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Resh & Carde. 2009. Encyclopedia of insects.

Resh & Carde. 2009. Encyclopedia of insects.

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Encyclopedia of insects Document Transcript

  • 1. Encyclopedia ofINSECTS
  • 2. This page intentionally left blank
  • 3. Encyclopedia ofINSECTS Second Edition Editors Vincent H. Resh University of California, Berkeley Ring T. Carde ´ University of California, Riverside AMSTERDAM • BOSTON • LONDON • NEW YORK • OXFORD • PARIS SAN DIEGO • SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier
  • 4. Cover Art: The jewel scarab, Chrysina cusuquensis, known only from a fragment of forest in northern Guatemala(Photograph courtesy of David Hawks).Letter-Opening Photo Credits:R: Snakefly (Raphidioptera) photographed at Nanaimo (Vancouver Island), British Columbia, Canada.(Photograph Copyright © Jay Patterson.)Y: Aedes aegypti, Uganda strain (a vector of yellow fever), bloodfeeding from the photographer’s hand.(Photograph by Leonard E. Munstermann.)Other letter-opening photographs furnished by the authors. (See relevant article for credit.)Copyright Exceptions:“Cat Fleas” by Nancy C. Hinkle and Michael K. Rust, “Cell Culture” by Dwight E. Lynn, “Extension Entomology” byNancy C. Hinkle, Beverly Sparks, Linda J. Mason, and Karen M. Vail, and “Nomenclature and Classification, Principlesof” by F. Christian Thompson are in the public domain.“Embiidina” by Edward S. Ross, Figures 1–4 Copyright © Edward S. Ross. “Swimming, Lake Insects” by Werner Nachtigall,Figures 1–3 Copyright © Werner Nachtigall. “Wolbachia” by Richard Stouthamer, Figure 1 Copyright © Richard Stouthamer.This book is printed on acid-free paper.Academic Press is an imprint of Elsevier30 Corporate Drive, Suite 400, Burlington, MA 01803, USA525 B Street, Suite 1900, San Diego, CA 92101-4495, USA32 Jamestown Road, London NW1 7BY, UKSecond edition 2009Copyright © 2009, Elsevier, Inc. All rights reserved.No part of this publication may be reproduced, stored in a retrieval system or transmitted inany form or by any means electronic, mechanical, photocopying, recording or otherwisewithout the prior written permission of the publisherPermissions may be sought directly from Elsevier’s Science & Technology RightsDepartment in Oxford, UK: phone (ϩ44) (0) 1865 843830; fax (ϩ44) (0) 1865 853333;email: permissions@elsevier.com. Alternatively you can submit your request onlineby visiting the Elsevier web site at http://www.elsevier.com/locate/permissions, andselecting: Obtaining permission to use Elsevier materialISBN: 978-0-12-374144-8 For information on all Academic Press publications visit our website at www.elsevierdirect.comTypeset by Macmillan Publishing Solutionswww.macmillansolutions.comPrinted and bound in China09 10 11 12 10 9 8 7 6 5 4 3 2 1
  • 5. CONTENTSCONTENTS BY SUBJECT AREA xvii Anatomy: Head, Thorax,CONTRIBUTORS xxi Abdomen, and Genitalia 11GUIDE TO THE ENCYCLOPEDIA xxx David H. Headrick and Gordon GordhFOREWORD xxxii Anopheles Mosquito 21PREFACE TO THE SECOND EDITION xxxiv see MosquitoesPREFACE xxxvABOUT THE EDITORS xxxvi Anoplura 21 see Phthiraptera Antennae 21 A Catherine LoudonAcari 1 Ants 24see Mites; Ticks Nigel R. FranksAccessory Glands 1 Aphids 27Diana E. Wheeler John T. SorensenAcoustic Behavior 2 Apis Species 31see Hearing Eva CraneAedes Mosquito 2 Aposematic Coloration 33see Mosquitoes Mathieu JoronAestivation 2 Apterygota 38Sinzo Masaki Ring T. Cardé and Vincent H. ReshAfricanized Bees 4 Aquatic Habitats 38see Neotropical African Bees Richard W. Merritt and J. Bruce Wallace Arachnida 48Agricultural Entomology 4 see Daddy-Long-Legs; Mites; Scorpions;Marcos Kogan and Ronald Prokopy Spiders; Ticks; VinegaroonsAlderfly 8 Archaeognatha 48see Megaloptera Helmut SturmAmber 8 Arthropoda and Related Groups 50George Poinar Jr. James H. Thorp
  • 6. vi Contents Auchenorrhyncha 56 Blood 112 Christopher H. Dietrich see Circulatory System Autohemorrhage 64 Blood Sucking 112 Vincent H. Resh M. J. Lehane Autotomy 64 Body Size 114 Ring T. Cardé Christer Björkman, Karl Gotthard, and Mats W. Pettersson Boll Weevil 116 R. N. Foster B Bombyx mori 117 Bedbugs 65 Satoshi Takeda Christiane Weirauch and Alec C. Gerry Book Louse 119 Bee 66 see Psocoptera see Apis Species Borers 119 Beekeeping 66 Timothy D. Paine Eva Crane Brain and Optic Lobes 121 Bee Products 71 Nicholas J. Strausfeld Eva Crane Bristletail 130 Beetle 75 see Archaeognatha see Coleoptera Bubonic Plague 130 Biodiversity 75 Irwin W. Sherman Nigel E. Stork Biogenic Amines 80 Arnd Baumann, Wolfgang Blenau, and Joachim Erber C Biogeographical Patterns 82 Caddisfly 133 Peter Zwick see Trichoptera Biological Control of Insect Pests 91 Caste 133 M. S. Hoddle and R. G. Van Driesche Sean O’Donnell Bioluminescence 101 Caterpillars 135 James E. Lloyd and Erin C. Gentry Frederick W. Stehr Biotechnology and Insects 105 Cat Fleas 138 Bryony C. Bonning Nancy C. Hinkle and Michael K. Rust Blattodea 108 Cave Insects 139 Donald G. Cochran Francis G. Howarth
  • 7. Contents viiCell Culture 144 Collection and Preservation 201Dwight E. Lynn Charles V. Covell Jr.Chemical Defense 145 Collembola 206Murray S. Blum Kenneth A. Christiansen, Peter Bellinger and Frans JanssensChemoreception 148B. K. Mitchell Colonies 210 Sean O’DonnellChiggers and OtherDisease-Causing Mites 152 Colorado Potato Beetle 212Larry G. Arlian George G. KennedyChitin 156Ephraim Cohen Coloration 213 Helen GhiradellaChromosomes 158Graham C. Webb Commercialization of Insects and Their Products 220Chrysalis 162 Gail E. Kampmeier and Michael E. IrwinFrederick W. Stehr Conservation 227Cicadas 163 Tim R. NewMaxwell S. Moulds Crickets 232Circadian Rhythms 165 Richard D. Alexander and Daniel OtteTerry L. Page Crypsis 236Circulatory System 169 Paul M. BrakefieldThomas A. Miller and Günther Pass Cultural Entomology 239Classification 173 James N. Hoguesee Nomenclature and Classification Cuticle 245Cockroach 173 Svend O. Andersensee BlattodeaCocoon 173Frederick W. Stehr DCodling Moth 174 Daddy-Long-Legs 247Stephen C. Welter Gonzalo GiribetCoevolution 175 Damselfly 248Douglas J. Futuyma see OdonataCold/Heat Protection 179 Dance Language 248David L. Denlinger P. Kirk VisscherColeoptera 183 DDT 251Joseph V. McHugh and James K. Liebherr Fumio Matsumura
  • 8. viii Contents Defensive Behavior 252 Drosophila melanogaster 301 Justin O. Schmidt Patrick M. O’Grady Delusory Parasitosis 257 Dung Beetles 304 see Ekbom Syndrome James Ridsdill-Smith and Leigh W. Simmons Dengue 257 Thomas W. Scott Dermaptera Susan M. Rankin and James O. Palmer 259 E Earwig 308 Development, Hormonal Control of 261 see Dermaptera Michael E. Adams Ecdysis 308 Diapause 267 see Molting David L. Denlinger Ecdysteroids 308 Michael E. Adams Digestion 271 Walter R. Terra Eggs 311 Diana E. Wheeler Digestive System 273 Walter R. Terra and Clélia Ferreira Egg Coverings 312 Diana E. Wheeler Diplura 281 Markus Koch Ekbom Syndrome 313 Nancy C. Hinkle Diptera 284 Embiidina 315 Richard W. Merritt, Gregory Edward S. Ross W. Courtney, and Joe B. Keiper Embryogenesis 316 Diversity 297 ´ Lisa Nagy and Miodrag Grbic see Biodiversity Endangered Insects 320 Division of Labor in Insect Societies 297 Scott Hoffman Black and Gene E. Robinson Mace Vaughan Dobsonfly 299 Endopterygota 324 see Megaloptera Ring T. Cardé Dog Heartworm 299 Entomological Societies 324 Edward G. Platzer Alan I. Kaplan Dormancy 300 Ephemeroptera 328 Richard E. Lee Jr. John E. Brittain and Michel Sartori Dragonfly 301 Estivation 334 see Odonata see Aestivation
  • 9. Contents ixEvolution 334 Fossil Record 396see Phylogeny of Insects David GrimaldiExcretion 334 Freshwater Habitats 403Timothy J. Bradley see Aquatic HabitatsExopterygota 339Ring T. Cardé Fruit Fly 403 see Drosophila melanogasterExoskeleton 339Svend O. AndersenExtension EntomologyNancy C. Hinkle, Beverly Sparks, 342 GLinda J. Mason, and Karen M. Vail Gallmaking and Insects 404Eyes and Vision 345 Katherine N. Schick and Donald L. DahlstenMichael F. Land Genetically Modified Plants 406 David A. Andow F Genetic Engineering Peter W. Atkinson and David A. O’Brochta 410Fat Body 356Ephraim Cohen Genetic Variation 416 George K. Roderick and Maria NavajasFeeding Behavior 357R. F. Chapman Grasshopper 419Fire Ants 362 see OrthopteraLes Greenberg Genomics 419Flea 364 Peter Arensburger and Peter W. Atkinsonsee Siphonaptera Grassland Habitats 424Flight 364 Teja Tscharntke, Ingolf Steffan-Michael Dickinson and Robert Dudley Dewenter, Andreas Kruess, and Carsten ThiesFly 372see Diptera Greenhouse Gases, Global Warming, and Insects 428Folk Beliefs and Superstitions 372 Peter StilingJames N. HogueFood, Insects as 376 Growth, Individual 431Gene R. DeFoliart Martin B. Berg and Richard W. MerrittForensic Entomology 381 Grylloblattodea 434M. Lee Goff D. C. F. Rentz and Sigfrid IngrischForest Habitats 386 Gypsy Moth 435David L. Wood and Andrew J. Storer Joseph S. Elkinton
  • 10. x Contents Hymenoptera 473 H Donald L. J. Quicke Hearing 440 Hypermetamorphosis 484 Ron Hoy and Jayne Yack John D. Pinto Hemiptera 446 Hyperparasitism 486 see Auchenorrhyncha; Daniel J. Sullivan Prosorrhyncha; Sternorrhyncha Hemolymph 446 Michael R. Kanost I Heteroptera 449 see Prosorrhyncha Imaginal Discs 489 Seth S. Blair Hibernation 449 Richard E. Lee Jr. Immunology 492 Nancy E. Beckage History of Entomology 449 Edward H. Smith and George G. Kennedy Industrial Melanism 496 Michael E. N. Majerus Homeostasis, Behavioral 458 P. Kirk Visscher Insecta, Overview 501 Homoptera 459 Vincent H. Resh and Ring T. Cardé see Auchenorrhyncha; Sternorrhyncha Insecticides 502 Honey 459 Fumio Matsumura Eva Crane and P. Kirk Visscher Insecticide and Acaricide Resistance 505 Honey Bee 461 Gregor J. Devine and see Apis Species Ian Denholm Honeydew 461 Angela E. Douglas Insectivorous Plants 511 Lewis J. Feldman Hornet 463 see Wasps Insectivorous Vertebrates 514 Charles R. Crumly Host Seeking, by Parasitoids 463 J. Daniel Hare and Ronald M. Weseloh Insect Zoos 516 Leslie Saul-Gershenz Host Seeking, for Plants 466 Elizabeth A. Bernays Integrated Pest Management 523 House Fly 469 Ronald Prokopy and Gregory A. Dahlem Marcos Kogan Human History, Insects Effect on 471 Integument 528 James N. Hogue Svend O. Andersen
  • 11. Contents xiIntroduced Insects 529 Lepidoptera 559Daniel Simberloff Jerry A. PowellIsland Biogeography 533 Lice 587George K. Roderick and see PhthirapteraRosemary G. Gillespie Lice, Human 587Isoptera 535 Terri L. MeinkingVernard R. Lewis Locusts 589 R. F. Chapman JJapanese BeetleDavid W. Held and Daniel A. Potter 539 M Magnetic Sense 592June Beetles 540 John Klotz and Rudolf JanderDaniel A. Potter and David W. Held Malaria 594Juvenile Hormones 541 William K. ReisenMichael E. Adams Mantodea 597 Lawrence E. Hurd K Mantophasmatodea 599 Klaus-Dieter Klass andKatydid 546 Christin Grossmannsee OrthopteraKiller Bees 546 Marine Insects 600see Neotropical African Bees Lanna Cheng Mating Behaviors 604 Darryl T. Gwynne L Mechanoreception 610 Andrew S. French andLacewing 547 Päivi H. Torkkelisee Neuroptera Mecoptera 611Ladybugs 547 George W. ByersMichael E. N. MajerusLarva 551 Medical Entomology 614Frederick W. Stehr John D. EdmanLearning 552 Medicine, Insects in 618Daniel R. Papaj Ronald A. ShermanLegs 555 Megaloptera 620Peter H. Adler Norman H. Anderson
  • 12. xii Contents Metabolism 623 Nest Building 688 S. N. Thompson and R. K. Suarez Robert L. Jeanne Metamorphosis 627 Neuropeptides 691 Frederick W. Stehr Miriam Altstein Migration 628 Neuroptera 695 Hugh Dingle Catherine A. Tauber, Maurice J. Tauber, and Gilberto S. Albuquerque Mimicry 633 Mathieu Joron Nomenclature and Classification, Principles of 707 Mites 643 F. Christian Thompson Barry M. OConnor Nutrition 715 Molting 649 S. N. Thompson and S. J. Simpson Lynn M. Riddiford Monarchs 654 Lincoln P. Brower O Mosquitoes 658 Ocelli and Stemmata 721 Bruce F. Eldridge Frederick W. Stehr Moth 663 Odonata 721 see Lepidoptera K. J. Tennessen Mouthparts 663 Orientation 729 R. F. Chapman Ring T. Cardé Movies, Insects in 668 Orthoptera 732 May R. Berenbaum and Sigfrid Ingrisch and D. C. F. Rentz Richard J. Leskosky Ovarioles 743 Muscle System 675 Diana E. Wheeler Robert Josephson Oviposition Behavior 745 Museums and Display Collections 680 Marc J. Klowden Gordon M. Nishida P N Parasitoids 748 Neosomy 685 Nick Mills Frank J. Radovsky Parental Care 751 Neotropical African Bees 686 Michelle Pellissier Scott Orley R. Taylor Parthenogenesis in Insects and Mites 753 Nervous System 688 Benjamin B. Normark and see Brain and Optic Lobes Lawrence R. Kirkendall
  • 13. Contents xiiiPathogens of Insects 757 Praying Mantid 837Brian A. Federici see MantodeaPhasmida 765 Predation/Predatory Insects 837Erich H. Tilgner Ronald M. Weseloh and J. Daniel HarePheromones 766Ring T. Cardé and Jocelyn G. Millar Prosorrhyncha 839Phoresy 772 Carl W. SchaeferMarilyn A. Houck Protura 855Photography of Insects 774 Markus KochMark W. Moffett Psocoptera 858Phthiraptera 777 Edward L. MockfordRonald A. Hellenthal and Roger D. Price Pterygota 860Phylogeny of Insects 780 Ring T. CardéPeter S. Cranston and Penny J. Gullan Puddling Behavior 860Physical Control of Insect Pests 794 Scott R. SmedleyCharles Vincent, Phyllis Weintraub, Pupa and Puparium 862and Guy Hallman Frederick W. StehrPhytophagous Insects 798Elizabeth A. BernaysPhytotoxicityAlexander H. Purcell 800 Q Queen 863Plant Diseases and Insects 802 see CasteAlexander H. PurcellPlant–Insect Interactions 806J. Mark Scriber RPlecoptera 810 Raphidioptera 864Kenneth W. Stewart Ulrike Aspöck and Horst AspöckPollination and Pollinators 813 Rearing of Insects 866Gordon W. Frankie and Robbin W. Thorp Norman C. LepplaPollution, Insect Response to 819 Recruitment Communication 869David M. Rosenberg and Vincent H. Resh James F. A. TranielloPolyembryony 821 Regulatory Entomology 877Michael R. Strand Robert V. DowellPopulation Ecology 826 Reproduction, Female 880Joseph S. Elkinton Diana E. Wheeler
  • 14. xiv Contents Reproduction, Female: Silk Production 921 Hormonal Control of 882 František Sehnal and Catherine Craig Diana E. Wheeler Silverfish 924 Reproduction, Male 885 see Zygentoma Marc J. Klowden Siphonaptera 924 Reproduction, Male: Michael W. Hastriter and Hormonal Control of 887 Michael F. Whiting Marc J. Klowden Snakefly 928 Research Tools, Insects as 888 see Raphidioptera Kipling W. Will Sociality 928 James E. Zablotny Respiratory System 889 Jon F. Harrison Soil Habitats 935 Patricia J. Vittum River Blindness 895 Vincent H. Resh Sound Production 939 see Hearing Spermatheca 939 S Marc J. Klowden Salivary Glands 897 Spermatophore 940 Gregory P. Walker Marc J. Klowden Scale Insect 901 Spiders 941 see Sternorrhyncha Rosemary G. Gillespie and Joseph C. Spagna Scales and Setae 901 Springtail 951 Shaun L. Winterton see Collembola Scorpions 904 Stamps, Insects and 951 Stanley C. Williams Charles V. Covell Jr. Segmentation 909 Sterile Insect Technique 953 Paul Z. Liu and Nipam H. Patel Jorge Hendrichs and Alan Robinson Sericulture 912 Sternorrhyncha 957 Satoshi Takeda Penny J. Gullan and Jon H. Martin Sex Determination 914 Stonefly 967 Michael F. Antolin and Adam D. Henk see Plecoptera Sexual Selection 917 Stored Products as Habitats 967 Kenneth Y. Kaneshiro Rudy Plarre and Wendell E. Burkholder Silk Moth 921 Strepsiptera 971 see Bombyx mori Michael F. Whiting
  • 15. Contents xvSwimming, Lake Insects 972 Touch 1011Werner Nachtigall see MechanoreceptionSwimming and Other Tracheal System 1011Movements, Stream Insects 975 Jon F. HarrisonBernhard Statzner Trichoptera (Caddisflies) 1015Symbionts Aiding Digestion 978 John C. MorseAndreas Brune Tsetse Fly 1020Symbionts, Bacterial 983 Stephen G. A. LeakMichael E. N. MajerusSystematics 987see Nomenclature and Classification U Urban Habitats 1025 T Michael K. RustTaste 988see ChemoreceptionTaxonomy 988 Vsee Nomenclature and Classification Venom 1028Teaching Resources 988 Justin O. SchmidtJohn H. Acorn and Felix A. H. Sperling Veterinary Entomology 1031Temperature, Effects on Bradley A. MullensDevelopment and Growth 990 ˇ ˇOldr ich Nedved Vibrational Communication 1034 ˇ Andrej Cokl and Meta Virant-DoberletTermite 993see Isoptera Vinegaroons 1038 Justin O. SchmidtTerrestrial Insects 993see Soil Habitats Vision 1041 see Eyes and VisionThermoregulation 993Bernd Heinrich Vitellogenesis 1041 William H. TelferThrips 999see ThysanopteraThysanopteraLaurence A. Mound 999 WThysanura 1003 Walking and Jumping 1044see Archaeognatha; Zygentoma Roy E. Ritzmann and Sasha N. ZillTicks 1003 Wasps 1049Daniel E. Sonenshine Justin O. Schmidt
  • 16. xvi Contents Water and Ion Balance, Hormonal Control of 1052 Z Thomas M. Clark Zoonotic Agents, Arthropod-Borne 1065 Wings 1055 Robert S. Lane Robin J. Wootton Zoraptera 1069 Wolbachia 1061 Michael S. Engel Richard Stouthamer Zygentoma 1070 Worker 1063 Helmut Sturm see Caste GLOSSARY 1073 SUBJECT INDEX 1093 Y Yellow Fever 1064 Thomas P. Monath Yellowjacket 1065 see Wasps
  • 17. CONTENTS BY SUBJECT AREAAnatomy ExcretionAnatomy: Head, Thorax, Abdomen, and Genitalia Eyes and VisionAntennae Fat BodyBrain and Optic Lobes FlightChitin Genetic EngineeringColoration GenomicsCuticle HearingDigestive System HemolymphExoskeleton HibernationEyes and Vision Homeostasis, BehavioralIntegument HoneydewLegs Imaginal DiscsMouthparts ImmunologyOcelli and Stemmata InsecticidesPupa and Puparium Juvenile HormonesSalivary Glands Magnetic SenseScales and Setae MechanoreceptionSegmentation MetabolismTracheal System MoltingWings Muscle System NeuropeptidesPhysiology NutritionAestivation Reproduction, FemaleAutohemorrhage Reproduction, Female: Hormonal Control ofAutotomy Reproduction, MaleBiogenic Amines Reproduction, Male: Hormonal Control ofBioluminescence Respiratory SystemBiotechnology and Insects Salivary GlandsBody Size SegmentationBrain and Optic Lobes Sex DeterminationCell Culture Silk Production in InsectsChemical Defense Symbionts Aiding DigestionChemoreception ThermoregulationChitin Tracheal SystemChromosomes VitellogenesisCircadian Rhythms Walking and JumpingCirculatory System Water and Ion Balance, Hormonal Control ofCold/Heat ProtectionCuticle BehaviorDDT Aposematic ColorationDevelopment, Hormonal Control of AutohemorrhageDiapause AutotomyDigestion BioluminescenceDigestive System Blood SuckingDormancy BorersEcdysteroids Caste
  • 18. xviii Contents by Subject Area Chemical Defense Mating Behaviors Chemoreception Ovarioles Circadian Rhythms Oviposition Behavior Colonies Parthenogenesis in Insects and Mites Crypsis Polyembryony Dance Language Reproduction, Female Defensive Behavior Reproduction, Female: Hormonal Control of Division of Labor in Insect Societies Reproduction, Male Eyes and Vision Reproduction, Male: Hormonal Control of Feeding Behavior Spermatheca Flight Spermatophore Hearing Vitellogenesis Hibernation Host Seeking, by Parasitoids Development And Metamorphosis Host Seeking, for Plants Body Size Learning Caterpillars Magnetic Sense Chrysalis Mating Behaviors Cocoon Mechanoreception Development, Hormonal Control of Migration Ecdysteroids Mimicry Egg Coverings Nest Building Growth, Individual Orientation Hypermetamorphosis Oviposition Behavior Imaginal Discs Parental Care Juvenile Hormones Pheromones Larva Phoresy Metamorphosis Predation/Predatory Insects Molting Puddling Behavior Neosomy Recruitment Communication Temperature, Effects on Development and Growth Sex Determination Sexual Selection Sociality Major Groups And Notable Forms Swimming, Lake Insects Ants Swimming and Other Movements, Stream Insects Aphids Thermoregulation Apis Species Vibrational Communication Apterygota Walking and Jumping Archaeognatha Arthropoda and Related Groups Evolution Auchenorrhyncha Amber Bedbugs Aposematic Coloration Blattodea Biogeographical Patterns Boll Weevil Coevolution Bombyx mori Fossil Record Cat Fleas Genetic Variation Cicadas Industrial Melanism Codling Moth Insecticide and Acaricide Resistance Coleoptera Island Biogeography Collembola Mimicry Colorado Potato Beetle Nomenclature and Classification, Principles of Crickets Phylogeny of Insects Daddy-Long-Legs Sexual Selection Dermaptera Sociality Diplura Wolbachia Diptera Drosophila melanogaster Reproduction Dung Beetles Accessory Glands Embiidina Egg Coverings Endopterygota Eggs Ephemeroptera Embryogenesis Exopterygota
  • 19. Contents by Subject Area xixFire Ants Predation/Predatory InsectsGrylloblattodea Symbionts Aiding DigestionGypsy Moth Symbionts, BacterialHouse Fly VenomHymenoptera Veterinary EntomologyInsecta, Overview WolbachiaIsopteraJapanese Beetle Interactions With HumansJune Beetles Apis SpeciesLadybugs BedbugsLepidoptera Bee ProductsLice, Human BeekeepingLocusts Blood SuckingMantodea Bombyx moriMantophasmatodea Bubonic PlagueMecoptera Chiggers and Other Disease-Causing MitesMegaloptera Commercialization of Insects and Their ProductsMites Cultural EntomologyMonarchs DDTMosquitoes DengueNeotropical African Bees Ekbom SyndromeNeuroptera Extension EntomologyOdonata Folk Beliefs and SuperstitionsOrthoptera Food, Insects asPhasmida Forensic EntomologyPhthiraptera HoneyPlecoptera Human History, Insects Effect onProsorrhyncha InsecticidesProtura Integrated Pest ManagementPsocoptera Lice, HumanPterygota MalariaRaphidioptera Medical EntomologyScorpions Medicine, Insects inSiphonaptera MosquitoesSpiders Museums and Display CollectionsSternorrhyncha Regulatory EntomologyStrepsiptera River BlindnessThysanoptera Silk Production in InsectsTicks Tsetse FlyTrichoptera Yellow FeverVinegaroons Zoonotic Agents, Arthropod-BorneWaspsZorapteraZygentoma Habitats Aquatic HabitatsInteractions With Other Organisms Cave InsectsAposematic Coloration Forest HabitatsBlood Sucking Grassland HabitatsCat Fleas Marine InsectsChiggers and Other Disease-Causing Mites Soil HabitatsDefensive Behavior Stored Products as HabitatsDog Heartworm Urban HabitatsFeeding BehaviorHost Seeking, by ParasitoidsHost Seeking, for Plants EcologyHyperparasitism Agricultural EntomologyMimicry Aposematic ColorationParasitoids BiodiversityPathogens of Insects Biogeographical PatternsPhoresy Biological Control of Insect PestsPhytophagous Insects Borers
  • 20. xx Contents by Subject Area Coevolution History And Methodology Conservation Amber Crypsis Biotechnology and Insects DDT Cell Culture Endangered Insects Collection and Preservation Gallmaking and Insects Cultural Entomology Genetic Variation Entomological Societies Genetically Modified Plants Folk Beliefs and Superstitions Greenhouse Gases, Global Warming, and Insects Forensic Entomology Honeydew Genetically Modified Plants Hyperparasitism Genetic Engineering Insecticides Genomics Insectivorous Plants History of Entomology Insectivorous Vertebrates Human History, Insects Effect on Integrated Pest Management Insect Zoos Introduced Insects Medical Entomology Migration Movies, Insects in Mimicry Museums and Display Collections Parasitoids Nomenclature and Classification, Principles of Pathogens of Insects Photography of Insects Phoresy Rearing of Insects Physical Control of Insect Pests Research Tools, Insects as Phytophagous Insects Sericulture Phytotoxicity Stamps, Insects and Plant Diseases and Insects Sterile Insect Technique Plant–Insect Interactions Teaching Resources Pollination and Pollinators Veterinary Entomology Pollution, Insect Response to Population Ecology Predation/Predatory Insects Swimming, Lake Insects Swimming and Other Movements, Stream Insects
  • 21. CONTRIBUTORSJohn H. Acorn Horst AspöckUniversity of Alberta, Canada Medical University of ViennaTeaching Resources RaphidiopteraMichael E. Adams Ulrike AspöckUniversity of California, Riverside Naturhistorisches Museum WienDevelopment, Hormonal Control of RaphidiopteraEcdysteroids Peter W. AtkinsonJuvenile Hormones University of California, RiversidePeter H. Adler Genetic EngineeringClemson University GenomicsLegs Arnd BaumannGilberto S. Albuquerque Forschungszentrum Jülich, GermanyUniversidade Estadual do Norte Fluminense, Brazil Biogenic AminesNeuroptera Nancy E. BeckageRichard D. Alexander University of California, RiversideUniversity of Michigan ImmunologyCrickets Peter Bellinger*Miriam Altstein California State University, NorthridgeAgricultural Research Organization, Volcani Center, Israel CollembolaNeuropeptides May R. BerenbaumSvend O. Andersen University of IllinoisThe Royal Danish Academy of Sciences and Letters Movies, Insects inCuticle Martin B. BergExoskeleton Loyola University ChicagoIntegument Growth, IndividualNorman H. Anderson Elizabeth A. BernaysOregon State University University of ArizonaMegaloptera Host Seeking, for PlantsDavid A. Andow Phytophagous InsectsUniversity of Minnesota, St. Paul Christer BjörkmanGenetically Modified Plants Swedish University of Agricultural Sciences andMichael F. Antolin Stockholm UniversityColorado State University Body SizeSex Determination Scott Hoffman BlackPeter Arensburger The Xerces SocietyUniversity of California, Riverside Endangered InsectsGenomics Seth S. BlairLarry G. Arlian University of Wisconsin, MadisonWright State University Imaginal DiscsChiggers and Other Disease-Causing Mites Wolfgang Blenau Universität Potsdam, Germany*Deceased November 20, 2000. Biogenic Amines
  • 22. xxii Contributors Murray S. Blum Donald G. Cochran University of Georgia Virginia Polytechnic Institute and State University Chemical Defense Blattodea Bryony C. Bonning Ephraim Cohen Iowa State University The Hebrew University of Jerusalem Biotechnology and Insects Chitin Fat Body Timothy J. Bradley University of California, Irvine ´ Andrej Cokl Excretion National Institute of Biology, Slovenia Vibrational Communication Paul M. Brakefield Leiden University, The Netherlands Gregory W. Courtney Crypsis Iowa State University Diptera John E. Brittain Natural History Museum, University of Oslo Charles V. Covell, Jr. Ephemeroptera University of Louisville Collection and Preservation Lincoln P. Brower Stamps, Insects and Sweet Briar College Monarchs Catherine Craig Harvard University/Tufts University Andreas Brune Silk Production in Insects Max Planck Institute for Terrestrial Microbiology, Marburg, Germany Eva Crane† Symbionts Aiding Digestion International Bee Research Association Apis Species Wendell E. Burkholder Beekeeping University of Wisconsin, Madison Bee Products Stored Products as Habitats Honey George W. Byers Peter S. Cranston University of Kansas University of California, Davis Mecoptera Phylogeny of Insects Ring T. Cardé Charles R. Crumly University of California, Riverside University of California Press, Berkeley Apterygota Insectivorous Vertebrates Autotomy Endopterygota Gregory A. Dahlem Exopterygota Northern Kentucky University Insecta, Overview House Fly Orientation Donald L. Dahlsten‡ Pheromones University of California, Berkeley Pterygota Gallmaking and Insects R. F. Chapman* Gene R. DeFoliart University of Arizona University of Wisconsin, Madison Feeding Behavior Food, Insects as Locusts Mouthparts Ian Denholm Rothamsted Research Lanna Cheng Insecticide and Acaricide Resistance Scripps Institution of Oceanography Marine Insects David L. Denlinger Ohio State University Kenneth A. Christiansen Cold/Heat Protection Grinnell College, Grinnell, IA Diapause Collembola Gregor J. Devine Thomas M. Clark Rothamsted Research Indiana University, South Bend Insecticide and Acaricide Resistance Water and Ion Balance, Hormonal Control of † Deceased September 6, 2007. *Deceased May 2, 2003. ‡ Deceased September 3, 2003.
  • 23. Contributors xxiiiMichael Dickinson Andrew S. FrenchCalifornia Institute of Technology Dalhousie University, Halifax, Nova ScotiaFlight MechanoreceptionChristopher H. Dietrich Douglas J. FutuymaIllinois Natural History Survey State University of New York, Stony BrookAuchenorrhyncha CoevolutionHugh Dingle Erin C. GentryUniversity of California, Davis University of FloridaMigration BioluminescenceAngela E. Douglas Alec C. GerryCornell University, USA University of California, RiversideHoneydew BedbugsRobert V. Dowell Helen GhiradellaCalifornia Department of Food and Agriculture State University of New York, AlbanyRegulatory Entomology ColorationRobert Dudley Rosemary G. GillespieUniversity of California, Berkeley University of California, BerkeleyFlight Island BiogeographyJohn D. Edman SpidersUniversity of California, Davis Gonzalo GiribetMedical Entomology Harvard UniversityBruce F. Eldridge Daddy-Long-LegsUniversity of California, Davis M. Lee GoffMosquitoes Chaminade University of HonoluluJoseph S. Elkinton Forensic EntomologyUniversity of MassachusettsGypsy Moth Gordon GordhPopulation Ecology U.S. Department of Agriculture Anatomy: Head, Thorax, Abdomen, and GenitaliaMichael S. EngelUniversity of Kansas Karl GotthardZoraptera Swedish University of Agricultural Sciences and Stockholm UniversityJoachim Erber Body SizeTechnische Universität Berlin, GermanyBiogenic Amines Miodrag Grbic ´ University of Western Ontario, CanadaBrian A. Federici EmbryogenesisUniversity of California, RiversidePathogens of Insects Les Greenberg University of California, RiversideLewis J. Feldman Fire AntsUniversity of California, BerkeleyInsectivorous Plants David GrimaldiClélia Ferreira American Museum of Natural History, New YorkUniversity of São Paulo, Brazil Fossil RecordDigestive System Christin GrossmannR. Nelson Foster Museum für Tierkunde, DresdenU.S. Department of Agriculture MantophasmatodeaBoll Weevil Penny J. GullanGordon W. Frankie University of California, DavisUniversity of California, Berkeley Phylogeny of InsectsPollination and Pollinators SternorrhynchaNigel R. Franks Darryl T. GwynneUniversity of Bristol University of TorontoAnts Mating Behaviors
  • 24. xxiv Contributors Guy Hallman Ron Hoy USDA-ARS, Weslaco, Texas Cornell University Physical Control of Insect Pests Hearing J. Daniel Hare Lawrence E. Hurd University of California, Riverside Washington and Lee University Host Seeking, by Parasitoids Mantodea Predation/Predatory Insects Sigfrid Ingrisch Jon F. Harrison Museum Koenig, Bonn Arizona State University Grylloblattodea Respiratory System Orthoptera Tracheal System Michael E. Irwin Michael W. Hastriter University of Illinois Brigham Young University Commercialization of Insects and Their Products Siphonaptera Rudolf Jander David H. Headrick University of Kansas, Lawrence California Polytechnic State University Magnetic Sense Anatomy: Head, Thorax, Abdomen, and Genitalia Frans Janssens Bernd Heinrich University of Antwerp, Belgium University of Vermont Collembola Thermoregulation Robert L. Jeanne David W. Held University of Wisconsin Auburn University Nest Building Japanese Beetle June Beetles Mathieu Joron Muséum National d’Histoire Naturelle, France Ronald A. Hellenthal Aposematic Coloration University of Notre Dame Mimicry Phthiraptera Robert Josephson Jorge Hendrichs University of California, Irvine JFAO/IAE Division, Vienna, Austria Muscle System Sterile Insect Technique Gail E. Kampmeier Adam D. Henk Illinois Natural History Survey Colorado State University Commercialization of Insects and Their Products Sex Determination Kenneth Y. Kaneshiro Nancy C. Hinkle University of Hawaii University of Georgia Sexual Selection Cat Fleas Ekbom Syndrome Michael R. Kanost Extension Entomology Kansas State University Hemolymph M. S. Hoddle University of California, Riverside Alan I. Kaplan Biological Control of Insect Pests East Bay Regional Park District, Berkeley, CA Entomological Societies James N. Hogue California State University, Northridge Joe B. Keiper Cultural Entomology The Cleveland Museum of Natural History Folk Beliefs and Superstitions Diptera Human History, Insects Effect on George G. Kennedy Marilyn A. Houck North Carolina State University Texas Tech University Colorado Potato Beetle Phoresy History of Entomology Francis G. Howarth Lawrence R. Kirkendall B. P. Bishop Museum, Honolulu, Hawaii University of Bergen, Norway Cave Insects Parthenogenesis in Insects and Mites
  • 25. Contributors xxvKlaus-Dieter Klass James E. LloydMuseum für Tierkunde, Dresden University of FloridaMantophasmatodea BioluminescenceJohn Klotz Catherine LoudonUniversity of California, Riverside University of California, IrvineMagnetic Sense AntennaeMarc J. Klowden Dwight E. LynnUniversity of Idaho U.S. Department of AgricultureOviposition Behavior Cell CultureReproduction, MaleReproduction, Male: Hormonal Control of Michael E. N. Majerus*Spermatheca University of CambridgeSpermatophore Industrial Melanism LadybugsMarkus Koch Symbionts, BacterialFreie Universität Berlin, GermanyDiplura Jon H. MartinProtura The Natural History Museum, London SternorrhynchaMarcos KoganOregon State University Sinzo MasakiAgricultural Entomology Hirosaki UniversityIntegrated Pest Management AestivationAndreas Kruess Linda J. MasonUniversity of Göttingen, Germany Purdue UniversityGrassland Habitats Extension EntomologyMichael F. Land Fumio MatsumuraUniversity of Sussex, Brighton University of California, DavisEyes and Vision DDTRobert S. Lane InsecticidesUniversity of California, Berkeley Joseph V. McHughZoonotic Agents, Arthropod-Borne University of GeorgiaStephen G. A. Leak ColeopteraInternational Trypanotolerance Centre, The Gambia Terri L. MeinkingTsetse Fly Global Health Associates of Miami (GHAM)Richard E. Lee, Jr. Lice, HumanMiami University, Oxford, OH Richard W. MerrittDormancy Michigan State UniversityHibernation Aquatic HabitatsM. J. Lehane DipteraUniversity of Wales, Bangor Growth, IndividualBlood Sucking Jocelyn G. MillarNorman C. Leppla University of California, RiversideUniversity of Florida PheromonesRearing of Insects Thomas A. MillerRichard J. Leskosky University of California, RiversideUniversity of Illinois Circulatory SystemMovies, Insects in Nick MillsVernard R. Lewis University of California, BerkeleyUniversity of California, Berkeley ParasitoidsIsoptera B. K. MitchellJames K. Liebherr University of Alberta, CanadaCornell University ChemoreceptionColeopteraPaul Z. LiuUniversity of California, BerkeleySegmentation *Deceased January 27, 2009.
  • 26. xxvi Contributors Edward L. Mockford Sean O’Donnell Illinois State University University of Washington Psocoptera Caste Colonies Mark W. Moffett University of California, Berkeley Patrick M. O’Grady Photography of Insects University of California, Berkeley Drosophila melanogaster Thomas P. Monath Acambis Inc., Cambridge, MA Daniel Otte Yellow Fever Philadelphia Academy of Natural Sciences Crickets John C. Morse Clemson University Terry L. Page Trichoptera Vanderbilt University Circadian Rhythms Max S. Moulds Australian Museum, Sydney Timothy D. Paine Cicadas University of California, Riverside Borers Laurence A. Mound CSIRO Entomology, Canberra, Australia James O. Palmer Thysanoptera Allegheny College Dermaptera Bradley A. Mullens Daniel R. Papaj University of California, Riverside University of Arizona Veterinary Entomology Learning Werner Nachtigall Günther Pass Universität der Saarlandes, Germany University of Vienna, Austria Swimming, Lake Insects Circulatory System Lisa Nagy Nipam H. Patel University of Arizona University of California, Berkeley Embryogenesis Segmentation Maria Navajas Mats W. Pettersson Institut National de la Recherche Agronomique (INRA), Swedish University of Agricultural Sciences and Centre de Biologie et Gestion des Populations, Stockholm University Montferrier sur Lez, France Body Size Genetic Variation John D. Pinto Oldr ich Nedve d ˇ ˇ University of California, Riverside University of South Bohemia, and Institute of Entomology, Hypermetamorphosis Czech Republic Temperature, Effects on Development and Growth Rudy Plarre Federal German Institute for Materials Research and Tim R. New Testing, Germany La Trobe University, Australia Stored Products as Habitats Conservation Edward G. Platzer Gordon M. Nishida University of California, Riverside University of California, Berkeley Dog Heartworm Museums and Display Collections George Poinar, Jr. Benjamin B. Normark Oregon State University University of Massachusetts, Amherst Amber Parthenogenesis in Insects and Mites Daniel A. Potter David A. O’Brochta University of Kentucky University of Maryland Biotechnology Institute Japanese Beetle Genetic Engineering June Beetles Barry M. OConnor Jerry A. Powell University of Michigan University of California, Berkeley Mites Lepidoptera
  • 27. Contributors xxviiRoger D. Price George K. RoderickUniversity of Minnesota University of California, BerkeleyPhthiraptera Genetic Variation Island BiogeographyRonald Prokopy*University of Massachusetts David M. RosenbergAgricultural Entomology Freshwater Institute, Winnipeg, CanadaIntegrated Pest Management Pollution, Insect Response toAlexander H. Purcell Edward S. RossUniversity of California, Berkeley California Academy of SciencesPhytotoxicity EmbiidinaPlant Diseases and Insects Michael K. RustDonald L. J. Quicke University of California, RiversideImperial College, University of London Cat FleasHymenoptera Urban HabitatsFrank J. Radovsky Michel SartoriOregon State University Museum of Zoology, LausanneNeosomy EphemeropteraSusan M. Rankin Leslie Saul-GershenzAllegheny College Center for Ecosystem Survival, San Francisco, CADermaptera Insect ZoosWilliam K. ReisenUniversity of California, Davis Carl W. SchaeferMalaria University of Connecticut ProsorrhynchaD. C. F. RentzCalifornia Academy of Sciences, San Francisco Katherine N. SchickGrylloblattodea University of California, BerkeleyOrthoptera Gallmaking and InsectsVincent H. Resh Justin O. SchmidtUniversity of California, Berkeley Southwestern Biological Institute, TucsonApterygota Defensive BehaviorAutohemorrhage VenomInsecta, Overview VinegaroonsPollution, Insect Response to WaspsPterygotaRiver Blindness Michelle Pellissier Scott University of New HampshireLynn M. Riddiford Parental CareUniversity of WashingtonMolting Thomas W. Scott University of California, DavisJames Ridsdill-Smith DengueUniversity of Western Australia, AustraliaDung Beetles J. Mark Scriber Michigan State UniversityRoy E. Ritzmann Plant–Insect InteractionsCase Western Reserve UniversityWalking and Jumping František SehnalAlan Robinson Biology Centre ASCRJFAO/IAE Division, Vienna, Austria Silk Production in InsectsSterile Insect Technique Irwin W. ShermanGene E. Robinson University of California, Riverside/The Scripps ResearchUniversity of Illinois, Urbana-Champaign Institute, La JollaDivision of Labor in Insect Societies Bubonic Plague Ronald A. Sherman University of California, Irvine*Deceased May 14, 2004. Medicine, Insects in
  • 28. xxviii Contributors Daniel Simberloff Nigel E. Stork University of Tennessee James Cook University, Australia Introduced Insects Biodiversity Leigh W. Simmons Richard Stouthamer University of Western Australia, Australia University of California, Riverside Dung Beetles Wolbachia S. J. Simpson Michael R. Strand University of Sydney University of Georgia Nutrition Polyembryony Scott R. Smedley Nicholas J. Strausfeld Trinity College, Connecticut University of Arizona Puddling Behavior Brain and Optic Lobes Edward H. Smith Helmut Sturm Cornell University (Emeritus), Asheville, NC University Hildesheim, Germany History of Entomology Archaeognatha Daniel E. Sonenshine Zygentoma Old Dominion University R. K. Suarez Ticks University of California, Santa Barbara John T. Sorensen Metabolism California Department of Food and Agriculture Daniel J. Sullivan Aphids Fordham University Joseph C. Spagna Hyperparasitism University of California, Berkeley Satoshi Takeda Spiders National Institute of Agrobiological Sciences, Japan Beverly Sparks Bombyx mori University of Georgia Sericulture Extension Entomology Catherine A. Tauber Felix A. H. Sperling Cornell University University of Alberta, Canada Neuroptera Teaching Resources Maurice J. Tauber Bernhard Statzner Cornell University CNRS–Université Lyon 1, France Neuroptera Swimming and Other Movements, Stream Insects Orley R. Taylor Ingolf Steffan-Dewenter University of Kansas University of Göttingen, Germany Neotropical African Bees Grassland Habitats William H. Telfer Frederick W. Stehr University of Pennsylvania Michigan State University Vitellogenesis Caterpillars K. J. Tennessen Chrysalis Florida State Collection of Arthropods, Gainesville, FL Cocoon Odonata Larva Metamorphosis Walter R. Terra Ocelli and Stemmata University of São Paulo, Brazil Pupa and Puparium Digestion Digestive System Kenneth W. Stewart University of North Texas Carsten Thies Plecoptera University of Göttingen, Germany Grassland Habitats Peter Stiling University of South Florida F. Christian Thompson Greenhouse Gases, Global Warming, and Insects U.S. Department of Agriculture Nomenclature and Classification, Principles of Andrew J. Storer Michigan Technological University, Houghton S. N. Thompson Forest Habitats University of California, Riverside
  • 29. Contributors xxixMetabolism Phyllis WeintraubNutrition Agricultural Research Organization, Gilat Research Center, IsraelJames H. Thorp Physical Control of Insect PestsUniversity of KansasArthropoda and Related Groups Christiane Weirauch University of California, RiversideRobbin W. Thorp BedbugsUniversity of California, DavisPollination and Pollinators Stephen C. Welter University of California, BerkeleyErich H. Tilgner Codling MothUniversity of GeorgiaPhasmida Ronald M. Weseloh The Connecticut Agricultural Experiment StationPäivi H. Torkkeli Host Seeking, by ParasitoidsDalhousie University, Halifax, Nova Scotia Predation/Predatory InsectsMechanoreception Diana E. WheelerJames F. A. Traniello University of ArizonaBoston University Accessory GlandsRecruitment Communication EggsTeja Tscharntke Egg CoveringsUniversity of Göttingen, Germany OvariolesGrassland Habitats Reproduction, Female Reproduction, Female: Hormonal Control ofKaren M. VailUniversity of Tennessee, Knoxville Michael F. WhitingExtension Entomology Brigham Young University SiphonapteraR. G. Van Driesche StrepsipteraUniversity of Massachusetts, AmherstBiological Control of Insect Pests Kipling W. Will University of California, BerkeleyMace Vaughan Research Tools, Insects asThe Xerces Society Stanley C. WilliamsEndangered Insects San Francisco State UniversityCharles Vincent ScorpionsAgriculture and Agri-Food Canada, Quebec Shaun L. WintertonPhysical Control of Insect Pests North Carolina State UniversityMeta Virant-Doberlet Scales and SetaeNational Institute of Biology, Slovenia David L. WoodVibrational Communication University of California, BerkeleyP. Kirk Visscher Forest HabitatsUniversity of California, Riverside Robin J. WoottonDance Language University of ExeterHomeostasis, Behavioral WingsHoney Jayne YackPatricia J. Vittum Carleton UniversityUniversity of Massachusetts HearingSoil Habitats James E. ZablotnyGregory P. Walker U.S. Department of AgricultureUniversity of California, Riverside SocialitySalivary Glands Sasha N. ZillJ. Bruce Wallace Marshall UniversityUniversity of Georgia Walking and JumpingAquatic Habitats Peter ZwickGraham C. Webb Max-Planck-Institut für Limnologie, GermanyThe University of Adelaide, Australia Biogeographical PatternsChromosomes
  • 30. GUIDE TO THE ENCYCLOPEDIA The Encyclopedia of Insects is a complete source of information ARTICLE FORMATon the subject of insects, contained within a single volume. Each Each article in this Encyclopedia begins with an introductory par-article in the Encyclopedia provides an overview of the selected agraph that defines the topic being discussed and indicates its signifi-topic to inform a broad spectrum of readers, from insect biologists cance. For example, the article “Exoskeleton” begins as follows:and scientists conducting research in related areas, to students andthe interested general public. The exoskeleton is noncellular material that is located on top In order that you, the reader, will derive the maximum benefit of the epidermal cell layer and constitutes the outermost partfrom the Encyclopedia of Insects, we have provided this Guide. It of the integument. The local properties and appearance of theexplains how the book is organized and how the information within exoskeleton are highly variable, and nearly all visible featuresits pages can be located. of an insect result from the exoskeleton. The exoskeleton serves as a barrier between the interior of the insect and the environment, preventing desiccation and the penetration ofSUBJECT AREAS microorganisms. Muscles governing the insect’s movements The Encyclopedia of Insects presents 273 separate articles on the are attached to the exoskeleton.entire range of entomological study. Articles in the Encyclopedia fall Major headings highlight important subtopics that are discussedwithin 12 general subject areas, as follows: in the article. For example, the article “Flight” includes the follow- ● Anatomy ing topics: “Evolution of Flight”; “Aerodynamics”; “Neural Control”; ● Physiology “Energetics”; “Ecology and Diversity.” ● Behavior ● Evolution CROSS-REFERENCES ● Reproduction ● Development and Metamorphosis The Encyclopedia of Insects has an extensive system of cross- ● Major Groups and Notable Forms referencing. References to other articles may appear either as mar- ● Interactions with Other Organisms ginal headings within the A–Z topical sequence, or as indications of ● Interactions with Humans related topics at the end of a particular article. ● Habitats As an example of the first type of reference cited above, the fol- ● Ecology lowing marginal entry appears in the A–Z article list between the ● History and Methodology entries “Bee Products” and “Biodiversity”: Beetle see ColeopteraORGANIZATION This reference indicates that the topic of Beetles is discussed elsewhere, under the article title “Coleoptera,” which is the name of The Encyclopedia of Insects is organized to provide the maximum the order including this group.ease of use for its readers. All of the articles are arranged in a single An example of the second type, a cross-reference at the end of analphabetical sequence by title. An alphabetical Table of Contents article, can be found in the entry “DDT.” This article concludes withfor the articles can be found beginning on p. v of this introductory the statement:section. As a reader of the Encyclopedia, you can use this alphabeticalTable of Contents by itself to locate a topic. Or you can first identify See Also the Following Articlesthe topic in the Contents by Subject Area (p. xvii) and then go to the Insecticides ■ Integrated Pest Management ■ Pollutionalphabetical Table to find the page location. This reference indicates that these three related articles all pro- In order to identify articles more easily, article titles begin with vide some additional information about DDT.the key word or phrase indicating the topic, with any descrip-tive terms following this. For example, “Temperature, Effects onDevelopment and Growth” is the title assigned to an article, rather BIBLIOGRAPHYthan “Effects of Temperature on Development and Growth,” The Bibliography section appears as the last element of an article,because the specific term Temperature is the key word. under the heading “Further Reading.” This section lists recent
  • 31. Guide to the Encyclopedia xxxisecondary sources that will aid the reader in locating more detailed in this Encyclopedia. The terms were identified by the contributorsor technical information on the topic at hand. Review articles and as helpful to the understanding of their entries, and they have beenresearch papers that are important to a more detailed understanding defined by these authors according to their use in the actual articles.of the topic are also listed here. The Bibliography entries in this Encyclopedia are for the benefit INDEXof the reader, to provide references for further reading or additionalresearch on the given topic. Thus they typically consist of a limited The Subject Index for the Encyclopedia of Insects contains morenumber of entries. They are not intended to represent a complete than 7000 entries. Within the entry for a given topic, references tolisting of all the materials consulted by the author(s) in preparing the general coverage of the topic appear first, such as a complete articlearticle. The Bibliography is in effect an extension of the article itself, on the subject. References to more specific aspects of the topic thenand it represents the author’s choice as to the best sources available appear below this in an indented list.for additional information.GLOSSARY The Encyclopedia of Insects presents an additional resource forthe reader, following the A–Z text. A comprehensive glossary providesdefinitions for more than 750 specialized terms used in the articles
  • 32. FOREWORDI would say that creating an encyclopedia of insects was a her- on, contribute millions more. Insect-based biological control of both culean task, but I think that sells the enterprise short. After all, insect and weed pests is worth additional millions in reclaimed land Hercules only had twelve labors assigned to him, and twelve and crop production, and even insect disposal of dung and otheryears to complete them—with insects, there are over 900,000 differ- waste materials, although decidedly unglamorous, is economicallyent species and many, many more stories to tell. Twelve years from significant in fields, rangelands, and forests throughout the country.now, there will likely be even more. Why, then, would anyone under- So, for no reason other than economic self-interest, there’s rea-take the seemingly impossible task of compiling an encyclopedia of son enough for creating an encyclopedia of insects. But what caninsects? To an entomologist, the answer is obvious. For one thing, be learned from insects that can’t be learned from an encyclopediathere’s the numbers argument—over 70% of all known species are of any other abundant group of organisms? Basically, the biologyinsects, so if any group merits attention in encyclopedic form, surely of insects is the biology of small size. Small size, which has been init’s the one that happens to dominate the planet. Moreover, owing large part responsible for the overwhelming success of the taxon, atin large part to their staggering diversity, insects are in more differ- the same time imposes major limits on the taxon. The range in sizeent places in the world than virtually any other organism. There are of living organisms, on earth at least, encompasses some 13 ordersinsects in habitats ranging from the High Arctic to tropical rainfor- of magnitude (from a 100 metric ton blue whale to rotifers weigh-ests to petroleum pools to glaciers to mines a mile below the sur- ing less than 0.01 mg). Insects range over five orders of magnitude—face to caves to sea lion nostrils and horse intestines. About the only from 30-g beetles to 0.03-g fairyflies—so eight orders of magnitudeplace where insects are conspicuously absent is in the deep ocean are missing in the class Insecta. Problems at the upper limit involve(actually, in deep water in general), an anomaly that has frustrated support, transport, and overcoming inertia, issues clearly not criticalmore than a few entomologists who have grown accustomed to world for organisms, like insects, at the lower end of the range.domination. Then there’s the fact that insects have been around for We humans, in the grand scheme of things, are big creatures andlonger than most other high-profile life-forms. The first proto-insects as a consequence we interact with the biological and physical worlddate back some 400 million years; by contrast, mammals have been entirely differently. Rules that constrain human biology often arearound only about 230 million years and humans (depending on how suspended for insects, which operate by a completely different set ofthey’re defined) a measly one million years. rules. The constraints and benefits of small size are reflected in every Probably the best justification for an encyclopedia devoted to aspect of insect biology. They hear, smell, taste, and sense the worldinsects is that insects have a direct and especially economic impact in every other way with abilities that stagger the imagination. Theyon humans. In the United States alone, insects cause billions of dol- are capable of physical feats that seem impossible—most fly, somelars in losses to staple crops, fruit crops, truck crops, greenhouse and glow in the dark, and others control the sex of their offspring andnursery products, forest products, livestock, stored grain and pack- even occasionally engage in virgin birth, to cite a few examples. Theiraged food, clothing, household goods and furniture, and just about generation times are so short and reproductive rates so high thatanything else people try to grow or build for sale or for their own they can adapt and evolve at rates that continually surprise (and sty-consumption. Beyond the balance sheet, they cause incalculable mie) us. The environment is “patchier” to smaller organisms, whichlosses as vectors of human pathogens. They’re involved in transmis- can divide resources more finely than can large, lumbering species.sion of malaria, yellow fever, typhus, plague, dengue, various forms Thus, they can make a living on resources so rare or so nutrient-poorof encephalitis, relapsing fever, river blindness, filariasis, sleeping that it defies belief, such as nectar, dead bodies, and even dung.sickness, and innumerable other debilitating or even fatal diseases, So they’re profoundly different from humans and other big ani-not just abroad in exotic climes but here in the United States as well. mals, and the study of insects can offer many insights into life onAll told, insects represent a drag on the economy unequaled by any earth that simply couldn’t be gained from a study of big creatures.other single class of organisms, a seemingly compelling reason for By the same token, though, they are cut from the same cloth—thekeeping track of them in encyclopedic form. same basic building blocks of life, same genetic code, and the like— In the interests of fairness, however, it should be mentioned that and their utility as research organisms has provided insights into allinsects also amass economic benefits in a magnitude unequaled by life on the planet.most invertebrates (or even, arguably, by most vertebrates). Insect- The Encyclopedia of Insects contains contributions from somepollinated crops in the United States exceed $9 billion in value annu- of the greatest names in entomology today. Such a work has to beally, and insect products, including honey, wax, lacquer, silk, and so a collective effort because nobody can be an expert in everything
  • 33. Foreword xxxiiientomological. Even writing a foreword for such a wide-ranging vol- activities than perhaps any other class of organisms, to be the ulti-ume is a daunting task. To be such an expert would mean mastering mate authority on insects also means mastering the minutiae of his-every biological science from molecular biology (in which the fruit tory, economics, art, literature, politics, and even popular culture.fly Drosophila melanogaster serves as a premier model organism) to Nobody can master all of that information—and that’s why this ency-ecosystem ecology (in which insects play an important role in rates clopedia is such a welcome volume.of nutrient turnover and energy flow). But, because insects, throughtheir ubiquity and diversity, have had a greater influence on human —May R. Berenbaum
  • 34. PREFACE TO THE SECOND EDITIONW e are pleased to have had the privilege of continuing as edi- Between publication of the first and second edition of the tors for the second edition of the Encyclopedia of Insects. Encyclopedia several contributors to the first edition died, including This edition contains several new entries and updates of Peter Bellinger, Donald Dahlsten, Reginald Chapman, Eva Crane,almost all of the original entries. Many new illustrations have been Michael Majerus, and Ronald Prokopy. Their substantial contributionsadded and references for further readings have been updated. to entomology will long be remembered. The first edition of the Encyclopedia of Insects was well received. We thank the staff of Elsevier Press for their assistance on thisAwards garnered include: The “Most Outstanding Single-Volume project. Christine Minihane originally proposed the preparation of aReference in Science,” presented by The Association of American second edition and Andy Richford shepherded it to completion. PatPublishers for 2003; An “Outstanding Academic Title, 2003,” by Gonzalez was invaluable in managing the flow of revised manuscripts.CHOICE magazine; and “Best of Reference, 2003,” by both the Stephen Pegg and Mani Prabakaran oversaw the printing process. WeNew York Public Librarians and the American Library Journal 2003. especially thank Alan Kaplan for reading over the final text for consist-These are a tribute to the quality of contributions to that volume. ency and accuracy. David Hawks provided the cover photograph.We anticipate that this updated, second edition will play the same We are pleased to dedicate our efforts in producing this secondrole in assisting students, teachers, and researchers in the entomo- edition to our mentors and professors, whose influence we still feellogical and biological sciences, along with interested readers among 40 years later: Stuart Neff, Louis Krumholz, Jack Franclemont andthe general public, in obtaining up-to-date and accurate information Wendell Roelofs.about these fascinating organisms. —Vincent H. Resh and Ring T. Cardé
  • 35. PREFACEI nsects are ever present in human lives. They are at once awe completed. This is the first order of insects to be described in over inspiring, fascinating, beautiful, and, at the same time, a scourge 80 years, and we are pleased to be able to include it as an entry, of humans because of food loss and disease. Yet despite their further underscoring that there is much left to learn about insects.negative effects, we depend on insects for pollination and for their Some topics, especially the “poster insects”—those well-known taxaproducts. As insects are the largest living group on earth (75% of below the level of orders for which entries are presented—may notall animal species), any understanding of ecological interactions at cover all that are desired by some readers. Given insect biodiversity,local or global scales depends on our knowledge about them. Given your indulgence is requested.the current interest in biodiversity, and its loss, it must be remem- We have gathered over 260 experts worldwide to write on thebered that insects represent the major part of existing biodiversity. entries that we have selected for inclusion. These specialists, ofAesthetically, insect images are often with us as well: early images course, have depended on the contributions of thousands of theirinclude Egyptian amulets of sacred scarabs; modern images include entomological predecessors. Because the modern study of entomol-dragonfly jewelry, butterfly stationery, and children’s puppets. ogy is interdisciplinary, we enlisted experts ranging from arachnolo- The idea of an Encyclopedia of Insects is new, but the concept of gists to specialists in zoonotic diseases. Given that the two of us havean encyclopedia is quite old. In 1745, Diderot and D’Alembert asked spent over 25 combined years as editors of the Annual Review ofthe best minds of their era—including Voltaire and Montesquieu— Entomology, many of our contributors were also writers for that peri-to prepare entries that would compile existing human knowledge in odical. We thank our contributors for putting up with our compulsiveone place: the world’s first encyclopedia. It took over 20 years to fin- editing, requests for rewrites, and seemingly endless questions.ish the first edition, which became one of the world’s first best-selling Our intended audience is not entomological specialists but ento-books and a triumph of the Enlightenment. mological generalists, whether they be students, teachers, hobbyists, What do we intend this encyclopedia to be? Our goal is to con- or interested nonscientists. Therefore, to cover the diverse interests ofvey the exciting, dynamic story of what entomology is today. It is this readership, we have included not just purely scientific aspects ofintended to be a concise, integrated summary of current knowl- the study of insects, but cultural (and pop-cultural) aspects as well.edge and historical background on each of the nearly 300 entries We thank the staff of Academic Press for their encouragementpresented. Our intention has been to make the encyclopedia scien- and assistance on this project. Chuck Crumly had the original con-tifically uncompromising; it is to be comprehensive but not exhaus- cept for this encyclopedia, convinced us of its merit, and helped ustive. Cross-references point the reader to related topics, and further greatly in defining the format. Chris Morris provided suggestionsreading lists at the end of each article allow readers to go into topics about its development. Jocelyn Lofstrom and Joanna Dinsmorein more detail. The presence of a certain degree of overlap is inten- guided the book through printing. Gail Rice managed the flow oftional, because each article is meant to be self-contained. manuscripts and revisions with skill and grace, and made many valu- The Encyclopedia of Insects also includes organisms that are able suggestions. Julie Todd of Iowa State University provided a cru-related to insects and often included in the purview of entomol- cial final edit of the completed articles. All these professionals haveogy. Therefore, besides the members of the class Insecta—the true helped make this a rewarding and fascinating endeavor.insects—the biology of spiders, mites, and related arthropods is We dedicate our efforts in editing the Encyclopedia of Insects toincluded. The core of this encyclopedia consists of the articles on the our wives, Cheryl and Anja; their contributions to our entomologicaltaxonomic groups—the 30 or so generally accepted orders of insects, and personal lives have been indescribable.the processes that insects depend on for their survival and success,and the range of habitats they occupy. The fact that entomology isa dynamic field is emphasized by the discovery of a new order ofinsects, the Mantophasmatodea, just as this encyclopedia was being —Vincent H. Resh and Ring T. Cardé
  • 36. ABOUT THE EDITORS Ring Cardé joined the Department of Entomology of the UniversityVincent Resh is Professor of Entomology and a Curator of the Essig of California, Riverside, in 1996 as Distinguished Professor and holdsMuseum at the University of California, Berkeley, since 1975. He is the position of A. M. Boyce Chair. He has served as Department Chairthe author of more than 300 articles on insects, mainly on the role since 2003. He has authored more than 230 articles on insect chemi-of aquatic insects in the assessment of water pollution and as vectors cal messengers, particularly on moth communication by pheromones,of disease. For 22 years, he was an editor of the Annual Review of and has edited four books on insect chemical ecology and pherom-Entomology and served as an ecological advisor to the United Nations ones. He is a fellow of the American Association for the AdvancementWorld Health Organization’s program on the control of river blindness of Science, the Entomological Society of America, the Entomologicalin West Africa. In 1995 he was elected as a Fellow of the California Society of Canada, and the Royal Entomological Society. In 2009Academy of Sciences and was the recipient of the University of he was awarded the Silver Medal by the International Society ofCalifornia at Berkeley’s Distinguished Teaching Award. Chemical Ecology.
  • 37. Sperm can be stored for some length of time in spermathecae, with the record belonging to ant queens that maintain sperm viability A A for a decade or more. Secretions of spermathecal glands are poorly characterized, and how sperm is maintained for such extended periods is not known. Spermathecal tissue seems to create a chemi- cal environment that maintains sperm viability, perhaps through reduced metabolism. A nutritional function is also possible. Transport of sperm out of storage can be facilitated by the secre- tions of the spermathecal gland, which presumably activate qui- escent sperm to move toward the primary reproductive tract. One potential function of female accessory glands that has been explored only slightly is the production of hormonelike substances that modu- late reproduction functions. Production of Egg Coverings Acari Female accessory glands that produce protective coverings for see Mites; Ticks eggs are termed colleterial glands. Colleterial glands have been best characterized in cockroaches, which produce an oothecal case sur- rounding their eggs. Interestingly, the left and right glands are ana- tomically different and have different products. Separation of the chemicals permits reactions to begin only at the time of mixing and ootheca formation. Other protective substances produced by glands Accessory Glands include toxins and antibacterials. Diana E. Wheeler Nourishment for Embryos or Larvae University of Arizona Viviparous insects use accessory glands to provide nourishment directly to developing offspring. Tsetse flies and sheep keds are dip-T he accessory glands of reproductive systems in both female terans that retain single larvae within their reproductive tracts and and male insects produce secretions that aid in sperm mainte- provide them with nourishment. They give birth to mature larvae nance, transport, and fertilization. In addition, accessory glands ready to pupate. The gland that produces the nourishing secretion,in females provide protective coatings for eggs. Accessory glands can rich in amino acids and lipids, is known as the milk gland. The Pacificbe organs distinct from the main reproductive tract, or they can be beetle roach, Diploptera punctata, is also viviparous and provides itsspecialized regions of the gonadal ducts (ducts leading from the ova- developing embryos with nourishment secreted by the brood sac, anries or testes). Typically, glandular tissue is composed of two cell types: expanded portion of oviduct.one that is secretory and the other that forms a duct. The interplaybetween male and female secretions from accessory glands is a keyelement in the design of diverse mating systems. ACCESSORY GLANDS OF MALES Accessory glands of the male reproductive tract have diverse func- tions related to sperm delivery and to the design of specific mating ACCESSORY GLANDS OF FEMALES systems. Management of Sperm and Other Male Contributions Sperm management by females involves a wide range of proc- Sperm Deliveryesses, including liberation of sperm from a spermatophore, digestion Males of many insects use spermatophores to transfer sperm toof male secretions and sperm, transport of sperm to and from the females. A spermatophore is a bundle of sperm contained in a pro-spermatheca, maintenance of stored sperm, and fertilization. tective packet. Accessory glands secrete the structural proteins nec- Accessory gland secretions can have digestive functions impor- essary for the spermatophore’s construction. Males of the yellowtant in sperm management. First, digestive breakdown of the sper- mealworm, Tenebrio molitor, have two distinct accessory glands, onematophore can free encapsulated sperm for fertilization and storage. bean-shaped and the other tubular (Fig. 1). Bean-shaped accessorySecond, male contributions can provide an important nutritional glands contain cells of at least seven types and produce a semisolidbenefit to their mates. Female secretions can digest the secretory material that forms the wall and core of the spermatophore. Tubularcomponents of male seminal fluid to facilitate a nutritive role. In accessory glands contain only one type of cell, and it produces a mixaddition, females can digest unwanted sperm to transform it into of water-soluble proteins of unknown function. Spermatophores arenutrients. Third, female secretions in some species are required to not absolutely required for sperm transfer in all insects. In manydigest sperm coverings that inhibit fertilization. insects, male secretions create a fluid medium for sperm transfer. Transfer of sperm to and from the spermatheca is generallyaccomplished by a combination of chemical signals and muscularcontractions. Secretions of female accessory glands in some species Effects on Sperm Management and on the Femaleincrease sperm motility or appear to attract sperm toward the sper- The effects of male accessory gland secretions on the female aremathecae. Transport of fluid out through the wall of the spermatheca best known for the fruit fly, Drosophila melanogaster, in which themay also create negative pressure that draws in sperm. function of several gene products has been explored at the molecular
  • 38. 2 Aestivation level. Since insects have a diversity of mating systems, the specificA functions of accessory gland secretions are likely to reflect this variation. In Drosophila, the accessory glands are simple sacs consisting of a single layer of secretory cells around a central lumen (Fig. 2). Genes for more than 80 accessory gland proteins have been identified so far. These genes code for hormonelike substances and enzymes, as well as for many novel proteins. The gene products or their deriva- tives have diverse functions, including an increased egg-laying rate, a reduced inclination of females to mate again, increased effective- ness of sperm transfer to a female’s spermatheca, and various toxic effects most likely involved in the competition of sperm from differ- ent males. A side effect of this toxicity is a shortened life span for females. Other portions of the reproductive tract contribute secre- tions with diverse roles. For example, the ejaculatory bulb secretes one protein that is a major constituent of the mating plug, and another that has antibacterial activity. See Also the Following Articles FIGURE 1 Male reproductive system of T. molitor, showing tes- Egg Coverings ■ Spermatheca ■ Spermatophore tes (T), ejaculatory duct (EJD), tubular accessory gland (TAG), and bean-shaped accessory gland (BAG). [From Dailey, P. D., Gadzama Further Reading J. M., and Happ, G. M. (1980). Cytodifferentiation in the accessory Chen, P. S. (1984). The functional morphology and biochemistry of insect glands of Tenebrio molitor. VI. A congruent map of cells and their male accessory glands and their secretions. Annu. Rev. Entomol. 29, secretions in the layered elastic product of the male bean-shaped 233–255. accessory gland. J. Morphol. 166, 289–322. Reprinted by permission Eberhard, W. G. (1996). “Female Control: Sexual Selection by Cryptic of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.] Female Choice.” Princeton University Press, Princeton, NJ. Gillott, C. (1988). Arthropoda—Insecta. In “Accessory Sex Glands” (K. G. Adiyodi, and R. G. Adiyodi, eds.), Vol. 3 of “Reproductive Biology of Normal Invertebrates,” pp. 319–471. Wiley, New York. Happ, G. M. (1992). Maturation of the male reproductive system and its mc endocrine regulation. Annu. Rev. Entomol. 37, 303–320. Wolfner, M. F. (2001). The gifts that keep on giving: Physiological func- tions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85–93. eg ed (A) Transgenic Accessory glands Acoustic Behavior see Hearing Aedes Mosquito see Mosquitoes (B) FIGURE 2 Accessory gland of D. melanogaster. (A) The cells in this normal accessory gland express b-galactosidase driven by a promoter of a gene for an accessory gland protein. (B) A transgenic accessory gland, Aestivation cells expressing the gene have been selectively killed after eclosion. These flies were used to explore the function of accessory gland secre- Sinzo Masaki tions. In transgenic males, accessory glands are small and translationally Hirosaki University inert. [From Kalb, J. M., DiBenedetto, A. J., and Wolfner, M. F. (1993). A Probing the function of Drosophila melanogaster accessory glands estivation is a dormant state for insects to pass the summer by directed cell ablation. Proc. Natl Acad. Sci. USA 90, 8093–8097. in either quiescence or diapause. Aestivating, quiescent Copyright 1993, National Academy of Sciences, U.S.A.] insects may be in cryptobiosis and highly tolerant to heat and
  • 39. Aestivation 3drought. Diapause for aestivation, or summer diapause, serves notonly to enable the insect to tolerate the rigors of summer but also toensure that the active phase of the life cycle occurs during the favo- Arable time of the year. QUIESCENCE Quiescence for aestivation may be found in arid regions. Forexample, the larvae of the African chironomid midge, Polypedilumvanderplanki, inhabit temporary pools in hollows of rocks andbecome quiescent when the water evaporates. Dry larvae of thismidge can “revive” when immersed in water, even after years of qui-escence. The quiescent larva is in a state of cryptobiosis and toleratesthe reduction of water content in its body to only 4%, surviving evenbrief exposure to temperatures ranging from ϩ102°C to −270°C.Moreover, quiescent eggs of the brown locust, Locustana pardalina,survive in the dry soil of South Africa for several years until theirwater content decreases to 40%. When there is adequate rain, theyabsorb water, synchronously resume development, and hatch, result-ing in an outburst of hopper populations. The above-mentionedexamples are dramatic, but available data are so scanty that it is dif-ficult to surmise how many species of insects can aestivate in a stateof quiescence in arid tropical regions. SUMMER DIAPAUSE Syndrome The external conditions that insects must tolerate differ sharplyin summer and winter. Aestivating and hibernating insects may showsimilar diapause syndromes: cessation of growth and development,reduction of metabolic rate, accumulation of nutrients, and increasedprotection by body coverings (hard integument, waxy material,cocoons, etc.), which permit them to endure the long period of FIGURE 1 Bogong moths, Agrotis infusa, aestivating in aggre-dormancy that probably is being mediated by the neuroendocrine gation on the roof of a cave at Mt Gingera, A. C. T., Australia.system. [Photograph from Common, I. (1954). Aust. J. Zool. 2, 223–263, Migration to aestivation sites is another component of diapause courtesy of CSIRO Publishing.]syndrome found in some species of moths, butterflies, beetles, andhemipterans. In southeastern Australia, the adults of the Bogongmoth, Agrotis infusa, emerge in late spring to migrate from theplains to the mountains, where they aestivate, forming huge aggrega-tions in rock crevices and caves (Fig. 1). Seasonal Cues Summer diapause may be induced obligatorily or facultativelyby such seasonal cues as daylength (nightlength) and temperature.When it occurs facultatively, the response to the cues is analogousto that for winter diapause; that is, the cues are received duringthe sensitive stage, which precedes the responsive (diapause) stage.The response pattern is, however, almost a mirror image of that forwinter diapause (Fig. 2). Aestivating insects themselves also may FIGURE 2 Photoperiodic response in the noctuid M. brassicaebe sensitive to the seasonal cues; a high temperature and a long controlling the pupal diapause at 20°C. Note the different ranges ofdaylength (short nightlength) decelerate, and a short daylength (long photoperiod for the induction of summer diapause (dashed line) andnightlength) and a low temperature accelerate the termination of winter diapause (solid line). [From Furunishi et al. (1982), repro-diapause. duced with permission.] The optimal range of temperature for physiogenesis duringsummer diapause broadly overlaps with that for morphogenesis, or the superficial similarity in their dormancy syndromes, the two typesextends even to a higher range of temperature. Aestivating eggs of of diapause involve basically different physiological processes.the brown locust, L. pardalina, can terminate diapause at 35°C andthose of the earth mite, Halotydeus destructor, do this even at 70°C.The different thermal requirements for physiogenesis clearly distin- See Also the Following Articlesguish summer diapause from winter diapause, suggesting that despite Cold/Heat Protection ■ Diapause ■ Dormancy ■ Migration
  • 40. 4 Agricultural Entomology Further Reading of aggregate losses caused by insects as vectors of pathogens and para-A Common, I. F. B. (1954). A study of the biology of the adult Bogong moth, sites of humans and domestic animals, as agents causing direct damage to dwellings and other artificial structures, and as pests of crop plants Agrotis infusa (Boisd.) (Lepidoptera: Noctuidae), with special refer- and farm animals, but the amounts run to probably hundreds of bil- ence to its behaviour during migration and aestivation. Aust. J. Zool. 2, 223–263. lions of dollars annually. Losses caused by insects and vertebrate pests Furunishi, S., Masaki, S., Hashimoto, Y., and Suzuki, M. (1982). Diapause worldwide in the production of only eight principal food and cash response to photoperiod and night interruption in Mamestra brassicae crops (barley, coffee, cotton, maize, potato, rice, soybean, and wheat) (Lepidoptera: Noctuidae). Appl. Entomol. Zool. 17, 398–409. between 1988 and 1990 have been estimated at $90.5 billion. Hinton, H. E. (1960). Cryptobiosis in the larva of Polypedilum vanderplanki In the late 1800s and early 1900s, entomology became established Hint (Chironomidae). J. Insect Physiol. 5, 286–300. in many academic and research institutions as a discipline equal in Masaki, S. (1980). Summer diapause. Annu. Rev. Entomol. 25, 1–25. rank with botany and zoology. The diversity of insects and their eco- Matthée, J. J. (1951). The structure and physiology of the egg of Locustana nomic importance was the justification for ranking the study of a class pardalina (Walk.). Union S. Afr. Dep. Agric. Sci. Bull. 316, 1–83. of animals (Insecta) as being equivalent to the study of two kingdoms Tauber, M. J., Tauber, C. A., and Masaki, S. (1986). “Seasonal Adaptations of of organisms (plants and animals other than insects). Through the Insects.” Oxford University Press, New York. first half of the twentieth century, there was a schism between basic and applied (or economic) entomology. Since then, common use of the expression “economic entomology” has declined, being replaced by designations of its principal branches, such as agricultural ento- mology, forest entomology, urban entomology, and medical and vet- Africanized Bees erinary entomology. A detailed historical account is beyond the scope of this article, but Table I provides a chronology of some landmarks see Neotropical African Bees in the development of agricultural entomology through the ages. The realm of agricultural entomology includes all basic studies of beneficial and pest insects associated with agricultural crops and farm animals. This article deals mainly with crops, but the general principles and concepts are equally applicable to farm animals. The Agricultural Entomology starting point of such studies is a correct identification of the insect species, in accordance with the science known as biosystematics. Marcos Kogan Oregon State University BIOSYSTEMATICS Scientific nomenclature is a powerful tool for obtaining informa- tion about the basic biology of closely related species within a genus. Ronald Prokopy† When systematic studies have been extended beyond the naming of University of Massachusetts species (taxonomy) and contain detailed information on geographic distribution, host records, and biology of one or more species in a T he study of all economically important insects is the object genus, it is often possible to extrapolate the information to other of the subdiscipline “economic or applied entomology.” closely related species of that genus. Although details of the biology Agricultural entomology, a branch of economic entomology, must be ascertained for each individual species, biosystematics offers is dedicated to the study of insects of interest to agriculture because a blueprint to follow when dealing with a new pest. For example, the they help increase crop production (e.g., pollinators); produce a genus Cerotoma (Coleoptera: Chrysomelidae) contains 10–12 species commodity (e.g., honey, silk, lacquer); cause injury leading to eco- distributed from southern Brazil to the northeastern United States. All nomic losses to plants grown for food, feed, fiber, or landscaping; seem to be associated with herbaceous plants in the family Fabaceae cause injury to farm animals; or are natural enemies of agricultural (bean family). The biology of two of the species, C. trifurcata in North pests and, therefore, considered to be beneficial. Study of all fun- America and C. arcuata in South America (Fig. 2), has been studied damental aspects of the ecology, life history, and behavior of insects extensively. Based on information for these two species, it is possible associated with agricultural crops and farm animals falls within the to infer that the other species in the genus share at least some of the realm of agricultural entomology. These studies provide the founda- following features: eggs are laid in the soil adjacent to growing legumi- tion for the design and implementation of integrated pest manage- nous plants; larvae feed on nitrogen-fixing root nodules and pupate in ment (IPM) programs (Fig. 1). soil inside pupal cases; first-generation adults emerge when seedlings emerge, and second-generation adults emerge when plants are in full ECONOMIC ENTOMOLOGY vegetative growth, feeding first on foliage and, later on, switching to feeding on developing pods. The biosystematic information on the Insects are regarded by some as the main competitors of humans genus allows students of agricultural entomology in South, Central, or for dominance on the earth. Humans depend on insects for pollination North America to understand, at least in general terms, the role of of many crops, for production of honey and silk, for the decomposition any other species of Cerotoma within their particular agroecosystem. of organic matter and the recycling of carbon, and for many other vital The flip side of this notion is recognition that closely related and ecological roles. But it is the negative impact of insect pests that has morphologically nearly undistinguishable (sibling) species may have been of greatest concern to humans. There are no reliable estimates many important biological differences. Examples of the critical need for reliable biosystematics studies are found in the biological control † Deceased May 14, 2004. literature. The present account is based on studies conducted by Paul
  • 41. Agricultural Entomology 5 System integr s ation and information system A Biological control Behavioral control Chemical control Cultural control Plant resistance Genetic control Integrated pest management bridge Weed science Rural sociology Plant Crop Crop pathology protection Agricultural production Agricultural economics entomology Biological Social sciences sciences The flowing river of societal needs and demandsFIGURE 1 A bridge metaphor: agricultural entomology is conceived as one of the main pillars, together with plant pathology and weedscience, supporting the “integrated pest management bridge.” The bridge connects two-way “traffic” between crop production and cropprotection. The other pillar is provided by the social sciences of economics and sociology. The main tension cables, which are system inte-gration and information systems, hold the vertical lines that together give stability to the bridge; these are the tactical components of IPM.Under the bridge runs the “river” of ever-shifting societal needs and demands. TABLE I Some Landmarks in the Historical Development of Agricultural Entomology Significant events Years ago from 2000 Date Beginnings of agriculture 10,000 8000 B.C.E. First records of insecticide use 4,500 2500 B.C.E. First descriptions of insect pests 3,500 1500 B.C.E. Soaps used to control insects in China 900 1100 Beginning of scientific nomenclature—10th edition of Linnaeus, Systema Naturae 242 1758 Burgeoning descriptions of insects 100–200 18th and 19th centuries First record of plant resistance to an insect 169 1831 Charles Darwin and Alfred Wallace jointly present paper on the theory of evolution 142 1858 First successful case of biological control: the cottony cushion scale, on citrus, in California, by 112 1888 the vedalia beetle First record of widespread damage of cotton in Texas by the cotton boll weevil 106 1894 First record of an insect resistant to an insecticide 86 1914 First edition of C. L. Metcalf and W. P. Flint’s Destructive and Useful Insects 72 1928 Discovery of DDT and beginning of the insecticide era 61 1939 First report of insect resistance to DDT 54 1946 Term “pheromone” coined by P. Karlson and P. Butenandt, who identified first such substance 45 1959 in the silkworm moth First edition of Rachel Carson’s Silent Spring 48 1962 Expression “integrated pest management” first appears in the press 32 1968 Rapid development of molecular biology 20 1980s Release of Bt transgenic varieties of cotton, corn, and potato 5 1990s Based in part on Norris et al. (2003).DeBach, one of the leading biological control specialists of the twen- of confusion and missed opportunities because of misidentification oftieth century. The California red scale, Aonidiella aurantii, is a seri- its parasitoids. The red scale parasitoid Aphytis chrysomphali had beenous pest of citrus in California and other citrus-producing areas of the known to occur in California and was not considered to be a very effec-world. Biological control of the red scale in California had a long history tive control agent. When entomologists discovered parasitized scales
  • 42. 6 Agricultural Entomology Yield type Defining factors: CO2A 1 Potential Radiation Temperature Crop genetics -Crop physiology -Crop phenology -Canopy architecture Limiting factors: Water 2 Attainable Nutrients -Nitrogen -Phosphorus Yield-increasing -Potassium measures Reducing factors: Insect pests 3 Actual Vertebrates Pathogens Yield-protecting Weeds measures Pollutants 1500 5000 10,000 20,000 Production level (kg ha–1) FIGURE 3 Factors impacting the yield potential of a generic crop. (Adapted from information on a Web site originated at IMI/ University of Miami, Summer Institute.) FIGURE 2 Morphological diversity and biological similarities in the genus Cerotoma: four of the dozen known species are illustrated To assess crop losses and attribute the losses to a specific cause by male and female specimens. The species are clearly distinguish- (e.g., the attack of a pest) requires setting up experiments to isolate able by morphological characters, but they have similar life histories the effect of the pest from all other constraints. Methodologies vary and behaviors. (From unpublished drawings by J. Sherrod, Illinois with pest category—whether the pests are insects, vertebrates, plant Natural History Survey.) pathogens, or weeds, for example. The quantitative relationship between crop losses and pest population levels is the basis for com- puting the economic injury level for the pest. The economic injury during foreign exploration, the parasitoids were misidentified as A. level is a fundamental concept in IPM. chrysomphali and therefore were not imported into California. It was later discovered that the parasitoids were in fact two different species, A. lingnanensis and A. melinus, both more efficient natural enemies of LIFE HISTORY AND HABITS the California red scale than A. chrysomphali. Now A. lingnanensis and Once the identity and pest status of a species have been well A. melinus are the principal red scale parasitoids in California. Further established, it becomes essential to extend the informational base biosystematics studies have shown that what was once thought to be on the life history and habits of the species to the conditions under single species, A. chrysomphali, parasitic on the California red scale in which the crop is grown. Economically important life history traits the Orient and elsewhere, and accidentally established in California, is include information on developmental threshold temperatures and in fact a complex including at least seven species having different bio- temperature-dependent developmental rates. These data are used in logical adaptations but nearly indistinguishable morphologically. modeling the phenology of the pest. Other essential studies include Knowledge of the name of a species, however, is not an indication the orientation, feeding, host selection, and sexual behavior of the of its true potential economic impact or pest status. A next impor- species. Many of these studies provide the foundation for strategic tant phase in agricultural entomology is, therefore, the assessment of planning in IPM and for the development of target-specific control benefits or losses caused by that species. tactics. For example, the study of sexual behavior can involve the definition of the role of pheromones in mating and the identification PEST IMPACT ASSESSMENT of those pheromones. These, in turn, may be used for monitoring pest incidence and abundance or in mating disruption, both valuable The mere occurrence of an insect species in association with a components of IPM systems for many crops. The study of host selec- crop or a farm animal does not necessarily mean that the species is tion behavior often leads to the identification of kairomones, equally a pest of that crop or animal. To be a pest it must cause economic important in IPM development. losses. The assessment of economic losses from pests is the subject of studies conducted under conditions that match as closely as pos- sible the conditions under which the crop is grown commercially PHENOLOGY or the animals are raised. Much of the methodology used in crop The life cycle of different insect species varies greatly, although loss assessment has been established under the sponsorship of the all insects undergo the basic stages of development from egg to Food and Agriculture Organization (FAO) of the United Nations as reproductive adult (or imago). Depending on the length of the life a means of prioritizing budget allocations and research efforts. Key cycle, there is considerable variation in the number of generations data for these studies relate to the determination of the yield poten- per year, a phenomenon called voltinism. A univoltine species has tial of a crop. The genetic makeup of a crop variety determines its one generation per year; a multivoltine species may have many gen- maximum yield in the absence of adverse environmental factors. erations per year. The range of variation in the Insecta is evident This is known as the attainable yield. To determine the attainable when one considers that the 17-year periodical cicada has one gener- yield, the crop is grown under nearly ideal conditions; the actual ation every 17 years, whereas whiteflies or mosquitoes may complete yield is what occurs when the crop is grown under normal farming a generation in about 21 days. Under temperate climate conditions, conditions. The difference between attainable and actual yields is a generations often are discrete, but under warmer subtropical condi- measure of crop loss (Fig. 3). tions, they frequently overlap. The definition of temporal periodicity
  • 43. Agricultural Entomology 7in an organism’s developmental cycle is called phenology. The rela- The set of species coexisting in an area and interacting to varyingtionship between the phenology of the crop and the phenologies ofits various pests is of interest in agricultural entomology. Fig. 4 shows degrees form what is known as an ecological community. In a crop community, the crop plants and the weeds that persist within the Aan example of such a relationship for soybean grown under condi- crop field or grow along the borders are the primary producers. Thetions typical for the midwestern United States. animals within the crop community maintain dynamic trophic rela- tionships: some feed on living plants, others on the decaying plants, POPULATION AND COMMUNITY ECOLOGY and still others on animals. Those that feed on the plants are the her- bivores, or primary consumers. Pests are primary consumers on the Population and community level studies are within the scope of crop plants. Parasitoids and predators are the secondary consumers.insect ecology. Although the species is the focal biological entity for Those that feed on the pests are beneficial natural enemies. Finally,agricultural entomology, for management purposes it is essential to decomposers and detritivores feed on decaying organic matter. Allunderstand population and community level processes. Populations biotic components of the community are interconnected by “foodare assemblages of conspecific individuals within a defined geograph- webs.” An understanding of food webs and trophic interactions inical area (e.g., a crop field, a river valley, a mountain chain). Many crop communities is important because it provides a basis for inter-insects have a large reproductive capacity. As calculated by Borror, preting the nature of disturbances in crop ecosystems. DisturbancesTriplehorn, and Johnson, a pair of fruit flies (Drosophila), for exam- in trophic relations may lead to outbreaks of pest organisms and theple, produces 100 viable eggs, half of which yield females that in need for control actions.turn will lay 100 eggs and so on for 25 possible generations in 1 year;by the end of the year, the twenty-fifth generation would contain1.192 ϫ 1041 flies, which, if packed tightly together, 60,000 to a liter, LINKS TO IPM SYSTEMS DEVELOPMENTwould form a ball of flies 155 million kilometer in diameter or a ball With the advent of IPM and its success in the last third of theextending approximately from the earth to the sun. Obviously, such twentieth century, it has become difficult to separate agriculturalunlimited population growth does not occur in nature. Normally, entomology from IPM. In entomology, the two fields of endeavorpopulations are regulated by the combined actions of both physi- are inextricably interconnected. A reliable database of biologicalcal (or abiotic) and biological (or biotic) factors of the environment. information provides the means to design and develop IPM strate-An understanding of the mortality factors that help regulate insect gies. For example, there is growing interest in methods of enhanc-populations is one of the most active areas of research in agricultural ing biological control through habitat management. The techniqueentomology. requires information on source–sink relationships among pests and Maturation Podding Harvest Blooming Emergence Planting Overwintering Overwintering Overwintered adults Overwintering adults Larvae Eggs & Adults in other crops & nymphs Overwintering wild vegetation adults Adults Larvae Adults migrate Local population from south dies in winterFIGURE 4 Crop phenology and pest phenology: relationship between the phenology of soybean in the midwestern United States andthree of its most common insect pests, the bean leaf beetle, C. trifurcata (Coleoptera: Chrysomelidae); the green stink bug, Acrosternumhilare (Hemiptera: Pentatomidae); and the green cloverworm, Hypena scabra (Lepidoptera: Noctuidae).
  • 44. 8 Amber natural enemies across crop plants, neighboring crops, natural vege- Price, P. W. (1997). “Insect Ecology.” Wiley, New York.A tation, and especially managed vegetation in the form of cover crops and field hedges. Theoretically, diversification of the crop ecosystem Schowalter, T. D. (2000). “Insect Ecology: An Ecosystem Approach.” Academic Press, San Diego, CA. leads to an increase in natural enemies and to greater stability of the system. The complexity of interactions, however, makes it difficult to interpret conflicting results of experiments designed to test working hypotheses. The analysis of within-field and interfield movement, the host selection behavior of phytophagous and entomophagous insects, multitrophic interactions among community members, and Alderfly see Megaloptera the dynamics of populations, all under the scope of agricultural ento- mology, are only a few of the many components of the knowledge base necessary to develop advanced IPM systems. The advent of the World Wide Web has had a major influence on accessibility to basic information on agricultural entomology. Most major agricultural research centers have developed Web pages that Amber organize information and make it available to students worldwide. More importantly, the dynamic nature of the Web offers the oppor- George Poinar Jr. tunity to provide weather-driven modeling capabilities that greatly Oregon State University increase the scope and applicability of studies about the phenology A and population dynamics of major pest organisms. Two sites that mber is a fossilized resin ranging from several million to 300 offer such capabilities are http://pnwpest.org/wea/ and http://www. million years of age. It has a melting point between 200°C and ipm.ucdavis.edu/PHENOLOGY/models.html. 380°C, a hardness of 2–3 on the Moh’s scale, a specific gravity Entomologists in the late 1800s and early 1900s studied the biol- between 1.04 and 1.10 and a surface that is insoluble to organic sol- ogy of insect pests in great detail. Articles and monographs pub- vents. Amber is a gold mine for the entomologist because it contains lished during that period remain valuable sources of information. a variety of insects preserved in pristine, three-dimensional condi- These early entomologists recognized that deep knowledge of the tion. Fossils in amber provide evidence of lineages dating back mil- life history of an insect and its habits could provide insights useful lions of years (Table I). External features are so well preserved that for the control of agricultural and other pests. The advent of organo- taxonomists can make detailed comparisons with living taxa to follow synthetic insecticides in the mid-1940s created the illusion that pest evolutionary development of families, genera and species. Aside from problems could be solved forever. Many entomologists redirected establishing direct evidence of an insect taxon at a particular time and their efforts to testing new chemicals and neglected basic insect biol- place, the presence of specific insects provides indirect evidence of ogy studies. The failure of insecticides to eradicate pests and the plants and vertebrates, establishes the time frame for symbiotic asso- environmental problems engendered by the misuse of these chemi- ciations, and provides clues for reconstructing ancient landscapes. cals led to the advent of IPM. For IPM to succeed, entomologists have had to return to the basics and again refocus their efforts on the study of insect biology. Agricultural entomology has come full circle as new generations of entomologists endeavor to refine knowledge of TABLE I the group of animals that remain humans’ most serious competitors. Significant Amber Deposits in the World Deposit Location Approximate age (million years) See Also the Following Articles Biological Control ■ History of Entomology ■ Integrated Pest Management ■ Baltic Northern Europe 40 Phytophagous Insects ■ Plant–Insect Interactions ■ Population Ecology Burmese Burma (Myanmar) 97–105 Canadian Alberta, Manitoba 70–80 Chinese Fushun Province 40–53 Further Reading Dominican Dominican Republic 15–40 French Charente-Maritime 100–105 Borror, D. J., Triplehorn, C. A., and Johnson, N. F. (1992). “An Introduction Hat Creek British Columbia, Canada 50–55 to the Study of Insects.” Saunders College Publishers and Harcourt Brace Lebanese, Jordanian Middle East 130–135 College Publishers, Philadelphia and Fort Worth. Mexican Chiapas 22–26 DeBach, P. (1964). “Biological Control of Insect Pests and Weeds.” Reinhold, New Jersey Northeastern United States 65–95 New York. Siberian (Taimyr) Russian arctic 78–115 Evans, H. E. (1984). “Insect Biology: A Textbook of Entomology.” Addison- Spanish Alava, Basque country; 100–115 Wesley, Reading, MA. San Just Huffaker, C. B., and Gutierrez, A. P. (1999). “Ecological Entomology.” Wiley, New York. Jones, D. P. (1973). Agricultural entomology. In “History of Entomology” (R. F. Smith, T. E. Mittler, and C. N. Smith, eds.), pp. 307–332. Annual Reviews, Palo Alto, CA. Recent searches for new amber deposits resulted in the discov- Norris, R. F., Caswell-Chen, E. P., and Kogan, M. (2003). “Concepts in ery of Cretaceous deposits in France, Spain and Jordan as well as Integrated Pest Management.” Prentice Hall, Upper Saddle River, NJ. Tertiary deposits in the Ukraine. An analysis of arthropods and plants Oerke, E. C. (1994). “Crop Production and Crop Protection: Estimated Losses in amber deposits has allowed workers to profile the original Baltic, in Major Food and Cash Crops.” Elsevier, Amsterdam and New York. Dominican, and Mexican amber forests.
  • 45. Amber 9 USE OF AMBER IN TRACING ARTHROPOD PROVIDING INDIRECT EVIDENCE OF OTHER LINEAGES ORGANISMS A As a result of the excellent preservation of amber arthropods, There are size and habitat limitations to the types of organismthe ancestry of specific genera and families can be traced back tens that were trapped in amber. For example, many plants would notof millions of years. An example is the family Ixodidae, the earliest normally have left flowers or leaves in the resin, and when they did,members of which appear in Burmese amber, thus demonstrating a these remains alone would likely be difficult to identify. Vertebrateslineage that has survived for 100 million years (Fig. 1). might have left hairs, feathers, or scales but these structures would also be difficult to identify. However, arthropods that are specific to certain hosts (e.g., ticks and mammals) can provide clues to plants and vertebrates that existed at that time. This use of fossils relies heavily on the principle of behavioral fixity, which asserts that, at least at the generic level, the behavior of a fossil organism would have been similar to that of its present-day descendants. Many insects form specific associations with plants and their presence indicates the occurrence of specific families and even gen- era of plants in the environment. Thus certain types of palm bugs in Dominican amber provide indirect evidence that pinnately leafed palms existed in the original amber forest. Fig wasps in Dominican amber provide evidence that figs grew in that ancient habitat. Palm bruchids in Cretaceous Canadian amber provide indirect evidence of Sabal palms in the original ecosystem. Orchid pollinia attached to insects provide yet another way to determine the presence of plants that would normally not be found in the fossil record. PROVIDING INDIRECT EVIDENCE OFFIGURE 1 The oldest known hard ticks of the family Ixodidae SPECIFIC HABITATSare found in early Cretaceous Burmese amber. The one shown here,described as Compluriscutula vetulum, has two more scutes than Amber insects can provide evidence of specific habitats. Divingfound in extant ticks. beetles (Coleoptera: Dytiscidae), caddisflies (Trichoptera), and dam- selflies (Odonata) all provide evidence of aquatic habitats. The first fossil anopheline mosquito from the New World, Anopheles domini- Discovering extinct generic and family lineages is also possible, canus, in Dominican amber, belongs to a group that normally ovipos-especially in Cretaceous amber. Many of these have characters link- its in ground pools. Other insects provide evidence of phytotelmataing them to more than one extant group and some have morphologi- (standing water in plant parts), wood, moss, bark, and detritus.cal features that no longer exist in extant insects. The early Cretaceoussolitary bee, Melittosphex burmensis, contains some wasp-like charac- PALEOSYMBIOSISters, which separate it from all extant families. Thus it was describedin the extinct family, Melittosphecidae (Fig. 2). Other unique extinct Because of the sudden death of captured organisms in amber,lineages include the Burmese amber ant-like stone beetle, Hapsomela symbiotic associations may be preserved in a manner unlikely toburmitis (Hapsomelinae) which has forelegs with an extra segment, the occur with other types of preservation. Also, the fine details ofprimitive crane fly, Dacochile microsoma, which has characters found preservation may reveal morphological features characteristic ofin two extant families of flies (Tanyderidae and Psychodidae), a family symbiotic associations. Cases of paleosymbiosis in amber includeof aphids (Parvaverrucosidae) with the hind wings reduced to hamulo- inquilinism, commensalism, mutualism, and parasitism.halters characteristic of scale insects and the Burmese amber hard tick, Paleoinquilinism involves two or more extinct organisms livingCornupalpatum burmanicum, which has both mite and tick characters. in the same niche but neither benefiting nor harming each other. Numerous insects form inquilinistic associations under tree bark, and many pieces of amber contain flies and beetles common to this habitat. Phoresis (one organism transported on the body of another organ- ism) is probably the most typical type of paleocommensalism in amber. This usually involves mites and pseudoscorpions being carried by insects. The arachnid benefits by being conveyed to a new environ- ment, where the food supply is likely to be better than the last one. The carrier generally is not harmed and only serves as a transporting agent. In paleomutualism, both organisms benefit and neither is harmed. Amber bees carrying pollen or pollinia provide evidence of insect–plant mutualism in which the bee obtains a food supply and the plant is pollinated. An example of insect–insect mutualism is demonstrated by a rare fossil riodinid butterfly larva in DominicanFIGURE 2 The primitive early Cretaceous solitary bee, Melittosphex amber. Specialized morphological features of this Theope caterpillarburmensis, in Burmese amber still retains some wasp characters. indicative of a symbiotic association are balloon setae and vibratory
  • 46. 10 Amber papillae in the neck area, and tentacle nectary organ openings on the one that causes Chagas disease today (Fig. 4). The presence of a batA eighth abdominal tergite. Extant caterpillars in this genus have simi- lar features and are associated with ants. The tentacle nectary organs hair adjacent to the triatomid indicates the likely vertebrate host. A Dominican amber mosquito infected with Plasmodium dominicana provide nourishment for the ants, whereas the vibratory papillae shows that at least one lineage of Plasmodium was already estab- (which beat against the head capsule and make an audible sound) lished in the New World long before humans arrived on the scene. and balloon setae (which emit a chemical signal) are used to attract ants when the caterpillar is threatened by an invertebrate predator or parasite. This fascinating association between butterfly larvae and ants was established at least 20 mya. Paleoparasitism by insects is very difficult to verify in the fossil record. There are many records of amber insects (especially wasps and flies) whose descendants today are parasitic on a wide range of organisms, but to discover an actual host–parasitic association is quite rare. However, there are reported cases of braconid larvae emerging from ants and adult trichopterans in Baltic amber. Paleoectoparasitism is the most obvious of all parasitic associations found in amber. The ectoparasite is often still attached to its host, and systematic studies can be conducted on both organisms. In amber, ectoparasites are usually the larvae of parasitic mites, such as the larvae of Thrombididae or Erythraeidae attached to various insects. These larval mites feed on the host’s hemolymph, then exit the insect and molt to the nymphal and adult stages, when they become free- living predators. Such parasitic mites are not to be confused with FIGURE 4 The first vertebrate-parasitic hemipteran, Triatoma phoretic ones, which are simply carried around by insects. dominicana, in Dominican amber was a vector of Trypanosoma Paleoendoparasitism is extremely difficult to verify because inter- antiquus, closely related to the causal agent of Chagas disease. nal parasites are rarely preserved as fossils. However, some parasites attempt to leave their hosts when they encounter resin. Mermithid nematodes (members of the genera Heydenius and Cretacimermis) A Cretaceous sand fly (Palaeomyia burmitis) with the remains of and hairworms (Nematomorpha) of the genera Palaeochordodes that a blood meal containing trypanosomatids in its midgut and infected have nearly completed their development often reveal their pres- reptilian cells in its foregut indicated that it was feeding on a reptile ence when they attempt to leave the host and become trapped in the infected with the Leishmania-like flagellate, Paleoleishmania proterus resin. Under normal conditions, they would enter soil or water and (Fig. 5). A Burmese amber biting midge (Diptera: Ceratopogonidae) initiate a free-living existence. infected with a primitive type of malaria (Paleohaemoproteus burmacis) Tracing the history of insect pathogens and parasites is also had characteristics indicating that it fed on large, cold-blooded ver- possible using amber. Insect diseases involving protozoa, viruses, tebrates. The presence of these diseases in the Cretaceous certainly nematodes, and fungi have been discovered in both Tertiary and meant that dinosaurs were also infected and widespread epidem- Cretaceous amber (Fig. 3). Indirect evidence of vertebrate parasitism ics could have contributed to the debilitation and demise of these can be obtained by a microscopic examination of vectors in amber. behemoths. Not only can the types of vertebrate pathogens be determined, but also what vertebrate groups were being attacked. A hematopha- gous bug (Tritoma dominicana) in Dominican amber was associ- ated with a trypanosomatid (Trypanosoma antiquus) resembling the FIGURE 5 The Burmese amber sand fly, Palaeomyia burmitis, contains various stages of the trypanosomatid, Paleoleishmania pro- terus, in its midgut and infected reptilian blood cells in its foregut. FIGURE 3 Evidence of paleoparasitism is shown by a superficial This not only shows that vectors of vertebrate diseases were present fungal infection caused by a member of the entomophthorales on 100 million years ago but also provokes the question as to how dino- the thorax of a mycetophilid fly in Dominican amber. saurs would have dealt with such emerging pathogens.
  • 47. Anatomy: Head, Thorax, Abdomen, and Genitalia 11 BIOGEOGRAPHICAL STUDIES Amber insects can provide evidence of past distributions as well Anatomy: Head, Thorax, Aas clues to climatic regimes that occurred at the original sites. Thereare many examples of amber insects at sites that are located far fromtheir descendants’ current habitat. Examples from Dominican amber Abdomen, and Genitaliainclude Mastotermes termites (Isoptera: Mastotermitidae) andLeptomyrmex ants (Hymenoptera: Formicidae) that were part of the David H. Headrickinsect fauna some millions of years ago in the Caribbean but occur California Polytechnic State Universitynowhere in the New World today. Both genera are represented todayby single relict species in the Australian region. A North American example is the presence of tropical arboreal Gordon Gordhants of the genus Technomyrmex (Hymenoptera: Formicidae) in U.S. Department of AgricultureEocene Hat Creek amber in British Columbia, Canada, hundreds of Akilometers north of their present-day range. These ants provide evi- natomy is a subdiscipline of morphology concerned withdence that the climate in that region of the world was tropical to sub- naming and describing the structure of organisms based ontropical in the Eocene. Other examples of past distributions involve gross observation, dissection, and microscopical examination.the mosquito, Toxorhynchites mexicanus, in Mexican amber, which Morphology and anatomy are not synonyms. Morphology is con-belongs to a subgenus that today is restricted to the Old World. cerned with the form and function of anatomical structure; becauseThere are many examples of insect genera in Dominican amber that anatomy is an expression of organic evolution, morphology seeks tono longer occur in the Dominican Republic or the Greater Antilles investigate possible explanations for organic diversification observedtoday, but still have living representatives in Mexico, and Central in nature. Before 1940, insect morphology focused on naming andand South America. Some examples are members of the butter- describing anatomical structure. The need for this activity has notfly genus Theope (Lepidoptera: Riodinidae) and the stingless bee diminished, as there is much about insect anatomy remains to begenus Proplebeia (Hyemnoptera: Apidae). Further evidence of cli- revealed, described, and understood. This article focuses on thematic shifts over time is clear with many Baltic amber insects whose anatomical structures of the three major tagmata of the insect body:descendants occur in the Old World tropics today. head, thorax, and abdomen, and on the external genitalia. A hypo- thetical ground plan for major structures is given, followed by themes RECONSTRUCTING ANCIENT LANDSCAPES in anatomical variation based on adaptation observed in the Insecta. Every amber fossil tells a story and is a piece of a jigsaw puzzlethat can be used to reconstruct the natural environment at the time CONTEXT OF ANATOMICAL STUDYthe amber was being produced. The challenges are to identify the Terms of Orientation and Conventionsinclusions, determine their biology and ecology by researching thehabits of their extant descendants, and then make inferences regard- Terms to describe orientation are not intuitive for insects. Mosting the original environment. There will always be gaps in the puz- orientation terms are derived from the study of the human body—azle because there are many life-forms that are too large to become body that stands upright—and their application to insects causesentrapped in amber or have a lifestyle that does not normally bring confusion. Some standard terms used with insects include anteriorthem into contact with the sticky resin. However, the habitat that (in front), posterior (behind), dorsal (above), ventral (below), medialexisted in that ancient world can, in large part, be reconstructed by (middle), and lateral (side). Anatomical description usually follows instudying select insects that can be typified as phytophagous, detriti- the same order; hence, we begin our discussion with the head, movevores, bark inhabitants, or parasites. As pointed out earlier, plants, on to the thorax and then the abdomen, and finish with the genitalia.insect prey, and vertebrate hosts can often be identified indirectly by Description of the relative placement of anatomical features can bediscovering fossils which are dependent upon them today. cumbersome, but they are critical elements in the study of anatomi- cal structure because relative position is one of the three basic tenets of homology, including size, shape, and embryology.Further ReadingKaddumi, H. F. (2005). “Amber of Jordan.” Kaddumi Publications, Amman, Jordan. Measures of SuccessPoinar, G. O., Jr. (2005). Triatoma dominicana sp. n. (Hemiptera: Reduviidae: The design of the insect body can be described as successful for Triatominae), and Trypanosoma antiquus sp. n. (Stercoraria: Trypanoso- many reasons: there are millions of species, they range in size over matidae), the first fossil evidence of a triatomine-trypanosomatid vector four orders of magnitude, their extensiveness of terrestrial and association. Vector-borne Zoonotic Dis. 5, 72–81. aquatic habitat exploitation (the diversity of resources), and once aPoinar, G. O., Jr. (2005). Plasmodium dominicana n. sp. (Plasmodiidae: successful form has been developed, there appears to be relatively Haemospororida) from Tertiary Dominican amber. Syst. Parasitol. 61, little change over evolutionary time (Fig. 1). The basic insect design 47–52.Poinar, G. O., Jr., and Poinar, R. (2008). “What Bugged the Dinosarus?.” allows for adaptation to a variety of environmental requirements. Princeton University Press, Princeton, NJ. The success of the design is rooted in the nature of the main mate-Ross, A. (1998). “Amber.” Harvard University Press, Cambridge, MA. rial used for its construction.Solórzano Kraemer, M. M. (2007). Systematic, palaeoecology, and palaeobio- geography of the insect fauna from Mexican amber. Palaeontographica A The Building Material 282, 1–133.Weitschat, W., and Wichard, W. (2002). “Atlas of Plants and Animals in Baltic When we look at an insect, it is the integument that we see. Amber.” Pfeil, Munich. Structurally, the integument is a multiple-layered, composite organ
  • 48. 12 Anatomy: Head, Thorax, Abdomen, and Genitalia anterior and posterior margins of each somite. These rings representA intersegmental lines of the body wall and define the limits of each somite. Internally, the grooves coincide with the lines of attachment of the primary longitudinal muscles. From a functional standpoint, this intrasegmental, longitudinal musculature permits flexibility and enables the body to move from side to side. More complex plans of body organization exhibit structural modi- fications. Secondary segmentation is characteristic of hard-bodied arthropods, including adult and nymphal insects. Secondary body segmentation is an evolutionarily derived anatomical feature. The musculature we see in secondary segmentation is intersegmental, or FIGURE 1 Fossil insects are easily recognizable today, indicating between segments (Fig. 2). The acquisition of secondary segmen- an early establishment of a successful design. Left to right: Heplagenes tation represents a major evolutionary step in the development of (Late Jurassic 150 mya, Liaoning, China); cricket (Eocene, 50 mya, the Arthropoda. The soft-bodied arthropod has primary segmenta- Green River formation, Utah); fulgorid (Eocene, 50 mya, Green River tion and muscles that are intrasegmental, or within each segment. formation, Utah). Movement of the body and its parts is relatively simple because the body wall is flexible. However, when the body wall becomes hard- ened, flexibility is restricted to the articulation between hardened that defines body shape, size, and color. The ultrastructure of the parts or the extension provided by intersegmental membranes. The integument is composed of living cells and the secretory products of arthropod is, in a metaphorical sense, clad in a suit of armor; most those cells. Each layer is of a different thickness and chemical com- movement is possible only if soft and flexible membranes are posi- position, and each displays physical properties different from those tioned between inflexible (hardened) body parts. Exceptions may be of the surrounding layers. Perhaps more importantly, the integument seen in the indirect flight mechanism of pterygote insects. is also the organ with the greatest diversity of structure and function. There are two common misconceptions about the integument. Occiput Pronotum Acrotergite Mesonotum Membrane First, some believe chitin is responsible for integument in the soft Head Postnotum and flexible membranous parts of the integument than in the hard, Intersegmental sclerotized plates. Integument hardness is attributed to an increased membrane number of cross-linkages between protein chains contained in the Intersegmental First abdominal tergite integument layers. Second, some believe that the integument is rigid muscle and that growth is incremental and limited to expansion during mol- Phragma ting; yet, some endopterygote insects are able to grow continuously FIGURE 2 Secondary segmentation. Diagram of sagittal section between molts. of dorsal sclerites of thorax. The integument determines the shape of the insect body and its appendages. One of the most captivating features of insects is their seemingly infinite variation in body shapes—everything from In all probability secondary segmentation evolved many times, a simple bag (Hymenoptera grub) to a mimic of orchid flowers and it probably continues to evolve in response to specific problems (Mantidae). Similarly, appendage shape is exceedingly plastic. Terms confronting insects today. Secondary segmentation is most evident such as “pectinate,” “flabbate,” and “filiform” are among more than and most readily appreciated in the insect abdomen. It is less appar- 30 terms taxonomists have proposed to describe antennal shapes. ent in the thorax and almost totally obscured in the head. Leg shapes are similarly highly variable and express functional modi- fications. Among these shapes are “cursorial,” “gressorial,” “rapto- rial,” “fossorial,” and “scansorial.” Again, these modifications of shape Sclerites reflect the function of structure. Finally, wing shapes are highly vari- The hardening of the body wall contributes significantly to the able among insects and are determined by body size and shape as external features observed in insects. Sclerites are hardened areas of well as by aerodynamic considerations. the insect body wall that are consequences of the process of sclero- tization. Sclerites, also called plates, are variable in size and shape. Tagmata Sclerites do not define anatomical areas and do not reflect a com- mon plan of segmentation. Sclerites develop as de novo hardening Most people recognize the three tagmata—head, thorax, and of membranous areas of the body wall, as de novo separations from abdomen—as characteristic of insects. The way they appear is rooted larger sclerotized areas of the body, and in other ways. in a division of responsibilities. The head is for orientation, ingestion, The hardened insect body displays many superficial and inter- and cognitive process; the thorax for locomotion; and the abdomen nal features that are a consequence of hardening. Understanding for digestion and reproduction. But even casual observations reveal the distinction between these conditions and the terms applied to further divisions of these body regions. them is critical in understanding insect anatomy and its application in taxonomic identification. These features are of three types. First, Segmentation of the Tagmata sutures (Latin, sutura ϭ seam), in the traditional sense of vertebrate Two types of segmentation are evident among arthropods, pri- anatomists, provide seams that are produced by the union of adjacent mary and secondary. Primary segmentation is characteristic of soft- sclerotized parts of the body wall. On the insect body, sutures appear bodied organisms such as larval holometabolans. The body wall in as etchings on the surface of the body and form lines of contact these organisms is punctuated by grooves or rings that surround the between sclerites. Second, sulci (Latin, sulcus ϭ furrow) represent
  • 49. Anatomy: Head, Thorax, Abdomen, and Genitalia 13any externally visible line formed by the inflection of cuticle. AntennaBiomechanically, a sulcus forms a strengthening ridge. In contrast,lines of weakness are cuticular features that are used at molting. Vertex ALines of weakness are frequently named as if they were sutures, butthey should not be viewed as such. For instance, the ecdysial cleav- Lateral ocellusage line is a line of weakness that is sometimes considered to be syn- Compound eyeonymous with the epicranial suture. The two features are similar in Fronsposition and appearance, but structurally they may have been derivedfrom different conditions. Finally, apodemes (Greek, apo ϭ away; Anterior tentorial pitdemas ϭ body) are hardened cuticular inflections of the body wall Frontoclypeal suturethat are usually marked externally by a groove or pit. Structures Clypeuscalled apophyses (Greek, apo ϭ away; phyein ϭ to bring forth) arearmlike apodemes. Apodemes have been defined as a hollow invagi- Clypeolabral suturenation or inflection of the cuticle and an apophysis as a solid invagi- (A) Labrumnation. Functionally, apodemes strengthen the body wall and serve asa surface for muscle attachment. Sclerites receive different names depending upon the region of Vertexthe body they are located. Tergites (Latin, tergum ϭ back) are scle-rites that form a subdivision of the dorsal part of the body wall (ter- Epicranial suturegum). Latrotergites are sclerites that form as a subdivision of thelateral portion of the tergum. Sternites (Latin, sternum ϭ breastbone) are sclerites that form as a subdivision of the ventral part of Frontal suturethe body wall (sternum), or any of the sclerotic components of thedefinitive sternum. Pleurites (Greek, pleura ϭ side) are sclerites inthe pleural region of the body wall that are derived from limb bases. (B) HEAD FIGURE 3 (A) Anterior view of the head of a grasshopper The head is a controversial area for anatomical nomenclature, (Orthoptera: Acrididae). (B) Larval pterygote head showing epicra-but it provides some of the best examples of evolutionary trends in nial and frontal sutures (Lepidoptera: Noctuidae).anatomy. Most insect morphologists believe that the head of moderninsects represents the fusion of several segments that were present in The frons is that part of the head immediately ventrad of the ver-an ancestral condition. However, the number of segments included tex (Fig. 3A). The frons varies in size, and its borders are sometimesin the ground plan of the insect head has been a contentious issue difficult to establish. In most insects the frons is limited ventrallyamong morphologists for more than a century. Any argument that by the frontoclypeal suture (epistomal suture), a transverse sutureattempts to explain head segmentation must take into account com- located below the antennal sockets. As its name implies, the sutureparative anatomical, embryological, and paleontological evidence, separates the dorsal frons from the ventral clypeus (Fig. 3A).and must examine modern forms of ancestral insects. The face is a generalized term used to describe the anteromedial portion of the head bounded dorsally by the insertion of the anten- Ground Plan of the Pterygote Head nae, laterally by the medial margins of the compound eyes, and ven- Given the difficulty in homologizing anatomical features of the trally by the frontoclypeal suture. In some insects the area termedhead, we describe regions associated with landmarks of a ground plan the face is coincident with some, most, or all of the frons.or an idealized hypognathous insect head. In terms of modern insects, The clypeus (Latin, shield) is a sclerite between the face andthe Orthoptera probably come closest to displaying all the important labrum (Fig. 3A). Dorsally, the clypeus is separated from the face orlandmark sutures and sclerites that form the head (Fig. 3A). frons by the frontoclypeal suture in primitive insects. Laterally, the The vertex (Latin, vertex ϭ top; pl., vertices) is the apex or dor- clypeogenal suture demarcates the clypeus. Ventrally, the clypeus issal region of the head between the compound eyes for insects with separated from the labrum by the clypeolabral suture (Fig. 3A). Thea hypognathous or opisthognathous head. This definition does not clypeus is highly variable in size and shape. Among insects with suck-apply to prognathous heads because the primary axis of the head has ing mouthparts, the clypeus is large.rotated 90° to become parallel to the primary axis of the body. The The gena (Latin, cheek; pl., genae) forms the cheek or sclero-vertex is the area in which ocelli are usually located. In some insects tized area on each side of the head below the compound eye andthis region has become modified or assumes different names. extending to the gular suture (Fig. 4). The size of the gena varies The ecdysial suture (coronal suture ϩ frontal suture, epicranial considerably, and its boundaries also often are difficult to establish.suture, ecdysial line, cleavage line) is variably developed among In Odonata the gena is the area between compound eye, clypeus,insects. The suture is longitudinal on the vertex and separates and mouthparts. The postgena (Latin, post ϭ after; gena ϭ cheek;epicranial halves of the head (Fig. 3B). Depending on the insect, the pl., postgenae) is the portion of the head immediately posteriad ofecdysial suture may be shaped like a Y, a U, or a V. The arms of the the gena of pterygote insects and forms the lateral and ventral partsecdysial suture that diverge anteroventrally, called the frontal sutures of the occipital arch (sensu Snodgrass) (Fig. 4). The subgenual area(frontogenal sutures), are not present in all insects (Fig. 3B). Some is usually narrow, located above the gnathal appendages (mandi-of these complexes of sutures are used by insects to emerge from the ble and maxillae), and includes the hypostoma (Figs. 3 and 4) andold integument during molting. the pleurostoma. The pleurostoma is the sclerotized area between
  • 50. 14 Anatomy: Head, Thorax, Abdomen, and Genitalia the anterior attachment of the mandible and the ventral portion of Hymenoptera (Pteromalidae and Eurytomidae); the broad heads ofA the compound eye. The hypostoma is posteriad of the pleurostoma between the posterior attachment of the mandible and the occipital the males are featured in various aspects of courtship behaviors. foramen. The subgenal suture forms a lateral, submarginal groove Topographical Features of the Head or sulcus on the head, just above the bases of the gnathal append- ages (Fig. 4). The subgenal suture is continuous anteriorly with the Morphologists experience considerable difficulty in defining frontoclypeal suture in the generalized pterygote head. Internally, regions and determining homologies of structure on the insect head. the subgenal suture forms a subgenal ridge that presumably provides We cannot unambiguously characterize topographical features of structural support for the head above the mandible and maxillae. In the insect head because more than a million species are involved some instances, the subgenal suture is descriptively divided into two. in the definition, and they show incredible diversity in head anatomy. The part of the suture that borders the proximal attachment of the Shape alone is not adequate or suitable because there are many head mandible to the head (Fig. 4) is called the pleurostomal suture (the shapes, and often a head shape can be derived independently in ventral border of the pleurostoma). The posterior part of the subge- several unrelated lineages. Some head shapes are influenced by nal suture from the mandible to the occipital foramen is called the behavior. hypostomal suture (the ventral border of the hypostoma). AXIAL POSITION The posture or orientation of the head in its resting position relative to the long axis of the body can be impor- Occiput Vertex tant in providing definitions of the anatomical features of the head. Occipital suture Compound eye Axial position in insects typically falls into three basic categories: Lateral ocellus Postoccipital suture hypognathous, prognathous, and opisthognathous. Ocular suture In general zoological usage, the word “hypognathous” (Greek, Postocciput Cervix Gena hypo ϭ under; gnathos ϭ jaw) serves to designate animals whose Cervical sclerites Frons lower jaw is slightly longer than the upper jaw. In entomological Subocular suture Postgena Frontal suture usage, “hypognathous” refers to insects with the head vertically ori- Posterior tentorial pit Anterior tentorial pit ented and the mouth-directed ventrad. Most insects with a hypogna- Labium Clypeus thous condition display an occipital foramen near the center of the Maxilla Mandible posterior surface of the head. The hypognathous condition is con- Labrum sidered by most insect morphologists to represent the primitive or generalized condition. The hypognathous position is evident in most major groups of insects and can be seen in the grasshopper, house FIGURE 4 Generalized view of an insect head. fly, and honey bee. Other conditions are probably derived from ancestors with a hypognathous head. In general zoological usage “prognathous” (Greek, pro ϭ forward; Head Size and Shape gnathos ϭ jaw) refers to animals with prominent or projecting jaws. In entomological usage, the prognathous condition is character- The size and shape of the head and its appendages reflect func- ized by an occipital foramen near the vertexal margin with mandi- tional adaptations that can be used to explain biological details of the bles directed anteriad and positioned at the anterior margin of the insect—the realm of morphology as opposed to anatomy. head. When viewed in lateral aspect, the primary axis of the head SIZE Upon casual observation, the size of any given insect’s is horizontal. Some predaceous insects, such as carabid beetles and head appears to be in proportion to the size of its body. A head that earwigs, display the prognathous condition. In other insects, such as is disproportionately small or large relative to body size suggests cucujid beetles and bethylid wasps, the prognathous position may that some adaptation has taken place that serves a functional need. reveal a solution to problems associated with living in concealed situ- Proportional head size varies considerably in the Insecta. Some ations such as between bark and wood or similar confined habitats. fly families have very tiny heads in relation to their body size (e.g., In general zoological usage, “opisthognathous” (Greek, opisthos ϭ Diptera: Acroceridae). Among Orthoptera, grass-feeding species behind; gnathos ϭ jaw) refers to animals with retreating jaws. In typically have larger heads than herbaceous-feeding species. The entomological usage, the opisthognathous condition is characterized large head is filled with powerful adductor muscles because grasses by posteroventral position of the mouthparts resulting from a deflec- (monocots) are more difficult to chew than dicotyledonous plants. tion of the facial region. The opisthognathous condition is displayed Furthermore, the postseedling stages of grasses are nutrient poor, in many fluid-feeding Homoptera, including leafhoppers, whiteflies, meaning that more grass must be bitten, chopped, or ground to pro- and aphids. vide adequate nutrition. SUTURES OF THE HEAD Head sutures are sometimes SHAPE Head shape varies considerably among insects. Many used to delimit specific areas of the head, but there are problems. unusual shapes seem to be influenced by behavior and may be used Establishing homology of sutures between families and orders to illustrate examples of structural form and function. The functional is difficult. From a practical viewpoint, standards have not been importance of head shape may be difficult to determine in pre- developed for naming sutures among insect groups. Some names served specimens. A few hours of observation with live insects can are based on the areas delimited (e.g., frontoclypeal suture); other provide considerable insight into the importance of shape. Globular sutures are named for the areas in which the suture is found (e.g., heads are seen in some insects, including the burrowing crickets coronal suture). Sutures frequently have more than one name (e.g., (e.g., stenopelmatines and gryllids). This form of head is adapted frontoclypeal suture and epistomal suture are synonymous). for pushing soil. Hypercephalic heads are seen in the males of some The compound eye is an important landmark on the insect head. Diptera (Sepsidae, Diopsidae, Drosophilidae, and Tephritoidea) and An ocular suture surrounds the compound eye and forms an inflection
  • 51. Anatomy: Head, Thorax, Abdomen, and Genitalia 15or an internal ridge of the integument (Figs. 3 and 4). The ocular mandible. Internally, the occipital suture develops into a ridge, pro-suture is not present in all insects and is difficult to see in someinsects unless the head is chemically processed for microscopic viding strength for the head. The postoccipital suture is a landmark on the posterior surface Aexamination. When present, the ocular suture probably provides of the head and is typically near the occipital foramen (Fig. 5A andstrength and prevents deformation of the compound eye. 5B). The postoccipital suture forms a posterior submarginal groove A subocular suture extends from the lower margin of the com- of the head with posterior tentorial pits marking its lower ends onpound eye toward the subgenal suture. In some species the sub- either side of the head. Some morphologists regard this suture asocular suture (Fig. 4) may extend to the subgenal suture; in other an intersegmental boundary (labium) between the first and secondspecies it may terminate before reaching another landmark. This maxillae. Internally, the postoccipital suture forms the postoccipitalsuture is straight and commonly found in the Hymenoptera, where it ridge that serves as an attachment for the dorsal prothoracic and cer-may provide additional strength for the head. vical muscles of the head. The absence of the postoccipital suture in pterygote insects is a derived condition. POSTERIOR ASPECT OF THE HEAD The entire pos- The postocciput of pterygotes forms the extreme posterior, oftenterior surface of the head is termed the postcranium (Fig. 5). The U-shaped sclerite that forms the rim of the head behind the postoc-surface may be flat, concave, or convex, depending on the group of cipital suture. The postocciput is interpreted as a sclerotic remnantinsects. The occiput (Latin, back of head) of pterygote insects is the of the labial somite in ancestral insects.posterior portion of the head between the vertex and cervix (Latin, In pterygotes such as Orthoptera the occipital foramen and theneck). The occiput is rarely present as a distinct sclerite or clearly mouth are not separated. More highly evolved insects have developeddemarcated by “benchmark” sutures. When present, the occiput sig- sclerotized separations between the mouthparts and the occipitalnifies a primitive head segment. In some Diptera the occiput forms foramen. At least three types of closure have been identified (Fig. 5):the entire posterior surface of the head. In other insects it forms a the hypostomal bridge, the postgenal bridge, and the gula. An under-narrow, horseshoe-shaped sclerite. standing of these structures provides insight into the operation of the Vertex head and suggests evolutionary trends in feeding strategies. Occiput The hypostomal bridge is usually developed in adult heads display- Postoccipital suture ing a hypognathous axial orientation. The bridge is formed by medial Postgena extension and fusion of hypostomal lobes (hypostoma) (Fig. 5A). The Occipital foramen Posterior tentorial pit hypostomal bridge is the ground plan condition of closure for the pos- Hypostomal suture terior aspect of the head, but it is not restricted to primitive insects. Hypostomal bridge The hypostomal bridge is found in highly developed members of the Mandible Heteroptera, Diptera, and Hymenoptera. In Diptera the hypostomal Labium bridge also has been called the pseudogula. Maxilla The postgenal bridge is a derived condition from the hypos- (A) tomal ground plan and is developed in adults of higher Diptera and Vertex aculeate Hymenoptera. The bridge is characterized by medial exten- Postoccipital suture sion and fusion of the postgenae, following a union of the hypostoma Occipital foramen Posterior tentorial pit (Fig. 5B). The posterior tentorial pits retain their placement in the Postgenal bridge postoccipital suture. Postgena The gula (Latin, gullet; pl., gulae) is developed in some Coleoptera, Maxilla Neuroptera, and Isoptera. Typically, the gula is developed in heads Labium displaying a prognathous axial orientation and in which posterior ten- Mandible (B) torial pits are located anteriad of the occipital foramen (Fig. 5C). The median sclerite (the gula) on the ventral part of a prognathous head apparently forms de novo in the membranous neck region between Occipital foramen the lateral extensions of the postocciput. The gula is a derived condi- Posterior tentorial pit tion that is found in some but not all prognathous heads. Gula Postgena Labium Endoskeletal Head Framework Maxilla Although the hardened integument of the head forms a structur- Mandible ally rigid capsule, this design is insufficient to solve the problems associated with muscle attachment and maintaining structural integ- (C) rity during chewing. Thus, insects have evolved a tentorium (Latin, tent; pl., tentoria): a complex network of internal, hardened, cuticu-FIGURE 5 Occipital closures: (A) hypostomal bridge, (B) postge- lar struts that serve to reinforce the head. The tentorium forms asnal bridge, and (C) gula. an invagination of four apodemal arms from the integument in most pterygote insects. The tentorium strengthens the head for chewing, The occipital suture (hypostomal suture sensu MacGillivray) is provides attachment points for muscles, and also supports and pro-well developed in orthopteroids, but it is not present in many other tects the brain and foregut.groups of pterygote insects (Fig. 4). When present, the occipital Anatomically, the tentorium consists of anterior and posterior arms.suture forms an arched, horseshoe-shaped groove on the back of the In most insects, the anterior arms arise from facial inflections locatedhead that ends ventrally, anterior to the posterior articulation of each just above the anterior articulations of the mandibles. Externally,
  • 52. 16 Anatomy: Head, Thorax, Abdomen, and Genitalia the arms are marked by anterior tentorial pits positioned on the The thorax of modern insects consists of three segments termedA frontoclypeal or subgenal (pleurostomal) suture (Fig. 4). Internally, the anterior region may form a frontal plate. Posterior arms originate the prothorax, mesothorax, and metathorax. The last two collectively are called the pterothorax (Greek, ptero ϭ wing or feather) because at the ventral ends of the postoccipital inflection. They are marked extant insects bear wings on these segments only. The individual dor- externally by posterior tentorial pits (Fig. 4). The posterior arms usu- sal sclerites or terga of the thoracic segments are also known as nota ally unite to form a transverse bridge or corpus tentorii (internally) (Greek, notos ϭ back; sing, notum). The nota of Apterygota and many across the back of the head. Dorsal arms (rami), found in many immature insects are similar to the terga of the abdomen with typical insects, arise from the anterior arms. They attach to the inner wall of secondary segmentation. The nota of each thoracic segment are seri- the head near antennal sockets. The dorsal arms are apparently not an ally distinguished as the pronotum, mesonotum, and metanotum. invagination of cuticle, because pits do not mark them externally. The size and shape of the prothorax are highly variable. The prothorax may be a large plate as in Orthoptera, Hemiptera, and Mandible Articulation and Musculature Coleoptera, or reduced in size forming a narrow band between the head and mesothorax as in Hymenoptera. The prothorax is usually The hypothetical ancestor of insects is thought to possess a man- separated or free from the mesothorax. The sclerites are separated dible with one point of articulation. Later, insects acquired a second by a membrane that may be large and conspicuous in more primi- point of articulation. The basis of this assumption comes from a sur- tive holometabolous insects such as Neuroptera and Coleoptera, or vey of the Hexapoda in that the modern Apterygota have a mono- reduced in size in more highly evolved holometabolous insects such condylic mandible and the Pterygota have a dicondylic mandible. as Diptera and Hymenoptera. The term condyle (Greek, kondylos ϭ knuckle) refers specifically The pterothorax includes the thoracic segments immediately pos- to a knoblike process. For the mandible, the condyle is the point teriad of the prothorax. In winged insects the relationship between of articulation with the head. On the head itself is an acetabulum thoracic segments involved in flight can be complicated. In contrast, (Latin, acetabulum ϭ vinegar cup), a concave surface or cavity for the thorax of larval insects and most wingless insects is relatively sim- the reception and articulation of the condyle. ple. The mesothorax and metathorax of these insects are separated The dicondylic mandible is the derived condition and is found by membrane. Adult winged insects show a mesothorax and metath- in the Lepismatidae and Pterygota. The dicondylic mandible has orax that are consolidated (i.e., more or less united) to form a func- secondarily acquired an articulation point anterior to the first point tional unit modified for flight. in the monocondylic mandible. These attachments form a plane The development of the pterothoracic segments varies among of attachment. In the monocondylic mandible there is no plane of winged insects. When both pairs of wings participate equally in attachment, and the mandibles move forward or rearward when the flight, the two thoracic segments are about the same size. This con- muscles contract. The two points of articulation create a plane of dition is seen in Odonata, some Lepidoptera, and some Neuroptera. movement that restricts the direction of mandible movement. When one pair of wings is dominant in flight, the corresponding thoracic segment is commensurately larger and modified for flight, THORAX whereas the other thoracic segment is reduced in size. This condi- The thorax represents the second tagma of the insect body. The tion is seen in Diptera and Hymenoptera, where the forewing is thorax evolved early in the phylogenetic history of insects. In most large and dominant in flight. The reverse condition is seen in the Paleozoic insects the thorax is well developed and differentiated Coleoptera, where the hind wing is large and dominant in flight. from the head and abdomen, and the three distinct tagmata prob- In more closely related insect groups, such as families within ably developed during the Devonian. an order, that are primitively wingless or in which wings have been In terms of insect phylogeny, the thorax of Apterygota is strikingly secondarily lost in modern or extant species, many modifications to different in shape compared with the head or abdomen. Of modern the thorax occur. Many wingless forms can be attributed to environ- apterygotes only the Collembola display taxa in which thoracic tag- mental factors that promote or maintain flightlessness. For instance, matization and segmentation are not obvious. island-dwelling insects are commonly short winged (brachypterous), Apparently, the primary, functional role of the thorax has always or wingless, whereas their continental relatives are winged, presum- been locomotion, since the primary modifications of the thorax have ably because for island species, flight increases the likelihood of been for locomotion (first walking, and then flight). Modification for being carried aloft, moved out to sea, and subsequently lost to the locomotion probably developed before other morphological adap- reproductive effort of the population. The anatomical consequences tations, such as metamorphosis. Diverse independent and interde- of flightlessness can be predictable; in the Hymenoptera, short wings pendent mechanisms for locomotion have evolved throughout the bring a disproportionate enlargement of the pronotum and reduction Insecta, including walking, flight, and jumping. Active participation in size of the mesonotum and metanotum. in flight by insects is unique among invertebrates. Sutures and Sclerites of Wing-Bearing Segments Anatomy of the Thorax The wing-bearing segments of the thorax are subdivided into The cervix is the connection between the head (occipital foramen) a myriad of sclerites that are bounded by sutures and membra- and the anteriormost part of the thorax (pronotum) (Fig. 2). nous areas. These sutures and sclerites are the product of repeated Typically, the area between the head and pronotum is membranous. modification of the thorax in response to various demands placed The ground plan for the insect cervix contains two cervical sclerites on the insect body by the environment. Similar modifications have on either side of the head that articulate with an occipital condyle of occurred independently in many groups of insects; some modifica- the head and the prothoracic episternum. Musculature attached to tions are unique. Generalizations are difficult to make, given the these sclerites increases or decreases the angle between the sclerites, large number of sutures and sclerites, coupled with the number of and creates limited mobility of the head. insects that there are to consider.
  • 53. Anatomy: Head, Thorax, Abdomen, and Genitalia 17 Dorsal Aspect form the part of the wing closest to the body and are not treated in The nota of the pterothorax are further subdivided into the pres- this article. The prealar bridge is a heavily sclerotized and rigid supporting Acutum, scutum, and scutellum; again, serially distinguished as mes-oscutum and mesoscutellum, and metascutum and metascutellum sclerite between the unsclerotized membrane of the pterothorax and(Fig. 6). Additionally, there are sclerites anterior and posterior to the the pleuron; it supports the notum above the thoracic pleura. Thenotum, as discussed shortly. prealar bridge is composed of cuticular extensions from the anterior part of the prescutum and antecosta. The anterior notal wing process is the anterior lobe of the lateral margin of the alinotum supporting Scutellum Scutum the first axillary sclerite (Fig. 6). The posterior notal wing process is Posterior wing Prescutum process a posterior lobe of the lateral margin of the alinotum that supports Prescutal suture Antecostal sulcus the third axillary sclerite of the wing base (Fig. 6). Anterior wing Postnotum process Wing stub Pleural wing process Basalare Lateral Aspect Phragma Episternum The pleuron (Greek ϭ side; pl., pleura) is a general term associ- Subalare Trochantin ated with the lateral aspect of the thorax. Adults, nymphs, and active Pleural sulcus Epimeron larvae all display extensive sclerotization of the pleural area. Sclerites Precoxal bridge Coxal opening forming this part of the body wall are derived from the precoxa, sub- Prosternum Postcoxal bridge coxa, or supracoxal arch of the subcoxa. Spinasternum Sternellum Basisternum PLEURAL REGIONS OF THE THORAX Apterygota and Immature Plecoptera The anapleurite isFIGURE 6 Diagram of the pterygote pterothorax. the sclerotized area above the coxa (supracoxal area) (Fig. 7). The coxopleurite is a sclerotized plate situated between the coxa and the The prescutum is the anterior portion of the scutum, laterally anapleurite (Fig. 7). It bears the dorsal coxal articulation, the ante-bearing prealar bridges separated by the prescutal suture from the rior part of which becomes the definitive trochantin. The sternop-mesoscutum. The scutum is the largest dorsal sclerite of the notum leurite, or coxosternite, is the definitive sternal sclerite that includesand is bounded posteriorly by the scutoscutellar suture, which the areas of the limb bases and is situated beneath the coxa (Fig. 7).divides the notum into the scutum and scutellum. The scutellum isgenerally smaller than the scutum. In Heteroptera it is a small trian-gular sclerite between the bases of the hemelytra. In Coleoptera the Notumscutellum is the small triangular sclerite between the bases of the Intersegmentalelytra. In Diptera and Hymenoptera the scutellum is relatively large, lineforming a subhemispherical sclerite, sometimes projecting posteriad. SpiracleThe posteriormost sclerite of the notum is the postnotum, separated Anapleurite Coxal articulationfrom the notum by secondary segmentation. In some insects there is Coxopleurite Coxal openinga postscutellum (metanotal acrotergite) that forms the posteriormostthoracic sclerite of the metanotum, or the posteriormost sclerite Sternopleurite Coxal articulationof the thorax. In Diptera the postscutellum appears as a transversebulge below the scutellum. FIGURE 7 Pleural aspect of apterygote thorax. The acrotergite and postnotum deserve further explanation.Again, the anteriormost sclerite is an acrotergite, the anterior pre-costal part of the notal plate. The postnotum is an intersegmentalsclerite associated with the notum of the preceding segment. The Pterygota The basalare is a sclerite near the base of the wingpostnotum bears the antecosta, a marginal ridge on the inner surface and anterior to the pleural wing process (Fig. 8). The basalare servesof the notal sclerite corresponding to the primary intersegmental as a place of insertion for the anterior pleural muscle of the wing.fold. The postnotum also usually bears a pair of internal project- The subalare is posterior to the basalare and the pleural wing processing phragmata. The antecostal suture divides the acrotergite from (Fig. 8). It too serves as a place for insertion of the wing’s posteriorthe antecosta, the internal ridge marking the original intersegmen- pleural muscle. The tegula is the anteriormost independent scle-tal boundary. Thus, when the antecosta and acrotergite are devel- rite associated with the wing base. The tegula is typically scalelike,oped into larger plates and are associated with the notum anterior articulates with the humeral sclerite, and protects the wing base fromto them, they are referred to as a postnotum. The final structure physical damage. The tegula is absent from Coleoptera and from theassociated with the dorsal aspect of the pterothorax is the alinotum metathorax of most orders. The pleural wing process is located at the(Greek, ala ϭ wing; notos ϭ back; pl., alinota). The alinotum is the dorsal end of the pleural ridge and serves as a fulcrum for the move-wing-bearing sclerite of the pterothorax. ment of the wing (Fig. 8). The parapteron is a small sclerite, articu- lated on the dorsal extremity of the episternum just below the wings (Fig. 6). Wing Articulation The pleural suture is an easily visible landmark on the pterotho- The thoracic components necessary for wing movement include racic pleura (Fig. 8). It extends from the base of the wing to the basethe prealar bridge, anterior notal wing process, and posterior notal of the coxa. The pleural ridge is formed internally by the pleuralwing process. The components of the wing itself that articulate with suture and braces the pleuron above the leg. The episternum is athe thoracic components are the humeral and axillary sclerites; they pleural sclerite anterior to the pleural suture and sometimes adjacent
  • 54. 18 Anatomy: Head, Thorax, Abdomen, and Genitalia Basalare Paired furcal pits are found in the laterosternal sulcus (Fig. 9). AA Pleural process Subalare transverse sternacostal sulcus bisects the ventral plate and thereby forms an anterior basisternite and posterior furcasternite (Fig. 9). Katepisternum Pleural suture Mesepistenum Spiracle The basisternite (basisternum) is the primary sclerite of the sternum Mesepimeron Anapleurite Anepisternum Coxopleurite (Fig. 9). It is positioned anterior to the sternal apophyses or sterna- costal suture and laterally connected with the pleural region of the Precoxal bridge Coxal opening Trochantin Postcoxal bridge precoxal bridge. The furcasternite (furcasternum) is a distinct part Coxosternite of the sternum in some insects bearing the furca (Fig. 9). The spin- asternum is a “spine-bearing” intersegmental sclerite of the thoracic venter, associated or united with the preceding sternum. The spin- FIGURE 8 Lateral aspect of the pterygote thorax (Orthoptera: asternum may become part of the definitive prosternum or mesos- Acrididae). ternum, but not of the metasternum. The sternellum is the second sclerite of the ventral part of each thoracic segment, frequently to the coxa (Fig. 8); the episternum is typically the largest lateral tho- divided into longitudinal parts that may be widely separated (Figs. racic sclerite between the sternum and the notum. The epimeron is 6 and 9). the posterior division of a thoracic pleuron adjacent to the coxa and posterior to the pleural suture (Fig. 8); it is typically smaller than the episternum and narrow or triangular. The episternum and the ABDOMEN epimeron of many insects have become subdivided into several sec- The abdomen is more conspicuously segmented than either the ondary sclerites bounded by sutures. The simplest condition shows head or the thorax. Superficially, the abdomen is the least special- the episternum divided into a dorsal anepisternum and a ventral ized of the body tagma, but there are notable exceptions such as katepisternum (Fig. 8). Similarly, the epimeron is divided into an the scale insects. The abdomen characteristically lacks appendages anepimeron and katepimeron. The trochantin is a small sclerite at except cerci, reproductive organs, and pregenital appendages in the base of the insect leg of some insects (Figs. 6 and 8). Some work- adult Apterygota and larval Pterygota. ers theorize that the trochantin may have developed into the pleural wall. The trochantin is often fused to the episternum or absent. Ground Plan of the Abdomen The precoxal bridge is anterior to the trochantin, usually continu- ous with the episternum, frequently united with the basisternum, The ground plan abdomen of an adult insect typically consists but also occurs as a distinct sclerite (Fig. 8). The postcoxal bridge of 11–12 segments and is less strongly sclerotized than the head or is the postcoxal part of the pleuron, often united with the sternum thorax (Fig. 10). Each segment of the abdomen is represented by a behind the coxa (Fig. 8). The sclerite extends behind the coxa and sclerotized tergum, sternum, and perhaps a pleurite. Terga are sepa- connects the epimeron with the furcasternum. The meron is a lat- rated from each other and from the adjacent sterna or pleura by a eral, postarticular basal area of the coxa and is sometimes found membrane. Spiracles are located in the pleural area. Modification disassociated from the coxa and incorporated into the pleuron. The of this ground plan includes the fusion of terga or terga and sterna meron is typically large and conspicuous in panorpid and neurop- to form continuous dorsal or ventral shields or a conical tube. Some teran insects. In Diptera the meron forms a separate sclerite in the insects bear a sclerite in the pleural area called a laterotergite. thoracic pleuron. Ventral sclerites are sometimes called laterosternites. The spiracles are often situated in the definitive tergum, sternum, laterotergite, or laterosternite. Ventral Aspect The ground plan of the sternum (Greek, sternon ϭ chest; pl., Tergite 10 sterna) consists of four sclerites, including an intersternite (spinaster- Epiproct nite), two laterosternites (coxosternites), and a mediosternite (Fig. 9). Tergite 1 The mediosternite and the laterosternite meet and join, and the line of Cercus Spiracle Paraproct union is called the laterosternal sulcus (pleurosternal suture) (Fig. 9). Pleural Valvula 3 membrane Valvula 2 Intersternite Sternite 1 (internal) Presternal suture Valvula 1 Laterosternite Basisternum Valvifer 1 Sternite 8 Valvifer 2 Sternalcostal sulcus Mediosternite Laterosternite FIGURE 10 Abdominal segmentation. (Basisternum Sternellum ϩSternellum) Furcasternite During the embryonic stage of many insects and the postembry- Laterosternal sulcus Laterosternal onic stage of primitive insects, 11 abdominal segments are present. sulcus Basisternite In modern insects there is a tendency toward reduction in the Furcal pits Sternacostal sulcus Furcasternite number of the abdominal segments, but the primitive number of Sternellum 11 is maintained during embryogenesis. Variation in abdominal seg- ment number is considerable. If the Apterygota are considered to be indicative of the ground plan for pterygotes, confusion reigns: adult Protura have 12 segments, Collembola have 6. The orthopteran fam- ily Acrididae has 11 segments, and a fossil specimen of Zoraptera has FIGURE 9 Ventral aspect of the thorax (Orthoptera: Acrididae). a 10-segmented abdomen.
  • 55. Anatomy: Head, Thorax, Abdomen, and Genitalia 19 Anamorphosis is present among some primitive ancestral hexa- proktos ϭ anus) (Fig. 10). A longitudinal, medial, membranous areapods such as the Protura—they emerge from the egg with eightabdominal segments and a terminal telson. Subsequently, three seg- connects the paraprocts ventrally. Primitive groups of extant insects such as Thysanura and Ephemeroptera, and some fossil groups such Aments are added between the telson and the last abdominal segment as Paleodictyoptera, display a conspicuous, long, median filamentwith each molt. In contrast, most insects undergo epimorphosis that apparently projects from the apex of the epiproct. This is calledin which the definitive number of segments is present at eclosion. the appendix dorsalis or caudal style. The appendage appears annu-Given the extent of variation in abdominal segmentation, morpholo- lated and similar in shape to the lateral cerci, but the function ofgists conventionally discuss the abdomen in terms of pregenital, gen- the appendix is unknown. The twelfth abdominal segment is calledital, and postgenital segmentation. the periproct in Crustacea, and it forms a telson in some embryonic insects. The periproct appears in adult Protura and naiadal Odonata. Abdominal Anatomy Typically, the abdominal terga show secondary segmentation with Abdominal Appendagesthe posterior part of a segment overlapping the anterior part of the Presumably, the hypothetical ancestor of the Insecta was a myr-segment behind it (Fig. 10). Such overlap prevents damage or injury iapod with one pair of appendages for each body segment. Amongto the animal while it moves through the environment, particularly contemporary insects the head appendages are represented by thein confined spaces. antennae, mandibles, and the first and second maxillae. Thorax The pregenital segments in male insects are numbered 1 through appendages are represented by legs, whereas the wings are consid-8; the pregenital segments in female insects are numbered 1 through 7 ered to be secondary in origin. In most Apterygota, paired abdomi-(Fig. 10). Among the Apterygota, male genitalia in Collembola are posi- nal appendages are apparent. In most true insects embryologicaltioned between segments 5 and 6 and in Protura between segments 11 appendages are formed and lost before eclosion. The appendagesand the paraproct. Genital segments of Pterygota include segment 9 in found in embryos apparently represent ancestral conditions that aremales and segments 8 and 9 in females. Postgenital segments of ptery- not expressed in postembryonic stages of modern insects. In moderngote insects are 10 and 11 in females and 9 and 10 in males. insects, most pairs of appendages have been lost, and the irregular In general there is little modification of the pregenital sclerites. distribution of the remaining appendages makes a summary evalua-A notable exception is found in the Odonata. Male Odonata do not tion difficult. Abdominal appendages do not resemble the structurehave an intromittent organ on segment 9. Instead, the male moves of thoracic legs of any insect.the abdominal apex forward and deposits sperm in a reservoir along Appendages are common among some entognathous hexapods,the anterior margin of the third abdominal sternum. Other modifi- and some ancestral forms display unique abdominal appendages.cations of the pregenital sclerites are not related to sexual behavior. Collembola are highly specialized entognathous Hexapoda. TheSome of these modifications are glandular. abdomen of Collembola bear saltatorial appendages, which gives the Modification of the genital sclerites from the ground plan is group its common name of springtail, and a ventral tube, the collo-frequently observed among insects. Adult Pterygota are character- phore, which is the basis of the ordinal name.ized by a well-developed reproductive system, including organs The collophore (Greek, kolla ϭ glue; pherein ϭ to bear) is foundof copulation and oviposition. This duality of function has resulted on the first abdominal segment of Collembola. The collophore formsin considerable differentiation of associated segments and contrib- a ventromedial tube that is eversible with hydrostatic pressure anduted to difference of opinion regarding homology of genitalic parts. is drawn inward with retractor muscles. Some morphologists believeAmong pterygote insects the male genitalia are generally positioned the collophore represents the fusion of paired, lateral appendages ofon segment 9. The ninth sternum is called a hypandrium (Greek, an ancestor. An early explanation of the collophore function noted ithypo ϭ beneath; aner ϭ male; Latin, -ium ϭ diminutive) in many was an organ of adhesion. The collophore also is used as a groominginsects, including Psocoptera. In Ephemeroptera, the tenth sternum organ in some Collembola. The collophore is connected to secretoryis called a hypandrium. Fusion of segments 9 and 10 in Psocoptera glands in the head, and the median longitudinal channel on the ven-results in a structure called the clunium (Latin, clunais ϭ buttock). ter of the thorax extends from the head to the base of the collophore. The gonopore (Greek, gone ϭ seed; poros ϭ channel) of the OTHER APPENDAGES Protura maintain short, cylindricalfemale reproductive system serves as the aperture through which appendages on each of the first three abdominal segments. Eachthe egg passes during oviposition. The gonopore usually is located of these arises from membranous areas between the posterolateralon segment 8 or 9. Enlargement of sternum 8 in some female insects angles of the terga and sterna. The position suggests a pleural origin.is called a subgenital plate. Modification of postgenital sclerites is frequently observed and APPENDAGES OF PTERYGOTA The aquatic neuropteranseems to be a functional response to adaptations associated with larva Sialis has long, tapering, six-segmented appendages on each ofcopulation and oviposition. Some modifications include fusion of the the first seven body segments. These appendages articulate to pleu-tergum, pleuron, and sternum to form a continuous sclerotized ring. ral coxopodites. Similar appendages are found on the abdomen ofThe phenomenon is notable in apterygota and pterygote insects. some aquatic coleopteran larvae. The eleventh abdominal segment forms the last true somite of the The tenth abdominal segment is present in most larval andinsect body. Frequently, this segment is found in embryonic stages adult Holometabola. As noted earlier, it is sometimes fused withof primitive insects even when it cannot be observed in postemer- segment 11. Segment 10 displays paired appendicular processesgent stages. When the eleventh segment is present, it forms a coni- called pygopodia in Trichoptera, Coleoptera, and Lepidoptera.cal endpiece that bears an anus at the apex, flanked laterally by cerci Pygopods form terminal eversible appendages in some beetle larvae.(Greek, kerkos ϭ tail) (Fig. 10). The dorsal surface of the eleventh Pygopodia are bilaterally symmetrical, with eight podia, or feet, persegment is called an epiproct (Greek, epi ϭ upon; proktos ϭ anus); side. Control of the podia is apparent because they are not alwaysthe ventrolateral surface is called a paraproct (Greek, para ϭ beside; everted or inverted. Podia are withdrawn into the segment and have
  • 56. 20 Anatomy: Head, Thorax, Abdomen, and Genitalia a common or median stalk. Each podium has several rows of equally ovipositor (Fig. 11). The ovipositor is a structure that develops fromA spaced acanthae that apparently serve as holdfasts. Functionally, the acanthae enable the larvae to attach to and move on different sub- modified abdominal appendages or segments. It functions in the pre- cise placement of eggs. It is commonly assumed that insects that do strates. When the larva walks on a flat substrate, the pygopodia are not show an ovipositor have ancestors that had an ovipositor. Thus, retracted into the body. When the larva walks on the edge of a leaf, the structure has been lost during the course of evolutionary adap- the pygopodia are everted and used as holdfasts. tation to a particular lifestyle. Female insects with a genitalic open- The larval prolegs of terrestrial Lepidoptera and Symphyta are ing on the posterior margin of the ninth abdominal segment typically not well developed, but they are adapted to grasping substrates. display a rudimentary or suppressed appendicular ovipositor. These These structures are considered to be serially homologous with legs, insects lack special provisions for egg placement, but sometimes but they are also referred to by some as adaptive structures with no they reveal other abdominal modifications intended to facilitate relation to legs. oviposition. The adult pterygote abdomen has appendages that are not gener- ally observed. These appendages are grouped for discussion based on the segments of the abdomen on which they are found. Epiproct Pregenital appendages are rare among insects. Adult white- flies have a curious structure on sternum 8 that propels honeydew Cercus away from the body. Genitalia are segmental appendages and are treated in the next section. Postgenital appendages include cerci Paraproct (Latin, circle), which are thought to represent primitive append- ages because they are found in the Apterygota (except Protura) 3rd Valvula (ovipositor) and many Pterygota. Cerci originate on abdominal segment 11 in a membranous area between the epiproct and the paraproct (Fig. 10). In insects that have lost segment 11, the cerci appear to originate on segment 10. Cerci occur in all orders among the Hemimetabola except for hemipteroids; among the Holometabola, they are found FIGURE 11 Appendicular ovipositor (Orthoptera: Tettigoniidae). only in the Mecoptera and Symphyta. Cerci are highly variable in size and shape and function. They are longer than the body in Thysanura, and in some Orthoptera cerci may be indistinct. Cerci resemble forceps in Japygidae and are annu- Female Genitalia lated in Dictyoptera. In Dictyoptera they detect air currents, are sen- Morphologists often use the Thysanura as a starting point for sitive to sound, and may be chemoreceptive. Some Ephemeroptera developing a generalized model to explain the evolution of the exter- use cerci to propel themselves through water. Japygidae and nal reproductive system of pterygote insects. The thysanuran abdo- Dermaptera probably use cerci to subdue prey. In some groups such men has basal sclerotized plates called coxopodites on which styli are as Embioptera and Orthoptera, cerci are sexually dimorphic and may attached. These plates are serially homologous along the abdomen, serve a role in copulation. and the pregenital plates are regarded as identical with the genital There are some features on the insect body that appear as append- plates. The plates located on segments 8 and 9 are considered to be ages but are not. Urogomphi (Greek, oura ϭ tail; gomphos ϭ nail; genital plates. The styli associated with these segments are called sing., urogomphus) are fixed or mobile cuticular processes on the gonapophyses. There are four gonapophyses on segments 8 and 9 apical abdominal segment of some coleopteran larvae. They may or (i.e., a pair of styli on each segment). The gonapophyses are medially may not be homologous with cerci, or other true appendages. concave and directed rearward. The basal sclerite is called a gono- coxa, and in some Thysanura it may be fused with the style. The primitive pterygote with a gonopore on segment 8 has an GENITALIA appendicular ovipositor that consists of three components. A basal The examination of the reproductive anatomy of different insect apparatus corresponds to the basal plate or primitive gonocoxite orders helps to develop an appreciation for the evolutionary trends of the thysanuran abdominal appendage. The second part is the in the formation of the external genitalia. The male genitalia are first valvifers (on the eighth sternum), and second valvifers (on the derived from the ninth abdominal segment. The female genitalia ninth sternum) are responsible for providing support and points are derived from the eighth and ninth abdominal segments. In the of articulation for the tube through which the egg passes (Fig. 12). female, the aperture through which the egg passes is called a gonop- Interpolated between the first and second valvifers is a small scle- ore. The gonopore serves as a boundary between the external and rite called a gonangulum, which articulates with the second gono- internal genitalia and is usually independent of the anus. Exceptions coxite and tergum 9. The gonangulum is present in Odonata and include some flies, such as the Tephritidae, where a common lumen Grylloblatoidea. It apparently is fused with the first valvifer in termed a cloaca serves for excretion, copulation, and oviposition. Dictyoptera and Orthoptera. In the remaining orders these struc- There is usually a single, medially located gonopore. The Der- tures are highly variable. maptera and Ephemeroptera are ancient groups of hemimetabolous The shaft of the ovipositor consists of two pairs of elongate, insects. Both orders display a condition in which the lateral oviducts closely appressed sclerites called the first and second valvulae (Fig. do not combine to form a median oviduct. Instead, the lateral oviducts 12). The first pair of valvulae is positioned on the eighth abdominal independently connect with paired gonopores on the conjuctival mem- sternum. The second pair of valvulae is located on the ninth abdomi- brane along the posterior margin of the seventh abdominal segment. nal sternum and is dorsal in position. Third valvulae are positioned Many female insects with a genitalic opening on the posterior on the posterior end of the second valvifers. These valvulae usually margin of the eighth abdominal segment display an appendicular serve as a sheath for the shaft of the ovipositor (Figs. 11 and 12).
  • 57. Antennae 21 Epiproct Cercus Apodeme A Sternite 9 Paraproct Spiracle Ejaculatory duct Valvifer 2 Valvula 3 Phallobase Valvifer 1 Valvula 2 Gonocoxite Valvula 1 Sternite 8 Gonopore Gonopore Phallomere opening (concealed) PhallothecaFIGURE 12 Female genitalia (diagrammatic), based on orthop- Endophallusteran female. Ectophallus Gonostyle Male Genitalia The primary function of the male genitalia in insects is insemina- Aedeagustion of the female. Methods of achieving insemination that involvespecial functions of the external genitalia include clasping and hold- Phallotremeing the female, retaining the connection with the female gonopore,the construction of spermatophores, and the deposition of spermato- FIGURE 13 Male genitalia (diagrammatic).phores or semen into the female genital tract; in some insects theinjection of semen takes place directly into the female body (trau- Further Readingmatic insemination of some Hemiptera). Other functions of the malegenitalia include excretion and various sensory functions. Chapman, R. F. (1982). “The Insects. Structure and Function.” 3rd Ed. The genitalia of male insects exhibit such an enormous variety of Hodder & Stoughton, London, U.K. DuPorte, E. M. (1957). The comparative morphology of the insect head.shapes and constituent parts, often further complicated by structural Annu. Rev. Entomol. 2, 55–77.rotation or inversion of all or some of the parts, that determination of a Gordh, G., and Headrick, D. H. (2001). “A Dictionary of Entomology.” CABground plan is virtually impossible. Examination of ancient orders shows International, Wallingford, Oxon, U.K.highly variable and specialized conditions. In general, the coxites of the Hinton, H. E. (1981). The Biology of Insect Eggs 3 Vols. Pergamon Press,eighth segment in most apterygotes are reduced and without gonapo- Oxford, U.K.physes, and they are absent altogether in the Pterygota. Thus, the male Matsuda, R. (1969). “Morphology and Evolution of the Insect Abdomen.external genitalia are derived from the ninth abdominal coxites. With Special Reference to Developmental Patterns and Their Bearings Again, the Thysanura have genitalia that closely resemble that of upon Systematics.” Pergamon Press, Oxford, U.K.the pterygote orders: a median intromittent organ or phallus, and Snodgrass, R. E. (1935). “Principles of Insect Morphology.” McGraw-Hill,paired lateral accessories (the periphallus of Snodgrass). The phal- New York and London. Tuxen, S. L. (1970). “Taxonomist’s Glossary of Genitalia in Insects.” 2nd Ed.lus is a conical, tubular structure of variable complexity (Fig. 13). Munksgaard, Copenhagen.Primitive insects may not display differentiated parts, and the entirestructure may be long, sclerotized, and tapering apicad. In a groundplan condition for pterygote insects, there is a sclerotized basal por-tion termed the phallobase and a distal sclerotized portion calledthe aedeagus (Fig. 13). The phallobase in insects is characterized byhighly variable development: sometimes sclerotized and supporting Anopheles Mosquito see Mosquitoesthe aedeagus, sometimes forming a sheath for the aedeagus. Thephallobase often contains an apodeme, which may provide supportor a point for muscle attachment. The phallobase and aedeagus arejoined by a membranous phallotheca (Fig. 13). The external wallsof the phallobase and aedeagus are called the ectophallus (Fig. 13). AnopluraThe gonopore is positioned at the apex of the ejaculatory duct and is see Phthirapteraconcealed within the phallobase. The gonopore is connected to theapex of the aedeagus via a membranous tube called the endophallus(Fig. 13). In some insects the endophallus may be everted throughthe aedeagus. The circular aperture at the apex of the aedeagus iscalled the phallotreme (Fig. 13). In some insects the endophal- Antennaelus and the gonopore may be everted through the phallotreme andinto the female’s bursa copulatrix. Genital lobes referred to as phal- Catherine Loudonlomeres form at the sides of the gonopore in the ontogeny of some University of California, Irvineinsects. Usually the phallomeres unite to form the phallus. A ntennae are segmented appendages that function primarily inSee Also the Following Articles chemoreception and mechanoreception. An insect has a sin-Body Size ■ Integument ■ Muscle System ■ Segmentation gle pair of antennae located on its head. Antennae in juvenile
  • 58. 22 Antennae insects are often very different in morphology from antennae in adult segment (most proximal) of the antenna, and it is attached to the headA insects, typically being larger or more elaborate in the adult stage. Adult antennae may be sexually dimorphic, appearing very different by a rim of flexible, intersegmental cuticle. Thus, the scape (and the rest of the antenna) can move with respect to the head. All the anten- in males and females. Antennae are absent in the wingless hexapods nal segments (and subsegments) are similarly joined to each other by belonging to the order Protura and may be extremely reduced in size thin, flexible cuticle. in some holometabolous larvae. The movements of an antenna are controlled in part by one or two pairs of muscles that attach inside the head (such as on the tentorium) STRUCTURE with the other end attached inside the scape. An additional pair of muscles runs from the scape to the next segment of the antenna, the The overall shape of most insect antennae is elongate and cylin- pedicel. The combined action of these two sets of muscles is capable drical (Fig. 1, top), although elaborations into plumose, lamellate, or of moving an antenna in almost any direction. The final (most distal) pectinate forms have arisen many times in different insect lineages segment of the antenna, the flagellum, is the most variable in morphol- (Fig. 1, bottom). An elongate, cylindrical morphology, probably the ogy among insects. The only hexapods that have intrinsic muscles in ancestral condition for insect antennae, is found in fossil insects and the flagellum (joining adjacent segments) are members of the wingless many other arthropods. There are three parts to an insect antenna: orders Collembola and Diplura (Fig. 2). In all true insects, there are the scape, the pedicel, and the flagellum (Fig. 2). The scape is the first no muscles in the flagellum. Many specialists prefer “annulus” or “sub- segment” to “segment” for an individual part of a flagellum in insects, because “segment” is reserved for parts with their own musculature. Movements of an annulated flagellum without intrinsic musculature may still occur, such as the spreading and closing of the lamellae or lateral extensions in an antenna (Fig. 1, bottom), but these movements are driven by changes in the pressure of the hemolymph (blood) inside the antenna and thus are hydraulic rather than muscular. In most insects, circulation of hemolymph through an antenna is facilitated by muscular pumping by an accessory heart located in the head near the base of the antenna. This antennal heart pumps the hemolymph into a blood vessel that discharges the hemolymph at the distal end of the antenna. The return flow of the hemolymph back to the head (and the general open circulatory system of the insect) is not inside a blood vessel. The lumen of an antenna also contains tracheae and nerves, which branch into any lateral exten- FIGURE 1 Insect antennae exhibit a variety of shapes including sions of the flagellum. Sensory neurons that respond to chemical or elongate morphologies (top) and those with lateral elaborations (bot- physical stimuli terminate in the deutocerebrum of the brain. The tom). [After Romoser, W. S., and Stoffolano, J. G., Jr. (1998). “The deutocerebrum is also the site of origin for the motor neurons that Science of Entomology,” WCB/McGraw-Hill, Boston, and Loudon, stimulate the muscles associated with the antennae. C., et al. (1994). J. Exp. Biol.193, 233–254, published by McGraw- Hill, with kind permission of the McGraw-Hill Companies.] GROWTH AND DEVELOPMENT Antennal growth and development in holometabolous insects (those that undergo complete metamorphosis) differs greatly from that in other insects. In holometabolous insects, adult antennae form from imaginal disks, which are clumps of undifferentiated cells that will develop into adult structures. The antennal imaginal disks may appear in the embryonic (fly) or late larval (moth) stage of the immature insect. Properties of the antennal imaginal disks determine to a large extent the chemical stimuli to which an adult will respond, as is seen from experiments in which antennal imaginal disks were cross-transplanted between larvae, which were then reared to adulthood and assayed. In hemimetabolous and apterygote (wingless) insects, the nymphs are very similar in overall form and habit to the adults, and their anten- nae resemble smaller, shorter versions of the adult antennae. As with all external structures that are replaced at each molt, a new antenna is formed inside the old antenna. The primary morphological change that occurs at each molt is that the flagellum lengthens with the addition of more segments or annuli, either at the distal end (orders Collembola FIGURE 2 Muscles in the antennae of springtails (Collembola) and Diplura), the proximal end (most insects), or along the length of (white; indicated by arrows) extend farther along the antennae than the flagellum (some members of the orders Orthoptera and Odonata). the muscles in the antennae of insects (to the proximal end of the Antennae are serially homologous to mouthparts and legs, reflect- terminal flagellomere vs. the proximal end of the pedicel, respec- ing the ancestral condition of a single pair of appendages per body tively). The inset shows a higher magnification view of the scape segment shared by arthropods and related groups. Common devel- and pedicel of the springtail antenna. [Photomicrographs taken by opmental features between legs and antennae can be seen, for exam- Dr. J. Nardi, and reproduced with kind permission.]. ple, in the action of the homeotic gene called Antennapedia, which
  • 59. Antennae 23results in the substitution of leglike appendages for antennae on the whole antenna. In contrast, the Böhm bristles, located near thethe head when expressed ectopically in mutant Drosophila. Leglikeappendages appearing in the antennal location in adult insects have scape–pedicel boundary, send information to the brain about the antennal position, rather than its movements. The variety of mech- Aalso been observed after regeneration of antennae following injury anosensory organs associated with the first two segments of theduring the larval stage (Fig. 3). antennae are believed to act together to inform a flying insect about its airspeed, because greater flying speed will cause greater deflec- tion of the antennae by the air rushing past. Contact chemosensory hairs, so called because the chemical compounds are usually detected when the insect is touching a liquid or solid surface with the anten- nae, often have mechanosensory capabilities as well and are usually located near the distal ends of antennae. The function of the antennal sensory organs will be affected by their arrangement on the antennae. For example, sensory organs on the distal tip of a very long antenna will permit chemical or physical sampling of the environment far from the body of the insect. Close packing of sensory hairs will decrease the airflow in their vicinity, and hence will modify both the chemical and physical sampling of the environment by those hairs. The function of the antennae will also be dependent on the behaviors of the insect that will affect the airflow around the antennae, such as flying, wing fanning, postural changes, or oscillating the antennae. A structure projecting into the environment is liable to collect debris that might interfere with itsFIGURE 3 Left: head of an adult Indian stick insect (Carausius sensory function; both antennal grooming behaviors and modifica-morosus) with a normal antenna on the left and a regenerated tions of leg parts against which an antenna is scraped are common inantenna with leglike morphology on the right. Right: head of adult insects. In some insects and other hexapods, antennae are modifiedC. morosus with two regenerated antennae with leglike morphol- for nonsensory functions such as clasping mates during copulationogy. [After Fig. 78 in Wigglesworth, V. B. (1971). “The Principles of (fleas and collembolans), holding prey items (beetle larvae), or form-Insect Physiology.” Chapman & Hall, London, with the kind permis- ing a temporary physical connection between an underwater air res-sion of Kluwer Academic Publishers.] ervoir and the atmosphere (aquatic beetles). FUNCTION See Also the Following Articles The primary function of antennae is the assessment of the chemi- Chemoreception ■ Hearing ■ Imaginal Discs ■ Mechanoreception ■cal and physical characteristics of the environment. Detection is Pheromonesmade with innervated chemosensory and mechanosensory organsthat are arrayed on the antennae. A single antenna usually has sen- Further Readingsory organs of several types, with different properties. Most of the Hansson, B. S., and Anton, S. (2000). Function and morphology of the anten-chemosensory organs are located on the flagellum and often take nal lobe: New developments. Annu. Rev. Entomol. 45, 203–231.the form of microscopic chemosensory hairs (sensilla), each only 1 Heinzel, H., and Gewecke, M. (1987). Aerodynamic and mechanical proper-or 2 μm in diameter. Some antennae, such as the feathery pectinate ties of the antennae as air-current sense organs in Locusta migratoria. II.antennae of silkworms (Bombyx mori), have tens of thousands of Dynamic characteristics. J. Comp. Physiol. A 161, 671–680.sensilla, which are capable of very thoroughly sampling the air that Kaissling, K. E. (1971). Insect olfaction. In “Handbook of Sensory Physiology”passes in the small spaces between them. A cockroach antenna may (L. M. Beidler, ed.), Vol. IV of “Chemical Senses,” Part 1, “Olfaction,”have hundreds of thousands of sensilla. The chemicals that may be pp. 351–431. Springer-Verlag, Berlin.detected by chemoreceptors on the antennae are usually biological Keil, T. A. (1999). Morphology and development of the peripheral olfactoryin origin and airborne (volatiles), although (depending on the insect organs. In “Insect Olfaction” (B. S. Hansson, ed.), pp. 5–48. Springer- Verlag, Berlin.species) the sampled chemical compounds are sometimes in a liq- Loudon, C., and Koehl, M. A. R. (2000). Sniffing by a silkworm moth: Winguid or associated with a solid surface. The chemicals intercepted by fanning enhances air penetration through and pheromone interception byantennae may alert the insect to the presence of prospective mates, antennae. J. Exp. Biol. 203, 2977–2990.food, suitable places to lay eggs, or predators. Pass, G. (2000). Accessory pulsatile organs: Evolutionary innovations in The physical stimuli detected by mechanoreceptors on the anten- insects. Annu. Rev. Entomol. 45, 495–518.nae may be used by the insect to indicate airspeed during flight, to Sane, S., Dieudonne, A., Willis, M., and Daniel, T. (2007). Antennal mech-detect vibrations of the air, or to detect solid boundaries in its envi- anosensors mediate flight control in moths. Science 315, 865–866.ronment by touch. Although a single mechanosensory hair will send Schneider, D. (1964). Insect antennae. Annu. Rev. Entomol. 9, 103–122.information to the brain about the local physical conditions exist- Schneiderman, A. M., Hildebrand, J. G., Brennan, M. M., and Tumlinson,ing at its microscopic location, an antenna also has mechanosensory J. H. (1986). Transsexually grafted antennae alter pheromone-directed behaviour in a moth. Nature 323, 801–803.organs that evaluate the physical forces acting on the antenna as a Steinbrecht, R. A. (1987). Functional morphology of pheromone-whole. These mechanosensory organs, located near the base of the sensitive sensilla. In “Pheromone Biochemistry” (G. D. Prestwich, andantenna, include Johnston’s organ, Böhm bristles, hair plates (groups G. J. Blomquist, eds.), pp. 353–384. Academic Press, London, U.K.of mechanosensory hairs), and campaniform sensilla (thin, flexible Zacharuk, R. Y. (1985). Antennae and sensilla. In “Comprehensive Insectpatches of cuticle that are innervated). Johnston’s organ is located Physiology Biochemistry and Pharmacology” (G. A. Kerkut, and L. I.in the pedicel and responds to changes of location or vibrations of Gilbert, eds.), Vol. 6, pp. 1–69. Pergamon Press, New York.
  • 60. 24 Ants Arguably, the best evidence of the ecological success of ants isA Ants that their worst enemies are other ants. Nigel R. Franks EUSOCIALITY, SOCIAL ORGANIZATION, AND University of Bristol SOCIAL DIVERSITY Except for a few species that have secondarily lost the worker T he ants comprise a single family, the Formicidae, within the caste, all ants are eusocial: they have an overlap of adult generations, superfamily Vespoidea and the order Hymenoptera. There are cooperative brood care, and reproduction dominated by a minority 20 extant subfamilies of ants with a total of 288 extant genera. of the colony’s members. Typically, an established ant colony con- Some 9000–10,000 species of ants have been described, and it is esti- sists of one or more queens (each of which may have mated with mated that there may be 15,000 species of ants alive in the world today. one or more winged males on a nuptial flight), an all-female set of The earliest known fossil ants are from the Cretaceous (ca 120 mya), but wingless workers, and the colony’s brood of eggs, larvae, and pupae. ants probably did not become common until the Eocene (ca 45 mya). The majority of queens mate only before they establish a colony. Thereafter, they store the sperm they have received. All ants have haplodiploid sex determination. This property EVOLUTION AND ECOLOGICAL SUCCESS probably had a major role in the evolution of their eusociality Ants are now extremely successful ecologically. Currently, they through kin selection. Males are haploid, having only a single set may even equal the biomass of humanity. They dominate, at their of chromosomes, and thus the sperm that individual males pro- size scale, many terrestrial ecosystems from latitudes north of the duce is genetically homogeneous. Hence, the (diploid) daughters boreal tree line to such southern climes as Tierra del Fuego, Chile. of the same mother and father are unusually closely related to one In certain tropical forests the contribution of ants to the biomass is another. This is likely to have favored the evolution of female work- spectacular. In Brazilian rain forests, for example, the biomass of ers. Nevertheless, there can be continuing conflicts within colo- ants has been estimated as approximately four times greater than the nies between the workers and the queen (or queens) over the sex biomass of all of the vertebrates combined. ratios they produce and which colony members produce the males. One of the reasons ants are so successful is that their colonies Queens can choose to produce either unfertilized (haploid) eggs have extremely efficient divisions of labor: they evolved factories destined to become males or fertilized (diploid) eggs. The latter millions of years before we reinvented them. Another reason is that may develop into workers or potential new queens (gynes) generally they can modify their immediate environment to suit themselves, depending on how much food they receive as larvae. The workers much as we do. Leafcutter ants (Atta), for example, evolved agri- may or may not be sterile. Fertile workers produce viable (unferti- culture tens of millions of years before humanity developed agron- lized) haploid eggs that can develop into males. Hence, there can be omy. Furthermore, leafcutter ants also use antibiotics and symbiotic conflict both among the workers and between the workers and the bacteria to protect the crop of fungi they grow on the leaves they queen over whose sons the colony produces. Indeed, in many spe- collect. By contrast, weaver ants (Oecophylla) fashion homes from cies of ants with only small numbers of workers in their mature colo- living leaves by sowing them into envelopes, using their larvae as liv- nies, there are dominance hierarchies among the workers, who fight ing shuttles and the silken thread they produce as glue. Ants can also one another over egg production. Sometimes the queen moves with dominate areas by mobilizing large numbers of well-coordinated for- active aggression against the most dominant worker to curtail its pro- agers; indeed, an ant colony’s foragers can be so numerous and well duction of sons in favor of her own. In addition, even when work- organized that they give the impression of being everywhere at once. ers are sterile and serve one, singly mated queen, they may prefer to Ants can also be important as seed distributors and as seed har- raise more of the queen’s daughters, to whom they are more closely vesters, in the turnover of soils, and in the regulation of aphid related, than the queen’s sons. It is clear, though, that the apparent numbers and the minimization of outbreaks of defoliating insects. social cohesion of ant colonies is often partly an illusion. For all these Economically important pest species include the imported fire ant reasons, the study of ants has had a major impact on recent pioneer- (Solenopsis invicta) in North America and leafcutter ants (such as ing evolutionary biology because these insects provide test cases by Atta) in the neotropics. There are also many ecologically destructive which the evolutionary resolution of the tension between coopera- “tramp” ants or invasive species that have been distributed to alien tion and conflict can be explored. habitats by human commerce. Among ants, there is a diversity of mating systems and social Ants and plants often have closely coupled ecological relation- organizations. So even though it is tempting to think of the typi- ships. Certain plants even encourage ants by producing rewards such cal ant colony as having a single, singly mated queen and occupy- as energy-rich elaiosomes on their seeds to encourage seed dispersal, ing a single nest site, the diversity of social systems among the ants nutritious Beltian bodies and extrafloral nectaries to entice ants to visit is in fact huge. For example, many ant species consist of faculta- their leaves and shoots (hence to remove the plant’s natural enemies tively multiqueened (polygynous) colonies. Indeed, roughly half of while there), or even by supplying preformed homes (domatia) to European ant species exhibit polygyny, and there seems to be no invite ants directly to inhabit and thus better protect them. Although reason to regard this as an unusual proportion. Some ant colonies are many ants are hunter-gatherers, very many species tend aphids for the founded by solitary queens; some by groups of unrelated queens that excess honeydew they excrete. By “milking” aphids in this way, ants may later fight over who will be the one to succeed. Other colonies can in effect become primary consumers of plant products and by thus simultaneously occupy multiple nests (polydomy), a habit often asso- operating at a lower trophic level they can build up a larger biomass ciated with polygyny, while others exhibit colony fission, with both than obligate carnivores would be able to do. Yet most ants mix their daughter colonies usually being monogynous. Most persistent polyg- diet by also consuming animal protein; for example, they will devour yny is associated with the secondary adoption of queens. Unusual their own aphid milk cows if the latter become sufficiently abundant. social systems include queenless ants, workerless ants (inquilines),
  • 61. Ants 25and slave-making ants. In certain queenless species, the worker- (A) (B)like females produce other diploid females through a parthenoge-netic process called thelytoky. By contrast, certain inquilines have Adispensed with the worker caste, and queens infiltrate and exploitestablished colonies of other species. Slave making may occur bothintraspecifically and interspecifically. Interspecific slave making isalso associated with nonindependent colony foundation in whichslave-maker queens infiltrate established colonies of their host spe- (C) (D)cies, kill the host queen or queens, and produce workers that arereared by currently available host workers. The slave-maker work-ers raid other neighboring host colonies to capture large larvae andpupae. Such raids thus replenish the stocks of slave workers, whichdo all the foraging and brood rearing for the slave makers. Thereare also ant species in which there are polymorphic queens, othersin which there are polymorphic males, and many in which there arepolymorphic workers. Dry weight (mg) One of the outcomes of eusociality is that established colonies FIGURE 1 The army ant, Eciton burchellii. (A) Head of majorcan be well defended by the workers against enemies. Thus, ant col- worker. (B) Head of minor worker. (C) Head width vs. pronotumonies are relatively K-selected; that is, they are selected to hold onto width allometry for workers. (D) Frequency–dry weight histogramresources and to persist for long periods rather than being ephem- for a large sample of workers. The allometrical relationship has aeral, here-today-gone-tomorrow, r-strategists. Associated with this slope greater than 1, so larger workers (such as majors) have dispro-trait is the extreme longevity of ant queens. It is estimated that they portionately large heads. The size frequency distribution is skewedcan live 100 times longer than other solitary insects of a similar size. to the right so relatively few of these very large majors are produced.Worker populations in mature, well-established monogynous colo- (Drawings © Nigel R. Franks.)nies range from a few tens to 20 million, and certain so-called super-colonies consist of a huge network of linked nests each with manyqueens. One supercolony of Formica yessensis in Japan may have asmany as 300 million workers. Given such longevities and densities, it Such worker polymorphism is now known to be associated withis clear that ants may also prove to be important model systems for the differential growth rates of different putative tissues and bodyunderstanding the spread of disease or the evolution of mechanisms parts during the preadult stages. Indeed, the study of ants made ato minimize the spread of disease among viscous populations of close major contribution to the development of the concept of allomet-kin. It is even possible that polygyny and multiple mating (polyan- ric growth (Fig. 1C and 1D). Notably polymorphic genera includedry) have evolved, at least in part, to promote genetic heterogeneity the army ants Eciton and Dorylus, leafcutter ants (Atta), carpen-within colonies and thus help to minimize disease risks. ter ants (Camponotus), and members of the genera Pheidole and Pheidologeton. Indeed, Camponotus and Pheidole are the two most species-rich ant genera. DIVISION OF LABOR However, genera with polymorphic workers are in the minority. The relatively large biomass of ants in many ecosystems can be Approximately 80% of ant genera consist entirely of species with mon-attributed not just to the way in which the ants interact with other omorphic workers, most of the remaining genera consist of species inorganisms but to the way in which they interact with their nestmates which there are at most only two easily recognizable worker morphs,in general and, in particular, to efficiencies that accrue from divisions and only about 1% of genera have species in which three or moreof labor. One of the most dramatic traits associated with the division worker morphs can be relatively easily recognized within colonies.of labor among the workers is physical polymorphism, which is the Polymorphism among the workers is mostly associated withpresence of different physical worker forms within the same colony. extreme physical specialization. Thus, Eciton majors have ice tong–In the African army ant, Dorylus wilverthi, for example, the small- like mandibles and are specialist defenders of the colony againstest workers at 0.12 mg dry weight are only 1% of the dry weight of would-be vertebrate predators or thieves (Fig. 1A). It has been shownthe largest workers (soldiers), and this relatively great size range is that colonies of Pheidole pallidula can produce more defensive majorsexceeded in certain other species (e.g., in Pheidologeton diversus, in response to stresses induced by conspecific competitors. Majors arethe smallest workers have a dry weight that is about 0.2% that of the not always for defense: large-headed majors in Pheidole and Messorlargest majors). It is not just the size range that is impressive in such serve as specialist grinders of harvested seeds. Even among suchspecies but also the degree of polymorphism among the workers. polymorphic species, however, the majority of workers belong toDarwin, writing in On the Origin of Species, seemed well aware not castes of generalists, which give their colonies an ability to respondonly of the phenomenon but also of its implications. Indeed, one of rapidly to changes in the environment. Such generalists show behav-Darwin’s most penetrating insights in his 1859 masterpiece was his ioral flexibility not possible with the extreme morphological speciali-suggestion that sterile forms evolved in social insects because they zation of certain physical castes. Nevertheless, divisions of labor alsoare “profitable to the community” and that “selection may be applied occur within the majority generalist caste. Such workers typically spe-to the family, as well as to the individual.” He further suggested that cialize in different tasks at different times during their lives. This isonce such colony-level selection had begun, the sterile forms could known as temporal polyethism, in contrast to physical polyethism.be molded into distinct castes “Thus in [the army ant] Eciton, there The sophisticated divisions of labor in monomorphic ants are beingare working and soldier neuters, with jaws and instincts extraordinar- investigated. In Temnothorax albipennis, the workers show very littleily different” (Fig. 1A and 1B). size variation, and colonies consist of, at most, a few hundred such
  • 62. 26 Ants workers living in flat crevices between rocks. Individual workers could have infiltrated ant colonies. For example, more than 200 species ofA easily roam all around such nests within a minute, but instead they have spatial fidelity zones; that is, they remain faithful to certain parts rove beetle (Staphylinidae) are associated with New World army ants alone, and other groups such as mites are probably even more species of the nest and the segregated tasks within such areas for months on rich. Often these infiltrators are called guests simply because their rela- end. The workers can even reconstruct their own spatial fidelity zones tionships with their host ant colony and to its resources are unknown relative to one another if, and when, their colony is forced to emigrate (Fig. 2). to a new nest site because of the destruction of the old site. In this (and many if not all) ant species, younger workers tend to work deep within the nest at its safe center, tending the queen, the eggs, and the larvae. As they get older, workers tend to move progressively out from the center of the nest, and toward the end of their lives, they even- tually engage in the most dangerous task of foraging in the outside world, where they are likely to meet predators and other hazards. However, the correlation between age and task is often very weak, and in an increasing number of species, it has been shown that the division of labor among monomorphic workers is extremely flexible. Workers can respond to the removal of other workers by reverting to tasks that they did earlier in their lives or, if need be, they may begin foraging even when they are very young. Thus, though age may influ- ence what workers do, it is unlikely to be the organizing principle of the division of labor in many species. Rather, it seems that workers are continuously monitoring their workloads and the delays they expe- rience while waiting to interact with their nestmates and will flexibly change their tasks accordingly to maximize their productivity. COMMUNICATION AND PHEROMONES FIGURE 2 Scanning electron micrograph of a worker of Lasius Ants have diverse systems of communication, but by far the most flavus with a kleptoparasitic mite, Antennophorus grandis, gripping important medium for signaling involves the chemicals known as its head. The mite steals food when two workers exchange nutritious pheromones. Ants can deposit chemical trails to recruit nestmates to liquids during trophallaxis. (Photomicrograph © Nigel R. Franks.) discoveries of food, but they also use pheromones during exploration of potential foraging areas and nest sites. Many ants can also produce highly volatile chemicals to signal alarm when they encounter dan- SELF-ORGANIZATION, COLLECTIVE gerous predators or other hazards. Different ants in different sub- families use a remarkable diversity of glandular structures even just INTELLIGENCE, AND DECISION MAKING to produce recruitment pheromones. These may be produced from A rapidly developing approach to the study of ants and other cloacal glands, Dufour’s glands, the hindgut, poison glands, pygidial social insects is the application of self-organization theories. Here glands, rectal glands, sternal glands, or even tibial glands on the back self-organization can be defined as a mechanism for building spatial legs. Furthermore, many pheromones appear to be complex mix- structures and temporal patterns of activity at a global (collective or tures of many chemical compounds. colony) level by means of multiple interactions among components at Pheromones can be effective in minute quantities; it has been the individual (e.g., worker) level. The components interact through estimated that 1 mg of the trail substance of the leafcutting ant, Atta local, often simple, rules that do not directly or explicitly code for the texana, if laid out with maximum efficiency, would be sufficient to global structures. The importance of studies of such self-organization lead a colony three times around the world. is that they can show how very sophisticated structures can be pro- Nestmate recognition is another important aspect of communica- duced at the colony level with a fully decentralized system of con- tion in ants. A pleasing metaphor for the ant colony is a factory inside trol in which the workers have no overview of the problems they are a fortress. Ant colonies are dedicated to the production of more ants; working to solve. but workers need to “know” that they are working for their natal col- A simple and very intuitive example of how ants use self- ony, and colonies also need to be well defended against other ants and organization is found in their ability to select shortcuts. Certain ants against infiltration by other arthropods, which might tap into their can select the shortest paths to food sources. Indeed, where there is resources. Ant colonies employ colony-specific recognition cues as a short and a long path to the same food source, the decision-making one of their defense systems. These are often in the form of cuticular mechanism can be surprisingly simple. The ants that happen to take hydrocarbons that can be spread throughout the colony both by groom- the shorter path get there and back more quickly than the ants that ing and trophallaxis (the latter is usually associated with liquid food happen to take the longer path. All the ants lay attractive trail phe- exchange). Slave-making ants circumvent the recognition cues of their romones, and such pheromones are reinforced more rapidly on the slaves by capturing them as larvae and pupae—these captives are not shorter path simply because that path is shorter and quicker. In such yet imprinted on their natal colony odor but later become imprinted on cases, individual ants do not directly compare the lengths of the two the odor of the colony that kidnapped them after they have metamor- paths, but the colony is able to choose the shorter one. Sometimes phosed into adult workers. Sometimes colony-specific odors also can the shorter path is used exclusively, while at other times a small be influenced by chemicals picked up from the colony’s environment. amount of traffic may continue to use the longer path. Having some Nevertheless, countless species of arthropods from mites to beetles traffic that continues to use the longer path is likely to be costly in
  • 63. Aphids 27the short term, but it may represent a beneficial insurance policy if MAJOR GROUPS AND HOST AFFILIATIONSthe shorter path becomes blocked or dangerous. Self-organizationalso has a major role in such phenomena as brood sorting, rhythms Aphids, as the superfamily Aphidoidea, belong to the Hemipteran A Sternorrhyncha with Aleyrodoidea (whiteflies), Psylloidea (jumpingof activity within nests, and building behaviors. This new approach plant lice), and Coccoidea (scale insects and mealybugs). Aphidoideamay help to answer, at least in part, the age-old challenge of how ant has three families: Adelgidae (adelgids), Phylloxeridae (phylloxerids),colonies are organized. and Aphididae. Some workers place the Adelgidae and Phylloxeroidea in a separate superfamily, Phylloxeroidea. Adelgids and phylloxeridsSee Also the Following Articles are primitive “aphids” and older groups, each with about 50 species. They differ from Aphididae by having an ovipositor and reproduc-Caste ■ Colonies ■ Nest Building ■ Pheromones ■ Sex Determination ■Sociality ing by means of ovipary, whereas Aphididae lack an ovipositor and are parthenogenetically viviparous, bearing live young. Adelgids are restricted to conifers in Pinaceae where some form charac-Further Reading teristic galls. Phylloxerids, which may also form galls, occur as theBolton, B. (2003). “Synopsis and Classification of Formicidae.” American tribe Phylloxerinini on Salicaceae, or as the tribe Phylloxerini on Entomological Institute, Gainesville, FL. Fagaceae, Juglandaceae, Rosaceae, Ulmaceae, and Vitaceae. AnBourke, A. F. G., and Franks, N. R. (1995). “Social Evolution in Ants.” important phylloxerid, Daktulosphaira vitifoliae, grape phylloxera, Monographs in Behavioral Ecology. Princeton University Press, can kill European grapevine cultivars unless they are grafted to Princeton, NJ. resistant rootstocks developed from American grape species. ThisCamazine, S., Deneubourg, J.-L., Franks, N. R., Sneyd, J., Theraulaz, G., and species devastated the wine industry a century ago. Bonabeau, E. (2001). “Self-Organization in Biology.” Princeton University Aphids (Fig. 1) are diverse and have many specialized morpho- Press, Princeton, NJ. logical structures that vary among groups. The most unique areCouzin, I. D., and Franks, N. R. (2002). Self-organized lane formation and optimized traffic flow in army ants. Proc. Roy. Soc. Lond. B 270, paired siphunculi (cornicles) that release an alarm pheromone. 139–146. These vary from being mere pores on the abdominal surface toFrederickson, M. E., Greene, M. J., and Gordon, D. M. (2005). Devil’s gar- being very elongate and sometimes elaborate tubes. Aphids also have dens’ bedeviled by ants. Nature 437, 495–496. a cauda, used to manage honeydew, on the abdominal terminus. ThisHölldobler, B., and Wilson, E. O. (1990). “The Ants.” Belknap Press, may vary from rounded, to knobbed, to long and fingerlike. Some Cambridge, MA. aphids produce waxy cuticular excretions and can resemble otherKeller, L., and Genoud, M. (1997). Extraordinary lifespans in ants: A test of Sternorrhyncha. Aphids probably had a Permian origin, but their old- evolutionary theories of ageing. Nature 389, 958–960. est fossils are Triassic (230 mya). Modern aphids began diversifica-Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B., and Pierce, N. E. (2006). tion with angiosperms in the lower Cretaceous (140 mya). Most fossil Phylogeny of the ants: diversification in the age of angiosperms. Science aphid groups became extinct during the Cretaceous–Tertiary bound- 312, 101–104. ary, and most current groups radiated during the Miocene. AphidsPowell, S., and Franks, N. R. (2007). How a few help all: Living pothole plugs speed prey delivery in the army ant Eciton burchellii. Anim. Behav. 73, originally evolved on woody plants in the Northern Hemisphere, and 1067–1076. are functionally replaced by whiteflies and psyllids in the SouthernSchmidt-Hempel, P., and Crozier, R. H. (1999). Polyandry versus polygyny Hemisphere. versus parasites. Philos. Trans. R. Soc. (Lond) (B) 354, 507–515. The taxonomy of Aphididae is quite difficult and subfamily demar-Sendova-Franks, A. B., and Franks, N. R. (1994). Social resilience in indi- cation has been argued through many classifications. Remaudiere vidual worker ants and its role in division of labour. Proc. R. Soc. (Lond) and Remaudiere’s 1997 classification, followed here, recognizes (B) 256, 305–309. about 25 aphid subfamilies, with tribal groupings for about 600 genera and 4700 species of aphids. Many aphid lineages coevolved with, and radiated among, their host plant groups. Often during their phylogenetic history, however, some aphid groups opportunistically switched to radically unrelated host groupings, driven by develop- mental requirements but tempered by evolutionary constraints. Aphids Many aphid subfamilies are small, but several are larger and important: Chaitophorinae on Salicaceae and Gramineae; the closely related Myzocallidinae, Drepanosiphinae, and Phyllaphidinae, often John T. Sorensen considered to be one subfamily and usually on dicotyledonous trees, California Department of Food and Agriculture but also Fabaceae and bamboo; Lachninae, mostly on Pinaceae, but also Fagaceae, Rosaceae, and roots of Asteraceae; and Pemphiginae,A phids are remarkable, evolutionarily exquisite creatures, often on roots and host alternating to dicotyledonous trees forming and are among the most successful insects. Aphid evolution galls. Other noteworthy subfamilies include Pterocommatinae, on has been shaped through nutrient-driven selection and by Salicaceae; Greenideinae, on Fagaceae; Mindarinae, on Pinaceae;the host plants on which they feed, and aphids have responded by and the host-alternating Anoeciinae and Hormaphidinae.developing intricate life cycles and complex polymorphisms. These The largest and most evolutionarily recent subfamily, Aphidinae,sap-feeding hemipterans have coped with a hostile world through has two large, diverse, and agriculturally important tribes:developing an exceptionally high reproductive rate and passive wind- Macrosiphini and Aphidini. Macrosiphini is diverse in genera; itsborne dispersal, a strategy in which individuals are quite expendable, species usually lack attendance by ants. Aphidini is diverse in spe-but survival and prosperity of their genes are guaranteed. Because cies, which are often ant attended, but less diverse in genera. Tribeof their intriguing evolutionary adaptations, aphids were among our Aphidini has two important subtribes. Subtribe Rhopalosiphinamost worthy competitors as humans entered the agricultural era. host alternates between Rosaceae and Gramineae or Cyperaceae.
  • 64. 28 Aphids Subtribe Aphidina host alternates mostly among Rosidae and In the simple and generalized monoecious holocyclic aphid lifeA Asteridae and is home to the large and agriculturally important genus Aphis. cycle (Fig. 2A), a single host plant species is used throughout the year and sexual morphs are produced in the fall, usually in response to decreasing day length. The males and oviparae mate, produc- ing genetically recombinant eggs that overwinter on the host plant and often experience high mortality. In the spring, the fundatrix emerges from the egg, matures, and gives parthenogenetic live birth to nymphs that become viviparae and continue in that reproductive mode through the summer. If the aphid group produces plant galls, the fundatrix is responsible for their production. The viviparae may be apterae (wingless) or alatae (winged), but (A) (B) in some groups all viviparae are alatae. The parthenogenetic repro- duction of viviparae allows a very rapid population buildup. At birth, each viviparous nymph has within it the embryos of its daughters and granddaughters, creating a “telescoping” of generations. Apterae, lacking wings and their associated musculature, are optimized for reproduction, and have more offspring per female than do alatae. Alatae invest resources in their flight apparatus and are optimized (C) (D) for dispersal. Alatae, however, begin progeny production earlier in life than do apterae, giving the alatae relatively reduced number of offspring and a better generational turnaround time. Apterae are produced selectively when nutrient production by their hosts is high. Once an aphid population has increased enough to induce crowding and stress its host’s nutrient levels, the population usually switches to alatae production. This allows dispersal to better feeding situations and optimizes the genetic survival of the clone. Alate flight is mostly (E) (F) passive in the wind, and after successfully alighting on their proper host, often by chance, alatae feed for a short time before begin- ning autolysis of their flight musculature. While precluding further flight, the autolysis self-cannibalistically provides nutrients for their offspring. The production of viviparae continues until fall conditions trigger production of the sexuals. A second, more complicated dioecious life cycle (Fig. 2B) has (G) (H) independently evolved among several different aphid groups that show seasonal alternation between differing hosts. This cycle prob- ably evolved in response to the seasonally inadequate supply of nitrogen-based nutrients, especially amino acids, on the primary host. The phloem sap that aphids feed upon has limited nitrogen availabil- ity, which inhibits adequate protein synthesis during aphid develop- ment. Woody deciduous plants normally translocate amino acids in (I) (J) quantity only during spring foliation and fall leaf senescence. The latter breaks down leaf protein allowing nitrogen translocation to the roots for overwinter storage and future spring plant growth. Aphid FIGURE 1 Aphid diversity and morphs: (A) Aphis nerii apterae, groups evolving on, and restricted to, such plants face a nitrogen (B) Uroleucon ambrosiae apterae, (C) Acyrthosiphon kondoi aptera deficit during summer, when active plant growth ceases and phloem giving birth, (D) Dysaphis plantaginea apterae, (E) Neophyllaphis sap is low or devoid of nitrogen. Such groups (e.g., Periphyllus spp.) podocarpi apterae with flocculent wax, (F) Prociphilus americanus may develop an aestivating nymph that halts growth until fall. apterae with filamentous wax and pseudococcidlike appearance, (G) Other groups, such as Aphidinae, whose ancestors originated Aphis spiraecola alata and apterae, (H) Cerataphis orchidearum on deciduous woody plants, have evolved to leave those primary aptera with wax fringe resembling an aleyrodid, (I) Rhopalosiphum hosts during the late spring, after the nitrogen flush of foliation has nymphae ovipara and winged male in copula, and (J) Acyrthosiphon ceased. In doing so, their spring alatae, as emigrants, migrate to her- kondoi (left) and A. pisum (right) alatae. [Photos by T. Kono (A–F, I, baceous secondary hosts that actively grow and translocate nitrogen J)/R. Garrison (G, H).] during summer. In fall, however, as these secondary hosts die back, the aphids return to their woody primary host by producing winged migrating males and gynoparae, the latter giving rise to oviparae. NUTRITION-DRIVEN EVOLUTION: LIFE Upon returning, the aphid’s sexuals (its males and oviparae) capture CYCLES AND POLYMORPHISM the primary host’s fall nitrogen flush and mate to lay their overwin- The complex life cycles of aphids have caused many specialized tering eggs in anticipation of the spring nitrogen flush. morphs to evolve. These have many confusing, synonymous names, Among most aphid lineages, the primary hosts are often specific but the names are minimized here. Aphid life cycles can be either as to plant genus. Secondary hosts for lineages, however, may vary monoecious or dioecious and involve holocycly or anholocycly. from being quite specific as to host species to using a broad number
  • 65. Aphids 29of botanical groups. Most lineages use a particular type of second- anholocyclic long enough, they may eventually evolve into obligateary host, such as grasses, roots, other woody plants, or herbs. Someaphids specialize on secondary hosts of a particular environmental anholocycly by losing the ability to produce sexual morphs, despite undergoing environmental conditions that normally trigger their pro- Aecotype. For example, Rhopalosiphum nymphae, water lily aphid, duction. In the U.S. Midwest, the anholocyclic clones of some aphiduses aquatic plants in many plant families. Among aphid lineages, species are blown, on seasonal winds, south in the fall to the warmernearly all morphs may be winged or wingless, depending on the Gulf States and back north in the spring, effectively allowing a pas-aphid group, its adaptation to its host(s), or their alternation. sive “migration” to avoid clonal mortality in the northern winter. Primary Secondary APHID BEHAVIOR Host Host Evolutionary selection has dictated efficiency in aphid behav- iors as well as the expendability of individuals. To feed proficiently, Monoecious holocycly Monoecious holocycly aphids insert and ratchet their rostrum-borne stylets between plant (A) Fundatrix Fundatrix (C) cells, seldom penetrating any until reaching the phloem sieve tubes to extract sap. The stylets are lubricated by pectinase-containing saliva that both loosens plant cell bonding and forms a stylet sheath Egg Aptera Alata Egg Aptera Alata that is left behind when the stylets are withdrawn. To cope with a sap diet, aphid guts have specialized groups of cells, mycetomes, Male containing rickettsialike symbiotic bacteria, mycetocytes, which aid Male ؉ + in synthesis of nutrients. These bacteria are passed between aphid Ovipara Ovipara generations and have coevolved with, and differentiated between, aphid phyletic lineages. Morph-specific behaviors promote genetic survival of the indi- vidual and its clones. Alatae initially taking flight are attracted to the Alata (emigrant) short wavelengths that predominate in the sky, which they fly toward Fundatrix to optimize dispersion. During descent their preference changes to the longer light wavelengths reflected by plants, especially the yel- low hue of senescent plants that are better nitrogen sources. After Egg Aptera Alata alighting, they accept a plant for feeding only after briefly probing their rostral tip below the plant’s epidermis to sense the presence (B) of specialized secondary plant compounds that are of no nutritional Male Dioecious Ovipara (D) value, but are specific to their given host. Apterae, in contrast, move holocycly only when necessary to procure a better feeding site or avoid pre- Gynopara Aptera Alata dation. Ants may tend some aphid groups in a form of facultative mutualism in which the ants may actively “farm” their aphid “cat- Anholocycly tle,” moving them among locations. In exchange for the aphid’s sug- ary honeydew, the ants protect them from predation and parasitism.FIGURE 2 Evolutionary development of generalized aphid life When stroked by an ant’s antennae, the aptera will raise the tip of itscycles. Initially, (A) aphids developed monoecious holocycly on an abdomen extruding a honeydew drop, which may be retracted if notancestral woody primary host, where aestivation occurred because accepted by the ant. In the absence of a tending ant, the aphid willsap amino acids were unavailable during summer growth cessation. revert to its normal flicking of the honeydew drop away with its hindNext, (B) multiple subfamilies independently evolved dioecious leg or cauda to prevent an accumulation of honeydew from foulingholocycly, where viviparae moved to summer-growing herbaceous the aphid colony. Generally, aphid groups with elongate siphunculisecondary hosts but returned to their ancestral host in autumn. In are less likely to be tended by ants.some aphids, (C) secondarily monoecious holocycly developed on Aphids use chemical and sound communication, especially to foilthe secondary host when the primary host was lost. Often in warm parasites and predators. When molested, aphids exude microdrop-areas, where selection for an overwintering egg is not imposed, some lets of trans-β-farnesene, an alarm pheromone, from their siphun-populations of dioecious and secondarily monoecious holocyclic cular pores. In response, adjacent aphids quickly drop to the groundaphids may lapse into (D) facultative anholocycly on their secondary to escape. Aphid oviparae use sexual pheromones released from spe-hosts; this condition may become obligate anholocycly if the ability cialized pores on their hind tibiae to attract males. Toxoptera spp.to produce sexuals is lost. emit audible warning stridulatory sounds to which their aggregation responds. The stridulatory mechanism in this genus consists of a row Some aphid lineages have evolved beyond dioecious holocycly to of short pegs on the hind legs that are rubbed against filelike ridgessecondary monoecious holocycly (Fig. 2C), by entirely leaving their on the lower abdominal epidermis below the siphunculi.primary woody host to remain on their secondary herbaceous host Some aphids use morph-specific behaviors to wound plants,and producing overwintering eggs on it. Another important form creating galls and leaf necrosis or distortion, thereby manipulatingof year-round residence on the secondary host occurs in warmer their host to promote nutrition and protection (Fig. 3). Fundatricesclimates, where populations do not require an egg for overwinter- of gall-forming species use species-specific patterns of feeding oring survival. Under such conditions, otherwise holocyclic dioecious probing behavior to induce characteristically shaped galls on theiror monoecious populations may lapse facultatively into anholocycly specialized hosts. Not only do plant galls provide a protective encase-on their secondary hosts (Fig. 2D). If such populations remain ment for aphid development, but aphids of even nongalling species
  • 66. 30 Aphids do better on galled tissue, probably because of a local increase in discuss in detail 14 aphids as the most serious agricultural pests.A plant nutrients in that tissue. Some non-gall-making species employ phytotoxins to induce leaf distortion or necrosis to similarly promote Thirteen of these are in the Aphidinae, the largest aphid subfamily, which contains a high proportion of herbaceous plant feeders. Of additional nutrient production by their host. these, Aphis craccivora, Aphis fabae, Aphis gossypii, and Aphis spiraecola are in tribe Aphidini, subtribe Aphidina; Rhopalosiphum maidis, Rhopalosiphum padi, and Schizaphis graminum are in tribe Aphidini, subtribe Rhopalosiphina; and Acyrthosiphon pisum, Diuraphis noxia, Lipaphis pseudobrassicae (sensu Eastop), Macrosiphum euphorbiae, Myzus persicae, and Sitobion avenae are in tribe Macrosiphini. The fourteenth species, Therioaphis trifolii, is in tribe Myzocallidini of subfamily Myzocallidinae (ϭCalaphidinae sensu Eastop), a group normally found on trees, but in which (A) (B) Therioaphis has diverged on to herbaceous Fabaceae. Aphids cause damage and lower agricultural yields in several ways. They can build to high population densities, removing plant nutrients, and may damage plants by removing enough sap to cause withering and death. If not washed off, aphid honeydew excrement can build enough on plants to be a growth medium for sooty molds that impair photosynthesis and promote other fungal diseases. Salivary secretions (C) (D) of some aphids are phytotoxic, causing stunting, leaf deformation, and gall formation, which is of particular concern to horticulture. Even if otherwise asymptomatic, aphid-feeding effects may affect plant hormone balances changing host metabolism to their advantage and essentially hijacking the plant’s physiological functions. The most serious problem posed by aphids is the vectoring of plant viruses. Virus-infected plants often show an aphid-attractive (E) (F) yellowing and have increased free amino acids, so aphids benefit by virus transmission. Stylet-borne viruses, occurring on the aphid’s epi- FIGURE 3 Aphid damage: (A) necrotic feeding damage on pecan, dermis, are not aphid specific. They are acquired quickly and trans- (B) leaf curling on ivy by Aphis hederae f. pseudohederae, (C) cone- mitted during rostral probing of the plant’s epidermis. These are like galls on spruce by Adelges sp., (D) leaf edge galls on poplar by nonpersistent viruses whose infectiousness is lost when the aphid Thecabius sp., (E) leaf petiole gall on poplar by Pemphigus sp.- gall molts. Circulative viruses, in contrast, live in the aphid’s gut and split showing yellow fundratrix, and (F) leaf galls on manzanita by require an incubation period before successful transmission. They are Tamalia sp. (Photos by T. Kono.) persistent viruses and an aphid, once infected, remains a vector for life. Circulative viruses have fairly specific virus–aphid–plant linkages Aphid social behavior is usually expressed as gregarious- and any given virus is transmitted by only one or few aphid species. ness within colonies, probably to confer better protection or response to attack. This is usually seen in apterae and nymphs, APHID CONTROL IN AGRICULTURAL CROPS but occurs in alatae of some species as clustering with tactile con- AND HOME GARDENS tact (e.g., Drepanosiphum platanoides). Some genera of the tribe Cerataphidini of Hormaphidinae have evolved sociality further to Agricultural control of aphids best uses an integrated pest man- produce defensive soldier morphs with enlarged forelegs. These sol- agement (IPM) strategy, where species are identified and tactics diers discriminate between other soldiers and nonsoldiers but do not reflect allowable tolerances on a crop. Cultivation of aphid-resistant attack soldiers of their own species. The investment in soldier pro- crop varieties is important. Aphids may be monitored using yellow duction by the colony is related to areas needing defense, such as a water pans or sticky traps in fields. In some agricultural regions, gall’s nutrient-rich surface. especially seed-growing areas with plant virus sensitivities, aerial suction trap networks are used to detect alatae and forecast popu- lation levels. IPM of aphids minimizes effects on nontarget species AGRICULTURAL IMPORTANCE (i.e., biological control agents, vertebrates). Tactics include cultural Aphid damage is among the most serious of agricultural and hor- control methods (e.g., minimizing ant populations, using ultraviolet- ticultural problems. A pest aphid species may affect only a very spe- reflecting films to repel alatae, or interplanting pollen and nec- cific crop, a group of related crop hosts (e.g., crucifers), or may be tar source plants among crop rows to promote natural enemies). quite polyphagous within and between plant families. Many of the Parasitic wasps or predators can be released for biological control. notoriously polyphagous aphid pests represent sibling species com- Effective predators include immature lacewings, aphid midges, and plexes that are morphologically identical but differ in karyotype. ladybird beetles, all of which voraciously consume aphids but are Generally, such aphid pests comprise anholocyclic clones, or bio- less likely to disseminate when released than adults. The spores of types, that differ in host preferences, the ability to transmit diseases, entomopathic fungi can be used. Aphid growth regulators can be or resistance to pesticides. applied by spray to prevent maturation. Chemical poisons, ranging Blackman and Eastop, in Van Emden and Harrington’s 2007 from pyrethroids to toxic organophosphates, should be minimized book, estimate that although about 450 species occur on crops, only but may be necessary sometimes. These may be applied as contact about 100 species pose significant economic problems. They list and sprays or dusts, or as systemic insecticides. Poisons not only hamper
  • 67. Apis Species 31biological control agents, but their heavy use promotes the insecti- warmer tropics. The most important species to humans is A. mellifera,cidal resistance and secondary resurgence of aphid populations. In residential settings, nontoxic controls should be emphasized which has been introduced all over the world for use in beekeeping. Aafter aphid detection by inspecting congregation sites such as buds, THE GENUS APISstems, fruits, and leaf undersides. Effective aphid control may simplyinvolve frequently hosing off leaf undersides with water. Safe spray Known Speciesapplications involve repellent garlic and water mixtures, or cuticle- The genus Apis contains 11 known species. A. mellifera (Fig. 1)disrupting/desiccating insecticidal soaps. Problems from aphid sooty is the source of most of the world’s honey. It is native throughoutmolds under overhanging trees are best controlled by hosing off Africa, the Middle East, and Europe except for the far north regions.driveway, patio, and walkway surfaces. Control for aphid galls or leaf All other Apis species are native to Asia. A. cerana which is kept indistortion can be problematic. Sometimes deciduous trees require hives in the temperate zone as well as the tropics, is smaller thanthe winter application of dormant oil to kill overwintering eggs. A. mellifera, and it makes smaller colonies. Other Asian speciesLandscape tree species should be carefully selected and placed, con- that build a multiple-comb nest in a cavity are A. koschevnikovi andsidering their aphid pests, because ultimately elimination of the tree A. nuluensis reported in Borneo and A. nigrocincta in Sulawesi.may be required to solve the problems.See Also the Following ArticlesAnts ■ Biological Control ■ SternorrhynchaFurther ReadingBlackman, R. L., and Eastop, V. F. (1994). “Aphids on the World’s Trees: An Identification and Information Guide.” CAB International, Wallingford, U.K.Blackman, R. L., and Eastop, V. F. (2000). “Aphids on the World’s Crops: An Identification and Information Guide.” 2nd ed. Wiley, New York.Blackman, R. L., and Eastop, V. F. (2006). “Aphids on the World’s Herbaceous Plants and Shrubs. Vol. 1. Hosts and Keys; Vol. 2. The Aphids.” Wiley, New York. FIGURE 1 Worker honey bees (Apis mellifera) on honeycomb.Dixon, A. F. G. (1998). “Aphid Ecology.”, 2nd ed. Chapman and Hall, (Photograph courtesy of P. Kirk Visscher.) London, U.K.Minks, A. K., and Harrewijn, P. (1987). Aphids, Their Biology, Natural Other Apis species native in parts of the Asian tropics build a Enemies and Control Vols. A, B, C Elsevier, Amsterdam. single-comb nest in the open. The most important to humans isMoran, N. (1992). The evolution of aphid life cycles. Annu. Rev. Entomol. A. dorsat