INSECT CHEMORECEPTION FUNDAMENTAL AND APPLIED Insect Chemoreception Fundamental and Applied by Michael F. Ryan Department ofZoology, University College Dublin KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW eBookISBN: 0-306-47581-2 Print ISBN: 1-4020-0270-X ©2002 Kluwer Academic Publishers NewYork, Boston, Dordrecht, London, Moscow Print ©2002 Kluwer Academic Publishers Dordrecht All rights reserved No part of this eBook maybe reproducedor transmitted inanyform or byanymeans,electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: http://kluweronline.com and Kluwer's eBookstore at: http://ebooks.kluweronline.com DEDICATED TO MY FAMILY PREFACE In this time of edited volumes when the list of individual contributors may reach double figures, it is appropriate to question the usefulness of a volume, with such a broad scope, by a single author. The answer is simple. For years he has believed that the rather sharp distinction between fundamental and applied aspects of this discipline, has ill-served the significance of each; and has diminished the incidence of fruitful synergies. Yet the need for these was never greater, and this case may be developed by a single author withexperience of each aspect. The inclusion of a Chapter on Genetic Engineering may raise some doubts, but it is enabled by the chosen title “Chemoreception”, as distinct from Chemoperception: the latter implies detection of a chemical, followed by a behavioural response. But the former broader category subsumes Chemoperception and allows for the reception of a chemical toxin so potent as to prelude a behavioural or physiological response, other than death. Accordingly, chemical toxins are a legitimate inclusion. In which event, their delivery through a GM plant is as appropriate for study as their application in a spray. Following a Chapter devoted to an Introduction and Overview, Part I comprises Chapters 2, 3, 4, 5, and 6 respectively, providing a fundamental framework. Part II comprising Chapters 7, 8, 9, and 10 examines applied aspects. For internal consistency, the sequence followed in Part I in regard to plant chemicals and pheromones (Chapters 2 and 3 respectively), is also followed in Part II (Chapters 7 and 8 for plants and Chapter 9 for pheromones). However, as progress in genetic engineering for insect pest control (Chapter 10) is less with insects than with plants, Chapters 7, 8, and 10 may be read as a continuum on plants. Chapter 10 brings to the fore the Third World dilemma of feeding, in the future, vastly more people from less land and poorer-quality water. The problem is most acute in sub-Saharan Africa where, from 1970 onward, food production grew at about half the rate of population growth, entailing decreased per capita food production. Undernourished people in this region are estimated to number some 300 million or half the world’s total. In seeking to find a balance between GM-based and sustainable ecological solutions, this Chapter explicitly calls for a renewed commitment from the West, especially from the young researcher. Shall a coalition develop? My most grateful thanks are due to the many who encouraged or helped, especially President Art Cosgrove, University College Dublin (UCD), and my colleagues at the Institute of Environment and Life, Department of Zoology, Coimbra University, Portugal, where my presence was enabled by the PRAXIS XXI programme of the EU, and by the Foundation for Science and Technology, Lisbon. vii viii A very special debt of gratitude is owed to Professor Maria Susana de Almeida Santos, Leader of the Nematology Group, whose kind hospitality sustained this enterprise at difficult and decisive moments. She also, with her colleague Professor Isabel Abrantes, critically read the manuscript leading to significant improvements and the avoidance of countless solecisms. The hand-drawn figures are by William Clarke, UCD except for Figure 33 by Professor Mary Behan, and Figure 39 by Dr. Peter Daly, both originally of UCD. Figures 18, 32, 35, 36, 37, 38, 72 and 74 are by Fernando Correia, Coimbra University; chemical structures and all remaining diagrams are by Dr. Wen-Yuan Chung, UCD. At Coimbra University, the species index was compiled by Sofia dos S. da R. Costa, and the entire manuscript was prepared and formatted with unforgettable insight, patience, and skill by M. Clara Vieira Santos. MFR September 2001 TABLE OF CONTENTS Preface vii 1. INTRODUCTION AND OVERVIEW 1 FUNDAMENTAL ASPECTS 1 Historical 1 Insect phylogeny 2 Insect systems 2 Insect senses 4 Plant/insect relationships 7 APPLIED ASPECTS 8 Firstgeneration insecticides 9 Second generation insecticides 9 Organochlorines 9 Organophosphates 10 Carbamates 10 Pyrethroid insecticides 10 Avermectins 12 Chitin inhibitors 13 Third generation insecticides 13 Fourth generation insecticides 14 ECOLOGICAL CONSEQUENCES 15 Insect resistance 15 Mortality of beneficial and innocuous insects and wildlife 16 Target pest resurgence 16 Secondary pest outbreak 16 Mortality of wild life 16 Contamination of food 17 Cancer 18 The present position 19 Risk assessment 20 REFERENCES 23 PART I – FUNDAMENTAL ASPECTS 2. PLANT CHEMICALS 27 CHEMICAL DEFENCE BY NUTRIENTS 28 CHEMICALDEFENCE BY ALLELOCHEMICALS: STRUCTURAL CATEGORIES 29 Phenolics 29 Terpenoids 31 Monoterpenes 33 ix x Sesquiterpenes 35 Diterpenes 35 Triterpenes 36 Alkaloids 36 Sequestration 37 Effects on insects 38 Polyacetylenes and other compounds 39 ALLELOCHEMICALS: FUNCTIONAL CATEGORIES 40 Allomones 40 Jasmonic acid 43 Proteinase inhibitors 44 Kairomones 46 Synomones 47 Antimones 48 TRITROPHIC INTERACTIONS 48 Evolutionary aspects 49 Blend composition 51 Comparison of direct and indirect defence 51 MICROBIAL INTERACTIONS 52 Nitrogen-fixers 54 Endophytes 54 Phylloplane microflora 54 Plant pathogens 55 Insect mutualists 55 Insect pathogens 55 THE CONCEPT OF COEVOLUTION 56 Specific reciprocal coevolution 57 Diffusecoevolution 57 Escape and radiation coevolution 58 Diversifyingcoevolution 59 Objections 59 FATE IN INSECTS OF ALLELOCHEMICALS 61 Evacuation 61 Metabolism 61 Cytochrome P-450-dependent polysubstrate monooxygenases (PSMOs) 62 Esterases and transferases 63 Reductases 64 Sequestration 65 Pheromone precursors 67 REFERENCES 69 xi 3. PHEROMONES 73 PHEROMONE-PRODUCING GLANDS 73 Coleoptera 73 Lepidoptera 75 CHEMICAL STRUCTURES AND NOMENCLATURE OF PHEROMONES 77 Pheromones of female Lepidoptera 79 Pheromones of male Lepidoptera, and of other Orders 79 SEX PHEROMONES 81 Female sex pheromones 82 Specificity 82 Male sex pheromones 83 Sex-pheromonebiosynthesis 84 The blend 86 Perception of the blend 86 Significance of the blend 87 Genetics of the blend 87 Hormonalregulation of sex-pheromoneproduction 88 Melanizationand reddish coloration hormone (MRCH) 89 Orientation to pheromone source 90 AGGREGATION PHEROMONES 92 Synergism 95 Chiral specificity 97 Aphid aggregation pheromones 97 OVIPOSITION PHEROMONES 97 SPACING (EPIDEICTIC) PHEROMONES 98 PHEROMONES OF SOCIAL INSECTS 99 Multifunctionality 100 Kin recognition 101 Overlapping defence and sex attractant functions 103 Alarmpheromones 104 Alarm pheromone glands 105 Dispersal and attack 105 Chemistry of the compounds 105 Function-shift in pheromone evolution 107 REFERENCES 109 4. THE CHEMORECEPTIVE ORGANS: STRUCTURAL ASPECTS 113 THE SENSORY NEURON 115 ASSOCIATED CELLS 117 SYSTEMATICS OF SENSILLA 119 xii EVOLUTION OFSENSILLA 121 Collembola 121 Odonata 122 Lepidoptera 123 SENSILLA OF IMATURE INSECTS 125 Aporous mechanosensilla 125 Thermo-hygrosensilla 125 Chemosensilla 126 Gustatory chemosensilla 126 Olfactory chemosensilla 126 The sensory neuron 126 Associated cells 127 Morphogenesis and moulting 127 Sensillar distribution 128 Antenna 128 Maxillae 128 Labium 128 Clypeo-labrum 128 Mandibles 129 Embryological development of sensilla 129 SENSILLAR ACCESS 131 Dimensional movement 131 SIGNIFICANT ORGANELLES 132 EXTERNAL MORPHOMETRY 134 Morphological correlates 135 Internal morphometry 135 REFERENCES 138 5. ELECTROPHYSIOLOGY OF CHEMORECEPTION 140 THE NEURON 140 The action potential 140 Channel characteristics 141 Stimulus-response relationships 141 Central processing 142 THE INSECT ANTENNA 143 THE ELECTROANTENNOGRAM 144 Relationship of EAG to olfactory stimulation 145 Uses of the EAG 146 CIRCUITRY OF THE SENSILLUM 148 Ionic currents of the sensillum 150