The Braconid and Ichneumonid Parasitoid Wasps Biology, Systematics, Evolution and Ecology

The Ichneumonoidea is a vast and important superfamily of parasitic wasps, with some 60,000 described species and estimated numbers far higher, especially for small-bodied tropical taxa. The superfamily comprises two cosmopolitan families - Braconidae and Ichneumonidae - that have largely attracted separate groups of researchers, and this, to a considerable extent, has meant that understanding of their adaptive features has often been considered in isolation. This book considers both families, highlighting similarities and differences in their
adaptations.

The classification of the whole of the Ichneumonoidea, along with most other insect orders, has been plagued by typology whereby undue importance has been attributed to particular characters in defining groups. Typology is a common disease of traditional taxonomy such that, until recently, quite a lot of taxa have been associated with the wrong higher clades. The sheer size of the group, and until the last 30 or so years, lack of accessible identification materials, has been a further impediment to research on all but a handful of ?lab rat? species usually cultured initially because of their potential in biological control.

New evidence, largely in the form of molecular data, have shown that many morphological, behavioural, physiological and anatomical characters associated with basic life history features, specifically whether wasps are ecto- or endoparasitic, or idiobiont or koinobiont, can be grossly misleading in terms of the phylogeny they suggest. This book shows how, with better supported phylogenetic hypotheses entomologists can understand far more about the ways natural selection is acting upon them.

This new book also focuses on this superfamily with which the author has great familiarity and provides a detailed coverage of each subfamily, emphasising  anatomy, taxonomy and systematics, biology, as well as pointing out the importance and research potential of each group. Fossil taxa are included and it also has sections on
biogeography, global species richness, culturing and rearing and preparing specimens for taxonomic study. The book highlights areas where research might be particularly rewarding and suggests systems/groups that need investigation. The author provides a large compendium of references to original research on each group. This book is an essential workmate for all postgraduates and researchers working on ichneumonoid or other parasitic wasps worldwide. It will stand as a reference book for a good number of years, and while rapid advances in various fields such as genomics and host physiological interactions will lead to new information, as an overall synthesis of the current state it will stay relevant for a long time.

Preface xiii

Acknowledgements xv

1 Introduction 1

Life history 5

Systematics 6

Part 1 Morphology and Biology 7

2 Adult External Morphology 9

Head 10

Antennal sensilla 12

Antennal glands and tyloids 14

Palps 15

Mesosoma 15

Legs 17

Wings wing venation and wing cells 18

Confusing and sometimes erroneously applied vein names 26

Wing flexion lines 27

Metasoma 29

Sexual dimorphism 30

Male external genitalia 32

3 The Ovipositor and Ovipositor Sheaths 35

The act of oviposition 39

Functional morphology of wood-drillers 41

Ovipositor stabilisation guides and buckling force 43

Ovipositor notches and endoparasitism 44

Ovipositor steering mechanisms 44

Proposed evolutionary and related ovipositor transitions 48

Number position and possible functions of ovipositor valvilli 50

Venom retention and delivery 52

Ovipositor secretory pores 53

Ovipositor sensilla 54

Ovipositor sheaths 55

4 Internal and Reproductive Anatomy 57

Nervous system 58

Digestive tract 58

Female internal reproductive system 59

Ovaries 59

Time scale of egg maturation 60

Spermatheca 61

Common oviduct and vaginal gland 62

Venom gland and reservoir 63

Dufour’s gland 64

Cuticular hydrocarbons 66

Sex pheromones 67

Male internal reproductive system 68

Sperm ultrastructure 69

Spermatogeny index 70

5 Immature Stages 71

Eggs and oögenesis 72

Hydropic and anhydropic eggs 72

Embryogenesis 73

Embryonic membranes 75

Larva 76

Larval feeding and nutrition 81

Larval food consumption and dietary efficiency 82

Lipid metabolism 82

Respiration in endoparasitoids 83

Larval secretions 83

The pupal stage 84

Cocoons 84

6 Idiobionts Koinobionts and Other Life History Traits 87

Parasitoidism 88

Idiobiont and koinobiont strategies 88

Generalists and specialists 89

Ecto- and endoparasitism 90

Permanent host paralysis 91

Gregarious development 91

Superparasitism 92

Larval combat and physiological suppression 93

Adaptive superparasitism 95

Multiparasitism 96

Obligate and preferential multiparasitism 99

Hyperparasitism and pseudohyperparasitism 99

Kleptoparasitism 100

Evolution of life history strategies 100

7 Sex Courtship and Mating 107

Sex determination 108

Local mate competition and avoidance of inbreeding 110

Sex allocation 110

Protandry and virginity 112

Thelytoky and cytoplasmic incompatibility 113

Mate location 117

Courtship 119

Swarming and lekking 120

Mating position 121

Multiple mating and sperm competition 121

Sex-related scent glands 123

Genome size and recombination 125

Cytogenetics 125

8 Host Location Associative Learning and Host Assessment 127

Tritrophic interactions 129

Host acceptance 130

Associative learning 130

Biosensors 134

Patch use 134

9 Overcoming Host Immune Reaction and Physiological Interactions With Host 137

Overcoming host immunity in endoparasitoids 138

Passive evasion of encapsulation by parasitoid eggs 139

Avoiding encapsulation by physical means 139

Effect of host age and haemocyte number 141

Other host defence mechanisms 141

Venoms 141

Neurophysiological venom actions 143

Venom effects on host immune response 144

Polydnaviruses 145

Effects of polydnaviruses on hosts 152

Other reproductive viruses 155

Improving host quality 156

Host castration and similar effects 156

Teratocytes 158

Intraspecific variation in resistance to parasitoids 159

Effects on host moulting pattern 160

Parasitoid-induced changes in host behaviour 160

10 Convergent Adaptations 163

Antennal hammers and vibrational sounding 164

Enlarged mandibles 167

Chisel-like mandibles 168

Concealed nectar extraction apparatus 168

Reduced number of palpal segments 169

‘Facial’ protruberances 169

Frontal depressions 170

Dorsal ridges on head or mesosoma 170

Brachyptery and aptery 170

Dorso-ventral flattening 171

Postpectal carina 173

Propodeal spines 173

‘Fossorial’ legs 173

Fore tibial spines 174

Fore tibial apical tooth 174

Expanded hind basitarsi 174

Toothed hind femur 174

Distitarsal scraper 175

Pectinate claws and claws with angular basal lobes 175

Glabrous wing patches and wing membrane scleromes 176

Carapacisation 177

Petiolate metasomas 177

Modifications to the posterior metasomal margin 178

Spermathecal colour 179

Compression of apical part of metasoma 179

The ‘ophionoid facies’ 179

White antennal stripes and tips 180

White ovipositor sheath stripes and tips 181

Number of larval instars 182

Egg-larval parasitism 182

Disc-like larval antennae 182

Reduction of larval hypostomal spur 183

Wide and heavily sclerotised larval epistoma 184

Suspended cocoons 184

Polyembryony 184

Phytophagy and cecidogenesis 184

Part 2 Taxonomic and Systematic Treatment 187

11 Overview of Ichneumonoidea: Relationships and Systematics 189

Monophyly of Ichneumonoidea Ichneumonidae and Braconidae 190

Relationship of Ichneumonoidea to other Hymenoptera 190

Fossil history and family-level phylogeny 192

Brief history of classification 194

Ancestral biology of Ichneumonoidea 196

Separating ichneumonids from braconids 197

Identifying specimens 198

12 Phylogeny and Systematics of The Braconidae 201

Historical perspective 202

Morphophylogenetic hypotheses 202

Molecular phylogenetics 204

Braconid classification 205

Eoichneumoninae^† 205

Trachypetiformes 205

Trachypetinae 205

Cyclostomes incertae sedis 209

Protorhyssalinae et al. 209

Apozyginae 210

The aphidioid clade or ‘Gondwanan’ complex 212

Aphidiinae 212

Maxfischeriinae 224

Mesostoinae (including Canberreriini and Hydrangeocolini) 225

The remaining cyclostomes 229

Doryctinae (including Ypsistocerini) 231

Pambolinae 236

Rhysipolinae 237

Rhyssalinae 238

Rogadinae s.l. Hormiinae Lysiterminae 243

Betylobraconinae 243

Hormiinae 243

Lysiterminae 245

Rogadinae sensu stricto 246

Alysioid subcomplex including Braconinae 250

Alysiinae and Opiinae 250

Alysiinae 251

General Alysiinae biology 251

Alysiini 253

Dacnusini 255

Opiinae 256

Braconinae 260

Exothecinae 269

Gnamptodontinae (= Gnaptodontinae) 270

Telengaiinae 271

The non-cyclostomes 271

Sigalphoid complex 271

Agathidinae 272

Sigalphinae 275

Helconoid complex 278

Helconinae 279

Helconoid group incertae sedis 281

Blacinae 282

Acampsohelconinae 283

Macrocentrine subcomplex 284

Macrocentrinae 284

Charmontiinae 287

Amicrocentrinae 287

Xiphozelinae 288

Homolobinae 290

Microtypinae 292

Orgilinae 292

Euphoroid complex 294

Euphorinae 294

Cenocoeliinae 310

The microgastroids 311

Cardiochilinae 312

Cheloninae (including Adeliini) 315

Dirrhopinae 319

Ichneutinae 320

Khoikhoiinae 322

Mendesellinae 322

Microgastrinae 322

Miracinae 335

Unplaced subfamilies 335

Masoninae 335

Meteorideinae 337

13 Phylogeny and Systematics of The Ichneumonidae 341

History of ichneumonid classification 342

Henry Townes (1913–90) and his idiosyncratic nomenclature 344

The extinct subfamilies 344

Tanychorinae^† 344

Palaeoichneumoninae^† 346

Labenopimplinae^† 348

Pherombinae^† 349

Townesitinae^† 349

The xoridiformes 349

Xoridinae 349

The labeniformes 353

Labeninae 353

Groteini 355

Labenini 355

Poecilocryptini 356

The pimpliformes 356

Acaenitinae 356

Collyriinae 359

Cylloceriinae 360

Diacritinae 360

Diplazontinae 361

Orthocentrinae (= Helictinae) 366

Pimplinae 367

Delomeristini 369

Ephialtini (= Pimplini of Townes) 369

Polysphincta group 371

Pimplini 373

Poemeniinae (= Neoxoridinae) 378

Poemeniini 378

Pseudorhyssini 378

Rodrigamini 378

Rhyssinae 379

The ichneumoniformes 383

Adelognathinae 383

Agriotypinae 385

Alomyinae 387

Cryptinae 388

Aptesini 391

Cryptini 391

Phygadeuontini 393

Ichneumoninae 394

The brachycyrtiformes 398

Brachycyrtinae 398

Claseinae (Clasinae) 398

Pedunculinae 399

The orthopelmatiformes 400

Orthopelmatinae 400

The ophioniformes 400

Lower ophioniformes 402

Banchinae 402

Lycorininae 406

Sisyrostolinae 407

Stilbopinae 407

Tryphoninae 411

Middle ophioniformes 416

Ctenopelmatinae 416

Mesochorinae 421

Metopiinae 422

Oxytorinae 424

Tatogastrinae 425

Tersilochinae (including Neorhacodinae and Phrudinae s.s.) 426

Higher ophioniformes 430

Anomaloninae 430

Campopleginae 432

Cremastinae 438

Hybrizontinae 439

Nesomesochorinae 442

Ophioninae 442

Unplaced subfamilies 445

Eucerotinae 445

Microleptinae 447

Part 3 Ecology and Diversity 451

14 Ecology 453

Adult diet 454

Host-feeding 454

Water sugar and pollen feeding 457

Fecundity 460

Voltinism and seasonality 462

Daily activity patterns 462

Diapause 463

Cold hardiness hibernation and overwintering 465

Coloration and thermoregulation 467

Biological control 467

Effect on host food consumption 471

Artificial diets 474

Artificial hosts 475

Use of alternative hosts 475

Hyperparasitism and kleptoparasitism 476

Predation 477

Pathogens 477

Transmission of host pathogens 479

Dispersal 480

Coloration and mimetic rings 480

Palatability and odours 481

Competition 482

Apparent competition 482

Host ranges of parasitoids 483

Parasitoid guilds and food webs 484

Evolution of host ranges and speciation 486

15 Local and Global Patterns In Diversity 489

Field research in the tropics and anomalous diversity 490

Estimation of global ichneumonoid species richness 492

Distribution related to climate and latitude 496

The nasty host hypothesis 497

Biogeography 503

Islands and their parasitoid faunas 505

Species accumulation curves 506

Altitudinal gradients 507

Estimating local species diversity 508

Ichneumonoidea as biodiversity indicators 510

Conservation 510

Effect of habitat degradation on ichneumonoid composition 511

Significance of cryptic species 511

16 Collecting and Rearing Ichneumonoidea 513

Field collecting adults 516

Pan traps 518

Sweep netting 519

Light trapping 521

Canopy fogging 521

Malaise traps 521

Rearings from wild-collected hosts 523

Rearing leaf rollers and tiers 524

Substrate rearings 524

Culturing 524

Mating in captivity 525

Mass rearing 525

Mounting specimens for taxonomic study 526

Preparing specimens from alcohol storage 526

Direct pinning 527

Side gluing 527

Card rectangles and card points 527

Secondary staging 528

Labelling 528

Preserving specimens for DNA analysis 528

Packaging and posting specimens to other workers 530

17 Epilogue 533

Phylogenetic questions 534

Host and parasitism questions 534

Physiological questions 535

Ecological questions 536

Glossary 539

References 547

Author index 633

General index 653

Host index 659

Ichneumonoid genus tribe and subfamily index 665

Ichneumonoidea species index 677

Color Plate Sections Are Inserted Between Pages Noted Below

First 13-page colour plate section (between pages 112 and 113)

Second 13-page colour plate section (between pages 224 and 225)

Third 13-page colour plate section (between pages 336 and 337)

Fourth 13-page colour plate section (between pages 448 and 449)

Donald L. J. Quicke is currently Visiting Professor at the Department of Biology, Faculty of Science, Chulalongkorn University, Thailand. He graduated from Oxford University with a degree in zoology and after doctoral and postdoctoral work on snail neurophysiology, sea anemone ecology and spider venoms, made parasitic wasps, and especially the ichneumonoid wasp family Braconidae, his main love and research interest. He held a lectureship at Sheffield University, moved to Imperial College London in 1993 and held a joint post between them and the Natural History Museum, London, until retiring in 2013 to live in Thailand. He was made Professor of Systematics in 2008. He has travelled widely collecting and studying parasitic wasps, especially in Africa. Over the past years he has described more than 560 new species and 76 new genera, including a number of fossil taxa, as well as making extensive studies of functional anatomy parasitic wasp ovipositors which are of enormous biological importance. A lot of his recent work has concerned global diversity estimation and patterns.