as well as to the several new contributors in areas in which the growth of research and, therefore, the relevant body of knowledge has grown so much as to warrant such additional coverage. Consequently, the original three-volume work has now grown like Topsy to a thoroughly revised six-volume work.

Thus, Volume II included two entirely new and distinct chapters on Radiation and on Circadian Rhythms and Photoperiodism in Insects. This volume includes a new chapter on Insect Pheromones by Dr. M. Jacobson. Subsequent volumes will include new chapters on The Pharmacology of the Insect Nervous System, Protein Synthesis in Insects, and Microsomal Mixed-Function Oxidases. The Physiology of Insect Behavior, originally covered in a single chapter by Professors Markl and Lindauer, has been expanded in this volume to two distinct chapters; one by Professor Markl covers the actual mechanisms of insect behavior and the second by Professor Lindauer social behavior and mutual communication.

Similarly, the Physiology of Circulation in Insects, formerly covered in one chapter by Dr. Jack Jones, has now been subdivided into three individual chapters in Volume V: one on Circulation by Dr. Jones, one on Electrophysiology of the Insect Heart by Dr. Thomas A. Miller, and one on Hemocytes of Insects by Dr. J. W. Arnold. The original chapter on Respiration in Insects by Dr. P. L. Miller has been expanded into two: Respiration: Aerial Gas Transport by Dr. P. L. Miller and Respiration: Aquatic Insects by Dr. P. J. Mill.

Once again, I am deeply indebted to my former teacher and mentor, Professor A. Glenn Richards, whose criticism and suggestions concerning the first edition have assisted me immeasurably in my endeavor to improve both the content and scope of this, the second edition.

I am especially grateful to Mrs. Estella Cooney, to Ricki Davidson, and to my daughter Susan, without whose technical and editorial assistance (under the stress of exacting technical standards which a work of this nature demands) the completion of this volume would have been impossible. Once more also, the cooperation and concern for quality of content and accuracy by each of the authors of the various chapters must be recognized with appreciation.

Finally, I cannot overemphasize the important roles played by the staff of Academic Press, in their unfailing encouragement, cooperation and tactical assistance throughout the planning and the ultimate completion of the collation of the various components of this, the second edition of The Physiology of Insecta.

MORRIS ROCKSTEIN

PREFACE TO FIRST EDITION

This multivolume treatise brings together the known facts, the controversial material, and the many still unsolved and unsettled problems of insect physiology in chapters written by the outstanding workers in each of a wide range of areas of insect function.

It is designed to meet a manifest need which has arisen from the phenomenal increase in research activity on insects (during the past two decades, especially) for an authoritative, comprehensive reference work in insect physiology.

Although the insect physiologist usually considers himself either a comparative physiologist or a general physiologist studying a particular process in insects, the fact is that each is a biologist whose primary interest is in the total organism in relation to a specific function. This viewpoint is reflected in the organization and arrangement of the chapters by section and volumes. Thus, instead of that classic arrangement of chapters which emphasizes organ or systemic physiology, this treatise has been organized into three main sections, each covering a major division of insect biology: the ontogeny of insects from reproduction to senescence of the individual; the insect’s perception of and reaction to its external environment; and the mechanisms by which the internal homeostatic state is maintained. The last-mentioned division, especially, includes many classic functions—from the role of the nervous system to nutrition, metabolism, respiration, circulation, maintenance of salt and water balance, and cuticular functions. In addition, under this major division the heretofore unemphasized areas of immunological responses and mechanisms of insect resistance to insecticides have been included, since the contributions of research investigators to these fields in recent times are widely recognized.

I hope that this diversified subject matter will serve an equally varied group of students of biology. To the student of comparative physiology as well as to the entomologist, the organization of the now extensive literature on insect physiology into one large work should be especially useful. To the applied entomologist, the chapters concerned with insect functions in relation to the external environment should prove especially interesting; they provide a basis for understanding the distribution, epidemiology, and bionomics of insects in general, but especially of those insects of medical and economic importance. Those chapters concerned with the maintenance of the constancy of the internal environment should be equally helpful, forming a rational basis for control of insect pests. Finally, the details of structure, both gross and histological, necessarily included in those chapters covering neurophysiology, circulation, respiration, digestion, and cuticular functions, should be of special interest to the anatomist or taxonomist concerned with the physiological implications of his own research interests in insects.

The responsibilities of editing an opus of this size include securing the complete cooperation and sustained efforts of one’s co-authors. To this I can attest without qualification. I must also acknowledge the critical, but always helpful suggestions—especially in the early planning and in the reading of some of the manuscripts—of my many colleagues, namely, Dr. A. Glenn Richards, Dr. V. B. Wigglesworth, Dr. Carroll M. Williams, Dr. Leigh E. Chadwick, Dr. Vincent G. Dethier, Dr. Herbert H. Ross, Dr. Curtis W. Sabrosky, and the late Dr. R. N. Snodgrass.

To Miss Norma Moskovitz, special expression of appreciation is due for her untiring efforts and sustained dedication to achieving a final product of exacting technical standards.

On a more personal level, the early encouragement of the late Elaine S. Rockstein and the patience and forbearance of my ofttimes neglected daughters Susan and Madelaine, especially during the past year, must be gratefully acknowledged as well.

MORRIS ROCKSTEIN

CONTENTS OF OTHER VOLUMES

Volume I

Physiology of Ontogeny—Biology, Development, and Aging

BIOLOGY OF THE INSECTA

Morris Rockstein

REPRODUCTION

Jan de Wilde and Arnold de Loof

REPRODUCTION—ENDOCRINE CONTROL

Jan de Wilde and Arnold de Loof

PHYSIOLOGICAL AND BIOCHEMICAL CHANGES DURING INSECT DEVELOPMENT

Ivar P. S. Agrell and Anders M. Lundquist

PHYSIOLOGY OF GROWTH AND DEVELOPMENT: ENDOCRINE ASPECTS

Lawrence I. Gilbert and David Shaw King

AGING IN INSECTS

Morris Rockstein and Jaime Miquel

AUTHOR INDEX–SUBJECT INDEX

Volume II

PART A

The Insect and the External Environment. I. Environmental Aspects

ENVIRONMENTAL ASPECTS–TEMPERATURE

E. Bursell

ENVIRONMENTAL ASPECTS–HUMIDITY

E. Bursell

ENVIRONMENTAL ASPECTS—RADIATION

Daniel S. Grosch

PART B

The Insect and the External Environment. II. Reaction and Interaction

CHEMORECEPTION

E. S. Hodgson

THE VISUAL SYSTEM OF INSECTS

Timothy H. Goldsmith and Gary D. Bernard

MECHANORECEPTION

J . Schwartzkopff

SOUND PRODUCTION

P. T. Haskell

INSECT BIOLUMINESCENCE

W. D. McElroy, H. H. Seliger, and M. DeLuca

CIRCADIAN RHYTHMS AND PHOTOPERIODISM IN INSECTS

D. S. Saunders

AUTHOR INDEX–SUBJECT INDEX

Volume IV

The Insect and the Internal Environment—Homeostasis I

NEURAL INTEGRATION (CENTRAL NERVOUS SYSTEM)

F. Huber

THE PHARMACOLOGY OF THE INSECT NERVOUS SYSTEM

Yves Pichon

NEURAL CONTROL OF SKELETAL MUSCLE

G. Hoyle

THE BIOCHEMISTRY OF THE CONTRACTILE ELEMENTS OF INSECT MUSCLE

K. Maruyama

BIOLOGICAL OXIDATIONS AND ENERGETICS IN INSECT MILTOCHONDRIA

B. Sacktor

PROTEIN SYNTHESIS IN INSECTS

J . Ilan and J. Ilan

AUTHOR INDEX—SUBJECT INDEX

Volume V

The Insect and the Internal Environment—Homeostasis II

NUTRITION

H. L. House

DIGESTION

H. L. House

FACTORS AFFECTING HEART RATES IN INSECTS

Jack Colvard Jones

ELECTROPHYSIOLOGY OF THE INSECT HEART

Thomas A. Miller

THE HEMOCYTES OF INSECTS

John W. Arnold

HEMOLYMPH: COMPOSITION

Marcel Florkin and Charles Jeuniaux

HEMOLYMPH COAGULATION

Ch. Gregoire

SALT AND WATER BALANCE EXCRETION

R. H. Stobbart and J. Shaw

INSECT DEFENSE MECHANISMS AGAINST MICROORGANISMS AND PARASITOIDS

Robert F. Whitcomb, Martin Shapiro, and Robert R. Granados

MICROSOMAL MIXED-FUNCTION OXIDASES

Moises Agosin and Albert S. Perry

AUTHOR INDEX–SUBJECT INDEX

Volume VI

The Insect and the Internal Environment—Homestasis III

THE PHYSIOLOGY OF INSECTICIDE RESISTANCE BY INSECTS

Albert S. Perry and Moises Agosin

The Structure and Formation of the Integument in Insects

Michael Locke

CHEMISTRY OF THE INSECT CUTICLE

R. H. Hackman

PERMEABILITY OF INSECT CUTICLE

W. Ebling

RESPIRATION: AERIAL GAS TRANSPORT

P. L. Miller

RESPIRATION IN AQUATIC INSECTS

P. J . Mill

RESPIRATION: SOME EXOGENOUS AND ENDOGENOUS EFFECTS ON RATE OF RESPIRATION

Margaret Keister and John Buck

AUTHOR INDEX–SUBJECT INDEX

Part A

The Insect and the External Environment. II. Reaction and Interaction

Outline

Chapter 1: INSECT BEHAVIOR: FUNCTIONS AND MECHANISMS

Chapter 2: SOCIAL BEHAVIOR AND MUTUAL COMMUNICATION

Chapter 3: INSECT PHEROMONES

Chapter 1

INSECT BEHAVIOR: FUNCTIONS AND MECHANISMS

Hubert Markl

Publisher Summary

Every individual has two tasks to accomplish (1) to develop its own life and sustain it and (2) to contribute to the continued existence of the species. The first demands selection of an appropriate habitat that must provide physical conditions favorable to the physiological processes and a living environment that supplies food as well as protection against damage by physical impact, parasites, or predators. The second demands the cooperation of several individuals of a species, thus, creating the necessity to communicate. Each insect species can exist only in a specifically limited range of ambient temperature, relative humidity, radiation, and other physical factors of the environment. Adaptation to highly specific sources of food, the cause of insects’ enormous radiation into innumerable species, assures each species a supply that does not fully have to be shared with its competitors. The specialization of the mouth parts and digestive tract so that energy losses during uptake and procession of food are minimized is one result, but this inevitably confronts the individual with the problem of finding, recognizing, and obtaining that very special food.

I. Introduction

II. Analysis of Functions

A. Selection of Habitat and Adjustment to the Physical Environment

B. Provisioning

C. Protection and Defense

D. Reproduction

III. Analysis of Mechanisms

A. Introductory Remarks

B. Orientation in Space and Time

C. Sources of Motivation

D. Fixed Action Patterns

E. Control of Start and Stop

F. Learning

G. Ontogeny of Behavior

H. Genetics of Behavior

I. Evolution of Behavior

IV. Conclusion

References

I Introduction

Insect behavior, obtrusive as a mosquito’s buzz, admirable as the honey bee’s perfect comb, awe-inspiring as locusts’ devastating migrations, has always been the source of amazement and curiosity for the naturalist and, consequently, the object of his scientific inquiry. Accordingly, an immense literature has accumulated. J. H. Fabre’s monumental work, studies by J. Regen, A. Faber, B. B. Fulton, W. Jacobs, and R. D. Alexander on sound communication in Orthoptera; N. Tinbergen on courtship of butterflies; G. P. Baerends, K. Tsuneki, and H. E. Evans on nesting and brood care in wasps; or W. M. Wheeler, T. C. Schneirla, and E. O. Wilson on the life of ants are just a few of the milestones in this field. Above all, von Frisch and his co-workers in several decades of work on the honey bee have opened our eyes to a plethora of behavioral accomplishments and have introduced some of the most potent tools for their scientific investigation.

In this chapter only a small, and admittedly subjective, selection of this vast material can be discussed in an effort to make the basic functions and mechanisms of insect behavior understandable. There are all kinds of books and periodicals dealing, often marginally, with insect behavior from ethological and psychological, parasitological and ecological, physiological or taxonomic points of view. No one could endeavor to survey this wealth of knowledge comprehensively or even impartially. In order not to overfreight the text with quotations, the reader is frequently referred to reviews, especially in the Annual Reviews of Entomology. Regrettable as it may seem, this bidistillation of literature becomes inevitable. No effort was made to treat behavioral aspects of the bionomics and ecology of different taxonomic groups. Finally, some important areas of insect behavior are dealt with in special chapters of this treatise and are therefore touched only briefly or not at all in this chapter. This includes behavior in relation to temperature (see Volume II, Chapter 1), humidity (see Volume II, Chapter 2), and radiation (see Volume II, Chapter 3); sensory bases of behavioral performance, as chemoreception (see Volume III, Chapter 4), photoreception (see Volume II, Chapter 5), mechanoreception (see Volume II, Chapter 6); periodic organization of behavior (see Volume II, Chapter 9); migration (see Volume III, Chapter 4); production of light (see Volume II, Chapter 8), sound (see Volume II, Chapter 7), or pheromones (see Volume III, Chapter 3) for communication; and all aspects of social behavior (see Volume III, Chapter 2). Mechanisms of locomotion, which are the basis of almost any behavior, are the subject matter of Volume III, Chapters 4–7, neural mechanisms are treated in Volume IV, Chapters 1–3, the fulfillment of food, water, and oxygen requirements in Volume V. This impressive array of cross-links demonstrates that behavior is the ultimate outcome, the final common pathway, as it were, of all components of an insect’s physiological machinery.

All study of behavior begins with the detailed description of the phenomena of observable activity and its development (ethogram). Experimental analysis then determines the necessary internal and external conditions for a specific performance. The final goal is to deduce the complex patterns of behavior from characteristics of the sensory, nervous, and motor systems of the animal. Last, but not least, the study of the biological function of an animal’s behavior pattern, its inherited and individually learned adjustment to the environment to the benefit of the propagation of the species, is indispensable if one wants to understand the selective forces that led to its existence. The comparison of homologous behavior in different taxa can finally aid in tracing the evolution of behavioral traits.

These aspects, though not in the same order, guide the following presentation.

II Analysis of Functions*

Every individual has two tasks to accomplish: (1) to develop its own life and sustain it and (2) to contribute to the continued existence of the species. The first demands selection of an appropriate habitat, which must provide physical conditions favorable to the physiological processes, and a living environment that supplies food as well as protection against damage by physical impact, parasites, or predators. The second demands the cooperation of several individuals of a species, thus creating the necessity to communicate. Finally, the offspring often require care by the parents even if only laying the eggs in a suitable selection of circumstances for the development of the larvae. Because of identical functions, similar behavior patterns serving these tasks have developed again and again in different groups of insects. We can arrange them according to functional criteria into several main types of activities.

A SELECTION OF HABITAT AND ADJUSTMENT TO THE PHYSICAL ENVIRONMENT

Each insect species can exist only in a specifically limited range of ambient temperature, relative humidity, radiation, and other physical factors of the environment. Although, as a rule, habitat selection by the parents, before depositing the eggs, ensures suitable conditions for the progeny, it may be still necessary for the individual to find and recognize its favorable microclimatological niche, since daily, lunar, tidal, annual, or arrhythmic changes of the environment as well as changing requirements during different developmental stages, impose the need to find a compromise according to the boundary conditions given by tolerance to different environmental factors. Often kinetic orientation (see Section III,B) will bring the animal to a rest where such a compromise is reached. Additional physiological and behavioral adaptations can expand the range of inhabitable biotopes: activity rhythms, adjusted to rhythmic changes in the environment, let the individual select favorable times of day or year and make it retreat to rest (for sleep in insects, see Rau and Rau, 1916; Linsley, 1962) or dormancy in a shelter during other times. Often the animal in an inactive state is less sensitive to physical influences. On the other hand, daily or seasonal migrations may enable an insect to move temporarily into an environment which is at other times uninhabitable. Synchronization of activities of conspecifics and restriction to specific times of day or year can also mitigate competition for an ecological niche common to more than one species and even help to keep sympatric sibling species isolated (e.g., Alexander and Bigelow, 1960; L. N. Brown, 1972).

Taken together, these different ways of selecting a habitat in space and time are basic to the proper working of all other physiological, ecological, and behavioral adaptations of a species. Its correct performance must be assured through the genetic endowment, consisting of a specific program for the development of sensory organs, nervous system, and motor machine, whose response and activity characteristics fit the basic needs for the existence of the species.

B PROVISIONING

There seems to be hardly a source of organic carbon which is not used at least to a certain extent as food for some insects. Roughly, one may separate phytophagous from carnivorous, saprophagous, and parasitic insects. Adaptation to highly specific sources of food, the cause of insects’ enormous radiation into innumerable species, assures each species a supply which does not fully have to be shared with its competitors. Specialization of its mouth parts and digestive tract so that energy losses during uptake and procession of food are minimized is one result, but this inevitably confronts the individual with the problem of finding, recognizing, and obtaining that very special food. If, as is typical for many holometabolous insects, larvae are specialized for different food than adults, these problems are multiplied. Usually they are primarily overcome by that most primitive, but nevertheless indispensable service of brood care, which most females provide by depositing their eggs on or close to the food source of their offspring. However, this puts into the hands of the imago the dual problem of locating both its own food and that which is wholesome to its progeny.

In those insects which have to take up water in order to regulate the osmotic concentration of their hemolymph, recognition and control of water uptake is not principally a different problem than it is for other foodstuffs. Behavior to provide and regulate the oxygen supply (breathing), a rather simple neurogenous activity rhythm in insects living in the open air (Chapter 5, Volume VI), can be quite complex in aquatic forms (Chapter 6, Volume VI), which often actively or passively (physical gills) have to collect the gas into a store. Access to air can be gained as shrewedly as in larvae of some Coleoptera (e.g., Donacia) and Diptera, which suck it out of the aerenchyme of water plants (Deibel, 1911; Ege, 1915a,b; Varley, 1939).

1 Phytophagous Insects

While phytophagous larvae of many insects have little difficulty in finding food plants because the eggs had been fastened to them by the mother, simple cues must be provided in other cases so that the first instar larva, with its primitive sense organs, can identify the food plant. Argynnis females deposit their eggs on tree trunks, only after they have confirmed the presence of Viola plants in the close vicinity, by means of tarsal chemoreceptors. Descending from the tree, the caterpillars have a good chance to crawl over their food plants (Magnus, 1950). For recognition of food plants from some distance, olfactory and visual stimuli are used; for final identification, gustatory and mechanical ones are used.

Visual cues even of the simplest kind can allow surprisingly selective attraction. Vanessa caterpillars are induced to climb stinging nettles by their odor and the dark-patched pattern of their leaves as seen against the sky (Götz, 1936). Lymantria caterpillars are attracted by vertical stripes which contrast darkly against the background; in the field this leads them to tree trunks (Hundertmark, 1937a, b). This is one example of many where insects have been found to be attracted by dark, vertical patterns and thus are guided to plants. Others are stick insects (Kalmus, 1937b), in which climbing parallel to light-dark borders has also a camouflaging effect and for which Jander and Volk-Heinrichs (1970) described a visual perceptor system detecting shrubs; locusts (Williams 1954; Wallace, 1958a,b; Dadd, 1963; Mulkern, 1967), and ants (Jander and Voss, 1963; Voss, 1967) (see also Section III,E,1). That a perference for vertical contours is not universal but adapted to the requirements of the species is demonstrated by the fact that adult cockchafers (Melolontha) after eclosion fly from the open field toward the dark, horizontal silhouette formed by a forest against the horizon (Schneider, 1952, 1967; Couturier and Robert, 1958, 1962; Robert, 1963). Visual stimuli (rapid expansion of a pattern) control also the landing response in many insects (de Talens et al. 1970; Coggshall, 1971).

Reactions to more specific visual patterns, mostly combined with response to scents, is typical for most flower-visiting insects (Knoll, 1921–1926; Kugler, 1950, 1970). The odor can excite activity and lead to the approach of visually stimulating objects (Vanessa: Use, 1929; Eumenis: Tinbergen et al., 1942; Limenitis, Apatura: Lederer, 1951). On the other hand, the sight of flowers can attract from the distance, and olfactory stimuli in the close vicinity determine the actual approach to a particular flower (Apis: von Frisch, 1914, 1919; Eristalis, Bombus: Kugler, 1950; sphingids: Knoll, 1925). Some colors are approached spontaneously; others can be learned as cues, if rewarded, in honey bees (Menzel, 1967) and the butterfly, Heliconius (Swihart and Swihart, 1970; Swihart, 1971). In addition to color, many other cues of the feeding place are retained by social Hymenoptera, e.g., the shape and color pattern of a flower (von Frisch, 1914; Hertz, 1929, 1930, 1931, 1933, 1934a,b; Zerrahn, 1933; Sakagami, 1956a,b,c; Wehner and Lindauer, 1966; Wehner, 1967a,b, 1968, 1971, 1972; Schnetter, 1968; Mazochin-Porshnyakov, 1969; von Weizsäcker, 1970; Jander, et al., 1970a), its scent, and even scent pattern (von Frisch, 1919; Opfinger, 1931; Lex, 1954; von Aufsess, 1960; Martin, 1965; Kriston, 1971; Koltermann, 1969, 1970), and visual landmarks of the surrounding as well as the compass direction from the nest in relation to the sun (see Section III,B). All this enables them to become oligolectic or even flower constant: within a certain time period the collecting activity is limited to a few or only one species of flowers in a limited collecting area, which not only guarantees pollination of the flowers but is also a prerequisite for communication of a food source in honey bees (see Chapter 2 of this volume) (Knoll, 1921–1926; von Frisch, 1943; Vowles, 1955; Manning, 1957; Weaver, 1957; Free, 1960, 1970; Kugler, 1970). Bombus learns different cues, depending upon the species of food plant: with inconspiciously flowering plants it uses their form and location, with conspicuously colored ones, their color (Manning, 1956b).

The collecting activity of bees is adjusted in time to the rhythm of the nectar and pollen production of many plants (Kleber, 1935; Kerfoot, 1967). The bees are able to remember not only the place where food is offered, but also the time of day at which that occurs and what kind of food is provided then and there (Beling, 1929; Wahl, 1932, 1933; Renner, 1957; Beier, 1968; Beier and Lindauer, 1970; Koltermann, 1969, 1970).

At the flower itself, nectar guides frequently lead to the location of the nectar source; visual ones (Knoll, 1921–1926; Bolwig, 1954; Lex, 1954; Manning, 1956a; Free 1971a), especially those which are marked by strong UV reflection (Daumer, 1956, 1958), and olfactory ones (Lex, 1954; von Aufsess, 1960; Martin, 1965) have been described. (For these and other aspects of the coevolution of flowering plants and anthophilous insects, see Baker and Hurd, 1968; Free, 1970; Kugler, 1970; Heinrich and Raven, 1972.)

Olfactory information for food-plant selection is not only prominent in the flying flower visitors. Even in lepidopterous larvae it is used, though only at close range (Schoonhoven and Dethier, 1966). Terricolous insect larvae and imagos, which feed on plant roots, can be attracted by the carbon dioxide that the roots produce (Klinger, 1957, 1961; Andersen, 1931).

The range of food plants or hosts accepted by phytophagous insects is largely determined by the chemical stimuli provided by the presence of more or less specific chemical components (e.g., sugars in nectar) and the absence of others which would repel the insect. Other than suspected by Fraenkel (1959), in most cases selection does not primarily depend on nonnutritive secondary plant substances, but on a more or less wide range of constituents (Mulkern, 1967; Schoonhoven, 1968). The acceptance spectrum is ultimately determined by the combined filter properties of chemical sense organs for smell and taste stimuli; the receptors involved can be specialists as well as generalists in their response specificity (see Chapter 4 of this volume). In addition, the mechanical structure of the material must have special qualities to make it acceptable for sucking, biting, or chewing (Atta: Cherrett 1972; Barrer and Cherrett, 1972). These sensory filters are adapted so that the food plant which yields the optimal reproductive success for a species elicits maximal feeding response (for example, in aphids, Mosbacher, 1963, 1964).

Dethier et al. (1960) have proposed a terminology for the classification of chemical stimuli which affect feeding behavior; it has been further modified and expanded by Beck (1965) and Lindstedt (1971). One may distinguish between attractant, arrestant, repellant (all self-explaining), incitant (releases tasting), suppressant (inhibits tasting), stimulant (promotes ingestion and continuation of feeding), and deterrent (stops feeding). Feeding is usually a catenary process of reactions leading in a more and more specifically narrowing sequence to the consummatory end. The feeding activators among the above-mentioned factors (attractants, arrestants, incitants, and stimulants) thus are the stimuli which release one by one the next link of the chain. The existence of the different inactivators (repellents, suppressants, deterrents) makes clear that there has not only been a symbiotic coevolution between flowers and anthophilous insects, but also an antibiotic coevolution between the plants and their insect enemies (Fraenkel, 1959; Brower and Brower van Zandt, 1964; Eisner, 1964; Beck, 1965; Reichstein, 1967; Munakata, 1970; Whittaker and Feeny, 1972) (see also Section II,C,1).

Numerous examples for the chemical control of feeding in phytophagous insects may be found in the reviews by Dethier (1947), Thorsteinson (1960), Beck (1965), Jacobson (1966), Schoonhoven (1968), Wood et al. (1970), Lindstedt (1971), and Zwölfer and Harris (1971). The largest body of evidence exists for lepidopteran larvae and for flies. Different lepidopteran caterpillars have specialized receptors for water, glucose, fructose, inositol, salts, and some deterrents (Ishikawa, 1963, 1966; Ishikawa and Hirao, 1963, 1966; Schoonhoven and Dethier, 1966). Schoonhoven (1967) finds maxillary receptors of Pieris responsive to mustard-oil glycosides, the stimulant contained in host plants (David and Gardiner, 1966). These glycosides promote feeding also in Plutella (Nayar and Thorsteinson, 1963). Glycosides are also involved in Ceratomia (Nayar and Fraekel, 1962), Protoparce (Yamamoto and Fraenkel, 1963), and Lepinotarsa (Schanz, 1953; Thorsteinson, 1955; Yamamoto and Fraenkel, 1959). It has been shown that the filter spectrum of the chemoreceptors can be influenced by experience and therefore most certainly has central nervous components: Manduca and Heliothis larvae prefer a plant on which they have been fed before, even if molts occur between feeding and test (Jermy et al., 1968). Bombyx larvae feed almost exclusively on mulberry leaves. Substances eliciting the feeding response can be found in many plants. The mulberry is distinguished by the mixture and amounts contained and by the absence of feeding inactivators. These experiments, which led to a formula for an artificial diet, demonstrate that three kinds of factors have to be present: attractants (citral, linalyl acetate, linalol, terpinyl acetate), incitants (β-sitosterol, isoquercitine, and morin) and swallowing stimulants (cellulose, sugar, inositol, silica, and potassium phosphate). For a normal development of the larvae, several additional substances are necessary which are, however, without influence on the acceptability of the diet (Hamamura, 1970; Hamamura and Naito, 1961; Hamamura et al., 1962; Ito, 1960; Ishikawa, 1963, 1966, 1967; Ishikawa and Hirao, 1963, 1964, 1965, 1966; Nayar and Fraenkel, 1962; Niimura and Ito, 1964; Watanabe, 1958).

For a particularly thorough study of the feeding behavior in flies we are indebted to Dethier and his associates (Dethier, 1952, 1955, 1957, 1961, 1967; Dethier et al., 1952, 1956; Dethier and Rhoades, 1954; Dethier and Bodenstein, 1958). Food odor elicits positive anemotaxis and can thus lead a fly to a source. Whether material is ingested is under the control of taste receptors on the tarsi, the stimulation of which leads to extension of the proboscis; when the latter contacts the food solution, its consistency and taste are experienced by sensory hairs of the mouthparts outside and inside the labellum. Electrophysiological studies indicate that each labellar hair contains five sensory cells (Hodgson, 1968) : one responsive to monovalent cations (Evans and de Mellon, 1962b, Gillary, 1966), one to monovalent anions or fatty acids (Steinhardt, 1965; Dethier and Hanson, 1965), one to certain carbohydrates (pentoses, hexoses, and di- and trisaccharides with α-glucoside linkages) (Hodgson, 1957; Omand and Dethier, 1969), one to water (Evans and de Mellon, 1962a), and one to mechanical movement (Wolbarsht and Dethier, 1958). In the maximally starved fly, two spikes within 20 mseconds from one labellar sugar receptor are sufficient to trigger proboscis extension (Getting, 1971). For sucking to commence under natural conditions there must be a balance between sugar-receptor (enough) and salt-receptor (not too much) activation. Feeding inactivators can turn off the feeding response at four levels: by affecting the olfactory receptors, the tarsal taste hairs, the labellar taste hairs, and the receptor papillae of the oral surface, the latter exerting the tightest control of ingestion. Food quality, receptor adaptation, central habituation, and central control by tonic inhibitory feedback from stretch receptors in the foregut and crop (Evans and Browne, 1960; Dethier and Gelperin, 1967; Gelperin, 1966a,b, 1967, 1971a,b; Gelperin and Dethier, 1967; Dethier and Bodenstein, 1958; Núñez, 1964; Getting, 1971; Getting and Steinhardt, 1972; Omand, 1971) exert control over acceptance. Spatial summation between different chemosensory inputs exists in nonlinear fashion (Dethier, 1953, 1955) (see also Chapter 4 of this volume; and Sections III,C and III,E).

After a food source has been located, the strategy of its exploitation may pose additional problems. Heinrich (1971) showed that Manduca caterpillars consume leaves in a way which ensures optimal economy independent of the leaves’ shape. Some cooperation may even be necessary between larvae from a batch of eggs in order to exploit successfully, as in Neodiprion (Ghent, 1960), Perga (Carne, 1966), or Malacosoma (Wellington, 1957).

A quite sophisticated way to gain access to desired material of vegetable origin has evolved in ants who live in a mutualistic relationship with honeydew-producing Homoptera. The latter, connected to the plant’s sap stream, deliver surplus material to the ants which is very rich in carbohydrates and amino acids (Kloft, 1959; Way, 1963). This must not be the end of this pseudophytophagous food chain: the beetle Amphotis ambushes Lasius workers who carry the honeydew home and induces them to feed him (Hölldobler, 1968). In ants’ nests, other myrmecophilic insects may profit from the same sources (Hölldobler, 1967, 1970, 1972; Malicky, 1969; Wilson, 1971).

Another complex of adaptations to a phytophagous alimentation is the culture of fungus on plant material, so to say an extension to the outside of the endosymbiosis with microorganisms so common in phytophagous insects (Buchner, 1953). The most highly evolved case is known from ants of the tribe Attini (Weber, 1966, 1972; newer results on the biochemical basis of this symbiosis: J. S. Martin and Martin, 1970; M. M. Martin and Martin, 1970, 1971), but less conspicuous examples are known from many wood-boring insects (Graham, 1967; Batra and Batra, 1967; Batra, 1963, 1966; Schedl, 1958; Francke-Grosmann, 1967).

2 Carnivorous Insects

A few examples out of many which have been investigated may demonstrate that prey catching in carnivores can be no less versatile and elaborate than food obtaining in phytophages. In some cases, a larva may switch from phytophagy at young age to predation (Franz, 1967). This, at first glance surprising, change of feeding habits may have causes similar to the evolution of carnivory in the cerambycid beetle Elytroleptus which is not only a precise Batesian mimic of Lycus (Linsley et al., 1961) but also preys on its model; the reason may be that Lycus incorporates plant substances into its blood, which make it unpalatable to many carnivores but renders it attractive to Elytroleptus, the member of a family generally found to be phytophagous and which, as it were, eats the meat for salad (Eisner et al., 1962).

The larvae of aphidivorous coccinellids, chrysopids, and syrphids have a good chance to come across leaf lice when searching at random, since their parents laid their eggs next to the prey on plants (Banks, 1957; Banks, 1964). Prey catching in odonate larvae has been studied extensively. Very young larvae detect and locate prey with antennal receptors by means of vibrational stimuli from several millimeters distance (Richard, 1970). This antennal forking of prey is typical for most Zygoptera (Alverdes, 1923; Caillère, 1965, 1968, 1970). In older larvae, and especially in Anisoptera, visual cues are also responded to (Buchholtz, 1951; Richard, 1960, 1965) and dominate prey catching almost entirely in Aeschna (Koehler, 1924; Sälzle, 1932), which are able to judge the size of prey according to distance (Baldus, 1926). Suboptimal visual stimuli release an approach effect (or, if an object is too big, escape effect) and optimal ones release an attack effect (Hoppenheit, 1964b). Flickering of a light spot enhances its attack-releasing effect (Vogt, 1964; Etienne, 1968), although only movement with moderate speed across the visual field makes a prey object highly attractive (Etienne, 1969). Similarly, visual and vibrational stimuli interact in prey capture by Nepa (Richard, 1962) and Ranatra (Cloarec, 1969). Movement of a visually perceived object is the most general attack-releasing stimulus in pray-catching insects (Parker, 1965, 1969; Faasch, 1968). This is also true for mantids which are able to estimate precisely the distance of a binocularly viewed object (Rilling et al., 1959; Maldonado and Levin, 1967; Maldonado et al., 1967; Maldonado and Barrós-Pita, 1970; Maldonado and Rodriguez, 1972; Barrós-Pita and Maldonado, 1970).

Dytiscids require activation by chemical stimuli from prey in order to attack; the prey is then located visually and by means of vibrations (Schaller, 1926). Vibrations on the water surface for far-range detection and visual cues for close-range orientation also control prey capture in Notonecta (Baerends, 1939; Rabe, 1953; Wolda, 1961; Markl and Wiese, 1969; Wiese, 1972) and waterstriders (Rensing, 1962; Wiese, 1969; Meyer, 1971a,b; Murphey, 1971a,b). As in all animals which locate their prey by means of surface waves on the water (Markl, 1973), waves with frequencies between approximately 5 and 500 Hz and above the threshold displacement of a few μm can release the approach.

Some Trichoptera larvae build net traps which sift prey out of running water (Brickenstein, 1955; Tachet, 1971). Hydrous larvae catch flat snails by wedging them between folds of the back from which they are forwarded to the mandibles by numerous contortions (Bols, 1935). The larvae of fireflies (Lampyridae) find and follow the mucus trails of their prey: snails (Schaller and Schwalb, 1961).

Sometimes a predator recognizes its prey by reacting to the latter’s intraspecific communication signals. Various predators of bark beetles (clerid and ostomid beetles: Person, 1940; Reid, 1957; Struble, 1942; Thatcher and Pickard, 1966; Vité and Crozier, 1968; Rice, 1969; dolichopodid dipters: Williamson, 1971) not only locate their prey by following the oleoresins emanating from trees attacked by the scolytids; they are also attracted by aggregating pheromones released by the bark beetles while selecting new host trees (Vité and Renwick, 1968). Thus, mass aggregation and mass reproduction of prey and predator are focused spatially and synchronized (Vité et al., 1964; Harwood and Rudinsky, 1966; Rice, 1969; Vité and Williamson, 1970; Williamson, 1971; Pitman and Vité, 1971).

An even more evolved stage is reached when the predator imitates signals used by its prey in order to attract it. Females of the firefly, Photuris, attract and devour flash-courting males of the genus Photinus by imiating the light responses of Photinus females (Lloyd, 1965). Aggressive mimicry may also be at work in asilid flies imitating their bumblebee prey (Brower et al., 1960).

Histerid and staphylinid beetles preying on the brood of ants locate their host by its colony odors (Akre, 1968; Akre and Rettenmeyer, 1966; Hölldobler, 1970). Some of these myrmecophilic insects apparently imitate the behavior and sometimes also the chemical signals of ant larvae and thus succeed in being transported by the ants to their own brood, on which they may prey (Hölldobler, 1967, 1970; Malicky, 1969).

3 Parasitic Insects

Insects feeding parasitically as adults are found among the Anoplura, Thysanoptera, Hemiptera, Lepidoptera, Diptera, and Siphonaptera (Askew, 1971; Hocking, 1971). [Host-finding in parasitoids, in which only the larvae live as parasites (see Section II,D,4) is a problem of broodcare.] In parasitic Diptera, hosts range from annelids to mammals; most other parasitic insects concentrate on homoeotherms. Though chemical signals are often decisive for host selection, it is usually difficult to determine which out of a mixture is (are) the active component (s). Orientation in thermal convection currents—especially if containing attractive odors—and in temperature gradients has been reported also.

Rhodnius is attracted by visible movements, vibrations, odor, and warmth (Wigglesworth and Gillett, 1934). It controls the elasticity of its abdominal cuticle by means of neurosecretory nerves during suction in order to accommodate large meals of blood (Bennet-Clark, 1962; Maddrell, 1963, 1966; Núñez, 1963a,b). Tabanids react best to glossy black, highly reflecting spherical objects, while odors and warmth increase the effectiveness of a dummy (Bracken et al., 1962; Bracken and Thorsteinson, 1965; Thorsteinson et al., 1966). Similarly, Glossina finds cattle by distance orientation towards dark, moving objects and by close-range reaction to components of the perspiration of cattle, e.g., acetic acid (Chapman, 1961).

Contradictory evidence is reported on the stimuli guiding Stomoxys and eliciting its probing response. While Krijgsman (1930), Hopkins (1964), and Schärffenberg and Kupka (1951, 1959) found chemical stimuli like ammonia and caprylic, caproic, and valeric acids effective in addition to air currents, increase in relative humidity, and increase of substrate temperature, Gatehouse (1970a,b), though confirming the positive effects of relative humidity and temperature, and also roughness and low reflectance of a surface, failed to release any probing by blood or sweat components in physiological concentrations.

A wealth of literature deals with host selection and localization by mosquitoes (Downes, 1958a,b; Clements, 1963; Müller, 1968). The first step is to seek out the host’s habitat; visual cues can help in this as well as in attracting mosquitoes to objects (Brown, 1958; Downe, 1960), a reaction which is enhanced also by temperature and humidity stimuli (Kalmus and Hocking, 1960; Roessler, 1961). Most disputed are the effects of chemical stimuli. Carbon dioxide in high doses, the odor of blood, sweat, urine, formic, acetic, and propionic acids, lactic acid, amines, ammonia, steroids, amino acids, and diphenols have been reported to be attractive (Schärffenberg and Kupka, 1951, 1959; Roessler, 1961; Schärffenberg, 1962; Brown and Carmichael, 1961; Skinner et al., 1965; Müller, 1968). These odors release positive anemotactic orientation (Bässler, 1958). Under natural conditions lactic acid may be the most important attractant (Müller, 1968). Biting is released by sweat components as propionic, acetic, butyric, and pyruvic acids (Müller, 1968), and sucking by glucose, the concentration of which is subthreshold in sweat and suprathreshold in blood (Frings and Hamrun, 1950; Owen, 1963; Hosoi, 1959; Feir et al., 1961; Müller, 1968).

Most blackflies locate their hosts by visual means, if their bloodsucking activity concentrates at the time after sunrise and before sunset, i.e., when light intensity changes rapidly. Those species searching their host during the night rely on olfactory cues (Davies and Peterson, 1956; Peterson, 1959; Bennet, 1960; Davies, 1960; Wolfe and Peterson, 1960; Wenk and Schlörer, 1963; Wenk, 1965a,b).

How intricately the attack of a parasite can be adapted to make optimal use of a host is well demonstrated by Fuldner’s study (1968), describing how the staphylinid Aleochara approaches the puparia of Calliphora.

A very special case of parasitism is the adaptation of various insects (e.g., staphylinid beetles: Hölldobler, 1967, 1970, 1972; lycaenid butterflies: Malicky, 1969; and even other species of ants: Buschinger, 1970; for a general review, see Wilson, 1971) for living in ant colonies. This adaptation can go to the extreme as in the beetle Atemeles pubicollis, which, after hatching in nests of Formica, leaves in active search for a Myrmica nest. There it hibernates and switches to Formica again the next spring, where reproduction occurs. This change of hosts guarantees that the beetle stays always with the host which has most abundant provisions for it at a given time (Hölldobler, 1970).

C PROTECTION AND DEFENSE

Of the hundreds or thousands of eggs laid by a female insect fortunately only two grow up to adults who reproduce again, averaged over a span of many years. From a single pair of flies there would already be in the fourth generation 125 billion great-greatgrandchildren if all offspring were to survive. This high number of losses makes clear that a strong selection pressure is directed to the creation of protective mechanisms of all kinds; these range from adaptive coloration to the construction of hiding places and from speedy escape to fierce attack.

1 Protective Coloration and Behavior

In all protective coloration it is essential that the insect’s appearance is made optimally effective through its behavior (Robinson, 1969). Cryptically colored species seek the background to which they are adapted and remain there in akinesis (e.g., Eumensis: Tinbergen et al., 1942). Or they fit into their environment by specific postures (geometrid caterpillars: de Ruiter, 1952), movements (leaflike rocking: Cott, 1957), or by adaptive color changes (Carausius: Giersberg, 1928; Acrida: Ergene, 1952, 1954; dragonfly larvae: Krieger, 1954). Caterpillars of Colias are camouflaged by strong countershading when seen from the backside; their dorsal light reaction assures best use of this. In contrast, the ventral side of the inversely countershaded pupae is oriented upward (Süffert, 1932; de Ruiter, 1955). Many desert insects camouflage themselves actively; for example, the acridid Chrotogonus buries itself in sand with eyes remaining above the surface (Kevan and Knipper, 1959).

That protective coloration and camouflage behavior actually do increase chances of survival was demonstrated in geometrid caterpillars: the branchlike appearance and the appropriate posture are necessary to deceive finches or jays. If by chance a bird discovers a caterpillar, it continues to seek out similar-appearing objects (searching image). But subsequent grasping of many real pieces of wood soon inhibits this behavior. Maximal distribution and limited population density in a given area, therefore, are prerequisites for the effectiveness of the camouflage (de Ruiter, 1952).

While predators may be deceived in this way, behavior accompanying aposematic coloration has the function of warning potential predators that the object is unpalatable or dangerous. The coloration of the protected species is then often imitated by other protected (Müllerian mimicry) and unprotected species (Batesian mimicry). Most songbirds avoid wasps because of the repelling taste of the poison. By experience, they learn to associate it with the yellow-black markings (Mostler, 1935; Liepelt, 1963). Sometimes the formation of groups of insects increases the effectiveness of the individual coloration (Cott, 1957). In Lycus loripes (Coleoptera) the males secrete a pheromone which leads to aposematic aggregations (Eisner and Kafatos, 1962). Lycus species present the unpalatable models for complex Müllerian and Batesian mimetic associations involving beetles and even moths (Linsley et al., 1961). This is only one out of thousands of examples. Lack of space forces us to refer to Heikertinger (1954), Cott (1957), Brower (1965), Wickler (1968), and Rettenmeyer (1970).

The protective effect of both forms of mimicry has been proven experimentally (Mostler, 1935; Schmidt, 1958a, 1960; Sexton, 1960; Brower van Zandt, 1958a,b, 1960; Brower, 1958, Brower et al., 1960, 1963, 1971; Brower van Zandt and Brower, 1962; Duncan and Sheppard, 1965; Pitman et al., 1971; Benson, 1972) and its evolution studied in population models (Fisher, 1958; Sheppard, 1959; Holling, 1965; Emlen, 1968). The protection of models may rest on two sources: (1) the possession of defensive weapons (see Section II,C,3), as for instance a poisonous sting, which makes many bees or wasps suitable models for, among others, droneflies (Er is talis, Brower van Zandt and Brower, 1962) or buprestid beetles (Acmaeodera, Silberglied and Eisner, 1969); (2) the absorption of substances from their vegetable food which have evolved in the plants as a protective device against phytophages and which may now make insects, who have managed to cope with these deterrants or poisons, unpalatable or poisonous to their enemies (Brower and Brower van Zandt, 1964; Reichstein, 1967; Brower et al., 1968; Brower, 1970). Since in one species there may be—as demonstrated in Danaus plexippus—members who feed on nonpoisonous and who feed on poisonous plants, this palatability dimorphism has prompted the advance of a new category of mimicry: automimicry, a special case of the fact that all members of the species normally are Müllerian mimics (Brower et al., 1967a, 1970).

Conspicuous coloration, especially eye spots (Fig. 1) and concomitant behavior displays, can serve to frighten a predator, so that the victim may escape, as has been shown in mantids (Crane, 1952; Maldonado, 1970; MacKinnon, 1970) and Lepidoptera (Blest, 1957a,b). In naive predators any conspicuous novel stimulus can at first inhibit attack (Coppinger, 1969, 1970). The more plastic the eye markings appear by arrangement of colors in concentric rings, the larger is the startling effect on birds. Rhythmic shaking and rustling noises may increase the effect. In addition, eye spots can detract from vulnerable parts. If, on the other hand, a bird has once found such an animal edible, then the conspicuous markings are of no further value, and they may now even enhance predation (Blest, 1957a). The same is true for Batesian mimics (Cook et al., 1969; Brower et al., 1967). The appearance of saturniids and sphingids bears no relation to their taxonomic position, but is correlated with their behavior; the less the protective coloration is developed, the easier it is to release escape. Animals bearing a frightening coloration swing rhythmically in response to disturbance. Cryptically colored species and those mimicking wasps remain motionless (Blest, 1957b).

Fig. 1 Warning display of the mantid Pseudocreobotra wahlbergi. (From Cott, 1957.)

The production of sound by Cerambyx cerdo (Tembrock, 1960) and many other insects which seem to lack hearing organs (Haskell, 1961), has also been ascribed a frightening function, though maybe often prematurely (Markl, 1969). Magicicada may even deter bird predators by the enormous sound intensity (more than 1000 dynes/cm²) in their synchronized mass choruses (Simmons et al., 1971).

2 Escape

Escape is easily released in most defenseless insects which do not stay immobile to assure the effect of their cryptic or aposematic coloration, be it that flight is released by visual, mechanical, or olfactory (Dethier, 1947, 1956; Wilson, 1971) stimuli. An especially impressive example of specialized escape behavior is the reactions of moths to ultrasonic impulses (Eggers, 1925; Schaller and Timm, 1950; Roeder and Treat, 1957, 1961a,b; Roeder, 1962, 1963; Agee and Webb, 1969). Even from a distance of some 30 meters, moths with hearing organs, e.g., noctuids, react to the bats’ cries by zigzag flight and by dropping to the ground. This increases their chance of survival by 40% as compared to nonreacting species (Fig. 2). Roeder has made these escape reactions the object of a singularly thorough investigation into the sensory-neuromotor mechanisms of a behavior pattern (Roeder, 1964, 1966a,b, 1967, 1969a,b; Payne et al., 1966). Acoustic escape reactions from bats’ cries have also been reported for green lacewings (Chrysopa: Miller, 1971) and hawkmoths (Choerocampinae: Roeder and Treat, 1970). Arctiid and ctenuchid moths produce sounds when exposed to bats’ cries (Blest et al., 1963; Blest, 1964) which may warn bats that these species are unpalatable. Among a series of Müllerian acoustic mimics there was also a Batesian beneficiary found (Dunning, 1968).

Fig. 2 Flight tracks registered by various moths just before and immediately after exposure to a series of simulated bat cries. The dotted appearance of the track is due to the individual wing beats of the moth. The beginning of each track appears in each photograph and the moth finally flies out of the field. (From Roeder and Treat, 1961a.)

3 Active Defense

Active defense against attackers is not rare in insects (for rival aggression see Section II,D,3). Mechanical means are of rather limited efficiency: roaches (Roeder, 1959) and many Orthoptera (Faber, 1953; Jacobs, 1953; Alexander, 1960; Robinson, 1968) kick or grasp with heavily spined hind legs; mantids do the same with their fore legs unless the enemy is too large (Crane, 1952; Roeder, 1966). In the mantid, Stagmatoptera, the choice between attack, frightening display, or cryptic reaction depends on the developmental stage of the mandid and the size and the distance of an object (Balderrama and Maldonado, 1973). Of course, many grasshoppers, beetles, or other insects with sharp-edged mandibles can bite severely when fighting.

More important as effective weapons is the sting apparatus in Hymenoptera, especially of social forms (see Chapter 2 of this volume), although even in them more effective, modern ways of chemical warfare have evolved (Maschwitz and Kloft, 1971). Urticating hairs of many lepidopterous caterpillars are another example of poison apparatus of presumably defensive significance (Maschwitz and Kloft, 1971).

The use of defensive secretions is extremely widespread in insects. See Roth and Eisner (1962), Schildknecht (1963, 1970), Jacobson (1966), Weatherston (1967), Eisner (1970, 1972), and Whittaker and Feeny (1971) for references to the numerous original papers and detailed information on the chemical nature of the substances used. Secretions acting as contact poisons and/or repellents have been identified in species of Blattaria, Phasmida, Dermaptera, Hemiptera, Coleoptera, Hymenoptera, and Lepidoptera and are most probably even more widespread. Compounds used include short-chained aldehydes, organic acids, quinones, nitriles, and others, among them such exotic but extremely adaptively applied substances as steroid hormones of vertebrates, in concentrations which can narcotize vertebrate predators (Schildknecht et al., 1966) or nucleoproteids affecting blood pressure in small mammals (Schildknecht and Tacheci, 1971). Sometimes a mixture is released, in which part of its constituents assure the penetration of an arthropod enemy’s cuticle while the rest are responsible for the toxic action. The defensive spray is often not only oozed out, but really sprayed at a considerable distance and sometimes even aimed exactly at the attacker (Fig. 3).

Fig. 3 Palomena prasina (L) (Pentatomidae) aims the protective secretion into the direction from which its leg is touched. The secretion becomes visible on paper by a color reaction with Feulgen reagents. (From Remold, 1962.)

To give some details at least for one thoroughly investigated case, the bombardier beetle Brachynus may serve as an example (Schildknecht, 1957; Eisner, 1958, 1972; Schildknecht and Holoubek, 1961; Schildknecht et al., 1970). These beetles spray attackers, e.g., ants, with a secretion containing quinones, which is discharged hot and with an audible detonation (Fig. 4). The quinones are formed by a reaction between phenolic precursors and hydrogen peroxide in the outer chamber of the two-partitioned gland. Highly concentrated (40-60%) catalases and peroxidases which are extremely heat resistent and capable of withstanding the extreme concentrations of H2O2 (25%) and hydroquinone (10%) catalyze the reaction. The pressure of the liberated oxygen propels the quinone spray right into the face of the aggressor. Carabid beetles, of which Brachynus is one, have been found to be particularly inventive in defensive secretions; the evolution of these defensive mechanisms can be clearly traced (Schildknecht et al., 1968a,b).

Fig. 4 Ant (Pogonomyrmex badius) attacking a bombardier beetle (Brachinus sp., Carabidae) and getting sprayed in return. (From Eisner, 1972.)

In social forms, defensive discharges may be pooled in order to multiply their effect