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THE BRACONID

AND ICHNEUMONID

PARASITOID WASPS

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THE BRACONID

AND ICHNEUMONID

PARASITOID WASPS

BIOLOGY, SYSTEMATICS,

EVOLUTION AND ECOLOGY

Donald L. J. QuickeFaculty of Science, Chulalongkorn University, Bangkok, Thailand

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Library of Congress Cataloging-in-Publication Data

Quicke, Donald L. J.The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology / by Donald L.J. Quicke.

pages cmIncludes bibliographical references and index.ISBN 978-1-118-90705-4 (cloth)

1. Parasitoids. 2. Parasitic wasps. 3. Braconidae. 4. Ichneumonidae. I. Title.QL496.12.Q55 2015595.7–dc23

2014015272

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Cover image: © Donald L. J. Quike

Set in 9/11pt Photina by Laserwords Private Limited, Chennai, India

1 2015

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To the memory of a wonderful dog called Mii,who lived at Saphan Taksin pier.

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CONTENTS

Preface, xiii

Acknowledgements, xv

1 INTRODUCTION, 1

Life history, 5Systematics, 6

PART 1 MORPHOLOGY AND BIOLOGY, 7

2 ADULT EXTERNAL MORPHOLOGY, 9

Head, 10Antennal sensilla, 12Antennal glands and tyloids, 14Palps, 15Mesosoma, 15Legs, 17Wings, wing venation and wing cells, 18Confusing and sometimes erroneously applied vein

names, 26Wing flexion lines, 27Metasoma, 29Sexual dimorphism, 30Male external genitalia, 32

3 THE OVIPOSITOR AND OVIPOSITORSHEATHS, 35

The act of oviposition, 39Functional morphology of wood-drillers, 41Ovipositor stabilisation guides and buckling force, 43Ovipositor notches and endoparasitism, 44Ovipositor steering mechanisms, 44Proposed evolutionary and related ovipositor

transitions, 48

Number, position and possible functions of ovipositorvalvilli, 50

Venom retention and delivery, 52Ovipositor secretory pores, 53Ovipositor sensilla, 54Ovipositor sheaths, 55

4 INTERNAL AND REPRODUCTIVEANATOMY, 57

Nervous system, 58Digestive tract, 58Female internal reproductive system, 59Ovaries, 59Time scale of egg maturation, 60Spermatheca, 61Common oviduct and vaginal gland, 62Venom gland and reservoir, 63Dufour’s gland, 64Cuticular hydrocarbons, 66Sex pheromones, 67Male internal reproductive system, 68Sperm ultrastructure, 69Spermatogeny index, 70

5 IMMATURE STAGES, 71

Eggs and oögenesis, 72Hydropic and anhydropic eggs, 72Embryogenesis, 73Embryonic membranes, 75Larva, 76Larval feeding and nutrition, 81Larval food consumption and dietary efficiency, 82Lipid metabolism, 82Respiration in endoparasitoids, 83Larval secretions, 83The pupal stage, 84Cocoons, 84

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viii Contents

6 IDIOBIONTS, KOINOBIONTS AND OTHERLIFE HISTORY TRAITS, 87

Parasitoidism, 88Idiobiont and koinobiont strategies, 88Generalists and specialists, 89Ecto- and endoparasitism, 90Permanent host paralysis, 91Gregarious development, 91Superparasitism, 92Larval combat and physiological suppression, 93Adaptive superparasitism, 95Multiparasitism, 96Obligate and preferential multiparasitism, 99Hyperparasitism and pseudohyperparasitism, 99Kleptoparasitism, 100Evolution of life history strategies, 100

7 SEX, COURTSHIP AND MATING, 107

Sex determination, 108Local mate competition and avoidance of inbreeding,

110Sex allocation, 110Protandry and virginity, 112Thelytoky and cytoplasmic incompatibility, 113Mate location, 117Courtship, 119Swarming and lekking, 120Mating position, 121Multiple mating and sperm competition, 121Sex-related scent glands, 123Genome size and recombination, 125Cytogenetics, 125

8 HOST LOCATION, ASSOCIATIVELEARNING AND HOST ASSESSMENT,127

Tritrophic interactions, 129Host acceptance, 130Associative learning, 130Biosensors, 134Patch use, 134

9 OVERCOMING HOST IMMUNE REACTIONAND PHYSIOLOGICAL INTERACTIONSWITH HOST, 137

Overcoming host immunity in endoparasitoids, 138

Passive evasion of encapsulation by parasitoid eggs,139

Avoiding encapsulation by physical means, 139Effect of host age and haemocyte number, 141Other host defence mechanisms, 141Venoms, 141Neurophysiological venom actions, 143Venom effects on host immune response, 144Polydnaviruses, 145Effects of polydnaviruses on hosts, 152Other reproductive viruses, 155Improving host quality, 156Host castration and similar effects, 156Teratocytes, 158Intraspecific variation in resistance to parasitoids, 159Effects on host moulting pattern, 160Parasitoid-induced changes in host behaviour, 160

10 CONVERGENT ADAPTATIONS, 163

Antennal hammers and vibrationalsounding, 164

Enlarged mandibles, 167Chisel-like mandibles, 168Concealed nectar extraction apparatus, 168Reduced number of palpal segments, 169‘Facial’ protruberances, 169Frontal depressions, 170Dorsal ridges on head or mesosoma, 170Brachyptery and aptery, 170Dorso-ventral flattening, 171Postpectal carina, 173Propodeal spines, 173‘Fossorial’ legs, 173Fore tibial spines, 174Fore tibial apical tooth, 174Expanded hind basitarsi, 174Toothed hind femur, 174Distitarsal scraper, 175Pectinate claws and claws with angular basal lobes,

175Glabrous wing patches and wing membrane

scleromes, 176Carapacisation, 177Petiolate metasomas, 177Modifications to the posterior metasomal

margin, 178Spermathecal colour, 179

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Contents ix

Compression of apical part of metasoma, 179The ‘ophionoid facies’, 179White antennal stripes and tips, 180White ovipositor sheath stripes and tips, 181Number of larval instars, 182Egg-larval parasitism, 182Disc-like larval antennae, 182Reduction of larval hypostomal spur, 183Wide and heavily sclerotised larval epistoma, 184Suspended cocoons, 184Polyembryony, 184Phytophagy and cecidogenesis, 184

PART 2 TAXONOMIC AND SYSTEMATICTREATMENT, 187

11 OVERVIEW OF ICHNEUMONOIDEA:RELATIONSHIPS AND SYSTEMATICS,189

Monophyly of Ichneumonoidea, Ichneumonidae andBraconidae, 190

Relationship of Ichneumonoidea to otherHymenoptera, 190

Fossil history and family-level phylogeny, 192Brief history of classification, 194Ancestral biology of Ichneumonoidea, 196Separating ichneumonids from braconids, 197Identifying specimens, 198

12 PHYLOGENY AND SYSTEMATICSOF THE BRACONIDAE, 201

Historical perspective, 202Morphophylogenetic hypotheses, 202Molecular phylogenetics, 204Braconid classification, 205

Eoichneumoninae†, 205Trachypetiformes, 205

Trachypetinae, 205Cyclostomes incertae sedis, 209

Protorhyssalinae et al., 209Apozyginae, 210

The aphidioid clade or ‘Gondwanan’ complex, 212Aphidiinae, 212Maxfischeriinae, 224Mesostoinae (including Canberreriini and

Hydrangeocolini), 225

The remaining cyclostomes, 229Doryctinae (including Ypsistocerini), 231Pambolinae, 236Rhysipolinae, 237Rhyssalinae, 238Rogadinae s.l., Hormiinae, Lysiterminae, 243Betylobraconinae, 243Hormiinae, 243Lysiterminae, 245Rogadinae sensu stricto, 246Alysioid subcomplex, including Braconinae,

250Alysiinae and Opiinae, 250

Alysiinae, 251General Alysiinae biology, 251Alysiini, 253Dacnusini, 255Opiinae, 256

Braconinae, 260Exothecinae, 269Gnamptodontinae (= Gnaptodontinae), 270Telengaiinae, 271

The non-cyclostomes, 271Sigalphoid complex, 271

Agathidinae, 272Sigalphinae, 275

Helconoid complex, 278Helconinae, 279Helconoid group incertae sedis, 281

Blacinae, 282Acampsohelconinae, 283Macrocentrine subcomplex, 284Macrocentrinae, 284Charmontiinae, 287Amicrocentrinae, 287Xiphozelinae, 288Homolobinae, 290Microtypinae, 292Orgilinae, 292Euphoroid complex, 294

Euphorinae, 294Cenocoeliinae, 310

The microgastroids, 311Cardiochilinae, 312Cheloninae (including Adeliini), 315Dirrhopinae, 319Ichneutinae, 320Khoikhoiinae, 322

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x Contents

Mendesellinae, 322Microgastrinae, 322Miracinae, 335

Unplaced subfamilies, 335Masoninae, 335Meteorideinae, 337

13 PHYLOGENY AND SYSTEMATICSOF THE ICHNEUMONIDAE, 341

History of ichneumonid classification, 342Henry Townes (1913–90) and his idiosyncratic

nomenclature, 344The extinct subfamilies, 344

Tanychorinae†, 344Palaeoichneumoninae†, 346Labenopimplinae†, 348Pherombinae†, 349Townesitinae†, 349

The xoridiformes, 349Xoridinae, 349

The labeniformes, 353Labeninae, 353

Groteini, 355Labenini, 355Poecilocryptini, 356

The pimpliformes, 356Acaenitinae, 356Collyriinae, 359Cylloceriinae, 360Diacritinae, 360Diplazontinae, 361Orthocentrinae (= Helictinae), 366Pimplinae, 367

Delomeristini, 369Ephialtini (= Pimplini of Townes), 369Polysphincta group, 371Pimplini, 373

Poemeniinae (= Neoxoridinae), 378Poemeniini, 378Pseudorhyssini, 378Rodrigamini, 378

Rhyssinae, 379The ichneumoniformes, 383

Adelognathinae, 383Agriotypinae, 385Alomyinae, 387Cryptinae, 388

Aptesini, 391Cryptini, 391Phygadeuontini, 393

Ichneumoninae, 394The brachycyrtiformes, 398

Brachycyrtinae, 398Claseinae (Clasinae), 398Pedunculinae, 399

The orthopelmatiformes, 400Orthopelmatinae, 400

The ophioniformes, 400Lower ophioniformes, 402

Banchinae, 402Lycorininae, 406Sisyrostolinae, 407Stilbopinae, 407Tryphoninae, 411

Middle ophioniformes, 416Ctenopelmatinae, 416Mesochorinae, 421Metopiinae, 422Oxytorinae, 424Tatogastrinae, 425Tersilochinae (including

Neorhacodinae andPhrudinae s.s.), 426

Higher ophioniformes, 430Anomaloninae, 430Campopleginae, 432Cremastinae, 438Hybrizontinae, 439Nesomesochorinae, 442Ophioninae, 442

Unplaced subfamilies, 445Eucerotinae, 445Microleptinae, 447

PART 3 ECOLOGY AND DIVERSITY, 451

14 ECOLOGY, 453

Adult diet, 454Host-feeding, 454Water, sugar and pollen feeding, 457

Fecundity, 460Voltinism and seasonality, 462Daily activity patterns, 462Diapause, 463Cold hardiness, hibernation and overwintering, 465Coloration and thermoregulation, 467Biological control, 467Effect on host food consumption, 471

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Contents xi

Artificial diets, 474Artificial hosts, 475Use of alternative hosts, 475Hyperparasitism and kleptoparasitism, 476Predation, 477Pathogens, 477Transmission of host pathogens, 479Dispersal, 480Coloration and mimetic rings, 480Palatability and odours, 481Competition, 482Apparent competition, 482Host ranges of parasitoids, 483Parasitoid guilds and food webs, 484Evolution of host ranges and speciation, 486

15 LOCAL AND GLOBAL PATTERNS INDIVERSITY, 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, 497Biogeography, 503Islands and their parasitoid faunas, 505Species accumulation curves, 506Altitudinal gradients, 507Estimating local species diversity, 508Ichneumonoidea as biodiversity indicators, 510Conservation, 510Effect of habitat degradation on ichneumonoid

composition, 511Significance of cryptic species, 511

16 COLLECTING AND REARINGICHNEUMONOIDEA, 513

Field collecting adults, 516Pan traps, 518Sweep netting, 519Light trapping, 521Canopy fogging, 521Malaise traps, 521

Rearings from wild-collected hosts, 523Rearing leaf rollers and tiers, 524Substrate rearings, 524

Culturing, 524Mating in captivity, 525

Mass rearing, 525Mounting specimens for taxonomic study, 526

Preparing specimens from alcohol storage,526

Direct pinning, 527Side gluing, 527Card rectangles and card points, 527Secondary staging, 528Labelling, 528

Preserving specimens for DNA analysis, 528Packaging and posting specimens to other workers,

530

17 EPILOGUE, 533

Phylogenetic questions, 534Host and parasitism questions, 534Physiological questions, 535Ecological questions, 536

Glossary, 539

References, 547

Author index, 633

General index, 653

Host index, 659

Ichneumonoid genus, tribe and subfamilyindex, 665

Ichneumonoidea species index, 677

COLOR PLATE SECTIONS ARE INSERTEDBETWEEN PAGES NOTED BELOW

First 12-page colour plate section (between pages 112and 113)

Second 12-page colour plate section (between pages208 and 209)

Third 12-page colour plate section (between pages336 and 337)

Fourth 16-page colour plate section (between pages432 and 433)

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PREFACE

The Ichneumonoidea is one of the largest and ecolog-ically most important groups of insects, with approxi-mately 41,000 valid described species and estimates ofseveral times that number still awaiting to be described.They are responsible for regulating the populations of alarge proportion of other insects, many of which wouldbe harmful to both the natural and agro-forestry sys-tems if their numbers were unchecked; ichneumonoidstherefore have a large economic and aesthetic impact.

My previous book on parasitoid wasps (Quicke 1997)attempted to cover the biology and ecology of all theHymenoptera with a parasitoid way of life and conse-quently did not go into any great detail about the lifehistories of particular groups. In this book, I am againcovering almost all aspects of development, biology,physiology, behaviour and ecology and additionallydevoting more space to morphology, systematicsand phylogeny, biodiversity research and the roles ofgroups in biological control. By concentrating hereon the Ichneumonoidea, the group with which I havemost research experience, I am able to present a greatdeal more information within a phylogenetic contextand also to discus what is known of the biologies ofeach of the subfamilies. Hence readers who are inter-ested in only one group can find out something aboutthem, their life histories, what research they have beeninvolved in, something about their classification andalso what there is still to be discovered about them.

The classification of the whole of the Ichneu-monoidea, along with most other insect orders, hasbeen plagued by typology, i.e. the notion that if a speciespossesses some particular character or combinationof characters, it must belong to a particular group.

Typology is a common disease of traditional taxonomyand although that is not to say that what constitutestraditional taxonomy is wrong or was necessarily a badthing, when strong new evidence comes to light, wehave to be willing to consider major changes. The newevidence that is now becoming available is provided bymolecular data and we are only just beginning to seethe implications. I want to take the opportunity in thisbook to push a molecular side of the argument becauseI think that creating phylogenies and classificationsbased only on morphological characters is particularlylikely to be flawed. Of course, I do not believe thatmolecules are incapable of being misleading, they cancertainly be that, but in general, and not necessarilyunder any very particular circumstances, molecularevidence is likely to provide our best insight into phy-logeny. In recent years, it has become apparent thatmany morphological characteristics associated withbasic life history features, specifically whether waspsare ecto- or endoparasitic, can be grossly misleading interms of the phylogeny they suggest.

One of the key issues with understanding the evolu-tionary traits in the superfamily is that, despite a vastliterature, most work on aspects of physiology or devel-opment is very patchily distributed and often in waysinadequate to control for phylogeny. Thus, what mightappear to be an interesting biological association couldjust represent a single evolutionary origin, since criticaltaxa have not been studied.

Recent advances in taxonomy and systematics, theconcomitant publication of better identification worksand the realisation that many earlier host records(perhaps 50% or more) are wrong, and sometimes

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xiv Preface

badly so, means that we are becoming better able toaddress some of the gaps and discover new, interest-ing evolutionary links. Progress is likely to continueat an even greater pace with better illustrated andmore accessible web-based tools. In this book, I hopeto draw attention to areas where particular types ofresearch might be most effectively employed, includinggroups that need more work on host associations or

general biology, and to follow up intriguing hints frompreliminary data on other groups. In particular, newphylogenetic hypotheses have highlighted groups forwhich either additional biological information or, innumerous cases, any biological information at allmight be particularly revealing for our understandingof the evolution of the group.

Donald L. J. QuickeBangkok, Thailand

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ACKNOWLEDGEMENTS

Over the many years that I have been interested inparasitic wasps in general and ichneumonoids inparticular, I have benefited from discussions with avery large number of people and to all of those I offermy thanks. However, I must make a few mentions inparticular and hope that I have not missed anyone outwho will be too upset by that. The following people,representing a number of fields from taxonomy andsystematics, behaviour, functional morphology andecology have been of particularly great help to me andhave all, in various ways, contributed to the ideas inand the development of this book: Andy Austin, Sergey

Belokobylskij, Ferdinando Bin, Gavin Broad, MikeFitton, Charles Godfray, Vladimir Gokhman, SerainaKlopfstein, Nina Laurenne, Victoria Pook, AlexandrP. Rasnitsyn, A. M. [Guida] Santos, Mike Sharkey, MarkShaw, Scott Shaw, Kees van Achterberg, Bob Wharton,Jim Whitfield and Alejandro Zaldivar-Riverón. I wouldalso like to thank the many people who have kindlyallowed me to use their published or unpublished pho-tographs and micrographs: as they say, a picture speaksa thousand words. All graphs were produced using thestatistical computing language R (R Development CoreTeam 2009).

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Chapter 1

INTRODUCTION

The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology, First Edition. Donald L. J. Quicke.© 2015 John Wiley & Sons, Ltd. Published 2015 by John Wiley & Sons, Ltd.

1

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A lthough most people are blissfully unaware ofthem, the ichneumonoid wasps are one of themost diverse groups of insects, and in terms

of their ecological role they are probably of enormousimportance. No-one really has a good idea about howdiverse they are and estimates vary widely. The totalnumber of valid species described to date, 18,000braconids and 23,000 ichneumonids1, is certainly agreat underestimate, but by how much is still any-one’s guess. Many works cite estimates of 40,000 and60,000, based upon expert opinion (Townes 1969,Gauld & Bolton 1988). Similar values have also beenobtained by various objective estimation measures, butit seems likely that these too are underestimates, andnarrowing the numbers down is not going to be easyfor the reasons explained in Chapter 15.

Unfortunately, neither family has attracted a lot ofattention from amateur entomologists, which seemsto be a prerequisite for a good knowledge of a group’staxonomy, distribution and biology. This may be partlybecause many of the species are rather small and oftendull coloured, although this does not seem to havedeterred generations of amateur coleopterists. Proba-bly the most important factor has been the dearth, untilfairly recently, of reliable and accessible identificationguides to the major groups (subfamilies), confoundedby the fact that the subfamily-level classification is onlynow becoming fairly stable, largely as a result of muchnew molecular work. Problems have been compoundedbecause numerous names were mis-applied by earlyworkers and, as these errors were slowly discoveredand corrected, many groups accumulated a historicalbacklog of alternative names. In many fields of science,the really old literature seldom has to be cited, but inzoology, a great deal of excellent work on anatomy andbiology was carried out 50 to 100 or so years ago. Asthis may be the only detailed work on a given group,it is still relevant today and the reader therefore has todeal with the sometimes confusing or even misleadingnomenclature.

Difficulties in the correct identification of specimens,and publications dealing with incorrectly identifiedspecimens, have also been a major stumbling blocks.To quote Perkins (1959), ‘It is perhaps, not surprisingthat keys to subfamilies are very imperfect, as excep-tions can be found to almost all characters that havebeen used in defining any subfamily, even in the limitedBritish fauna’. Partly because of overall improvingtaxonomic and systematic understanding, publishedresearch on both families is growing, that dealing

with the braconids slightly more quickly than thatfor the ichneumonids (Fig. 1.1). There may be severalreasons for this growth, not the least of which is thatmost researchers are now under great pressure topublish their findings quickly in bite-sized chunks andin high-impact journals, rather than presenting single,large tomes representing the results of many years oftheir work. The difference in the rate of publicationbetween the families could well be due to the ease ofidentification – recognising subfamilies is generallyeasier for braconids and knowing what subfamily youare dealing with is the essential first step towards aproper identification.

The Ichneumonidae and Braconidae are each suchlarge groups that few people since the early 20th cen-tury have attempted to work seriously on the wholeof either one of them, so it is hardly surprising that inrecent years almost no-one has attempted to tacklethem both. This, of course, means that the similaritiesand differences between them may have been less wellconsidered than they should have been. Superficially, itmight seem that these two families essentially parallelone another, they are sister groups and they broadlyoccupy the same range of niches – they predomi-nantly parasitise exposed and concealed moth andbeetle larvae with a few incursions into attacking flyand Hymenoptera larvae, rarer ones into other insectgroups and a few other ways of life such as spider eggpredation and even a few instances of true phytophagy.However, things may not be as simple as they seem,because despite some remarkable parallels, they alsoshow strong group differences in precisely what they doand in the types of adaptations they typically employ.

It should come as no surprise therefore, that ichneu-monids and braconids do not ‘behave’ in the same wayin so many aspects of their biology and morphology. Ifthey did, it seems likely that one would have driven theother to extinction or pushed them a long way in thatdirection. That both groups are highly speciose seemsvery likely to indicate that they do not compete in aprecise and consistent way, although many individualspecies no doubt do. Hence there are various sorts ofadaptations that appear to evolve frequently in onefamily but not or only rarely in the other. For example,numerous braconids have evolved carapace-like meta-somas where the basal 3 (or sometimes 4) metasomalterga are enlarged, frequently fused, or at least moreor less immovably joined and conceal all more pos-terior ones (see Chapter 10, section Carapacisation).Only a very few ichneumonid groups have members

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Introduction 3

1970 1975 1980 1985 1990 1995 2000 2005 2010

Web of Knowledge Publications

020

4060

8010

012

0

Braconidae

Ichneumonidae

Fig. 1.1 Numbers of papers on Braconidae and Ichneumonidae published each year in Science Citation Index (SCI) journals from1970 to 2012.

with carapaces and the numbers of species involvedis very small. Is this associated with the difference inarticulation between the second and third metaso-mal terga, which is one of the diagnostic features forseparating the two families? Endoparasitoid larvaebelonging to several different braconid lineages haveapparently independently evolved an everted rectumforming a structure called an anal vesicle (see Fig.5.1) that serves a variety of physiological roles, butthis adaptation, as far as is known, has only evolvedin two genera within the Ichneumonidae. Similarly,very elongate mouthparts (although variously involv-ing the glossa, malar region or maxillary palps) haveevolved on numerous independent occasions withinthose Braconidae dwelling in relatively arid habitats(see Chapter 10, section Concealed nectar extractionapparatus), but the number of such occurrences inthe Ichneumonidae is small (e.g. Rhynchobanchus:Banchinae). These modified mouthparts, collectively

referred to as a concealed nectar extraction apparatus,are an adaptation to obtain nectar from plants such asAsteraceae or Dipsaciaceae, which in turn are adaptedto prevent their nectar from drying up in places wherewater is in short supply. In this case, it may be becausebraconids tend to comprise a relatively larger propor-tion of species in such habitats, but the data are notreally available to test this.

Ichneumonids collectively utilise a somewhat diff-erent spectrum of hosts than braconids. They includemany more taxa that are parasitoids of otherHymenoptera, including both endo- and ectopara-sitism, in addition to acting as pseudohyperparasitoidsof other ichneumonoids (see Fig. 13.1; cf. Fig. 12.2),and endoparasitism including developing as truehyperparasitoids within a host, as well as some beingpredators within aculeate wasp and bee nests. In theBraconidae, members of two tribes within the Euphori-nae are endoparasitoids on adult Hymenoptera, a few

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4 Donald L. J. Quicke

ectoparasitoids attack leaf-mining sawflies and onlya few members of the Ichneutinae are endoparasiticwithin sawfly larvae, and Gauld (1988a) plausiblysuggested that these made the transition to sawflyhosts from ancestors that were endoparasitoids ofleaf-mining Lepidoptera. Further, no braconids apartfrom the rather special case of a few euphorinesparasitising adult ichneumonoids (see Chapter 12,section Syntretini), no braconids are hyperparasitoidsor even pseudohyperparasitoids. Two subfamilieswithin Ichneumonidae, involving several evolutionarytransitions, have become associated with spiders eitheras egg predators or as parasitoids of juvenile and adultindividuals. All of these seem to be connected by theiruse of silk, or volatile or non-volatile compounds asso-ciated with silk, in the host location – because of itsnon-solubility, silk proteins themselves seem an incred-ibly unlikely source of host-finding cues. Nevertheless,at least some braconids do utilise cues from host silktrails (Ha et al. 2006), but it does not seem to havebecome an important part of their behavioural reper-toire. Perhaps partly associated with this and theplaces where silk-cocooned hosts occur, ichneumonidsappear to have evolved vibrational sounding (a sortof echolocation) as a host location tool on multipleoccasions (and lost it on many also), whereas thereis no evidence for this host location mode in the Bra-conidae (see Chapter 10, section Antennal hammers andvibrational sounding).

Another important question that we ought to con-sider is why the ichneumonoids and chalcidoids havenot out-competed one another in one direction oranother. Some niches occupied by chalcidoids are notavailable to ichneumonids; for example, egg parasitism,which necessitates body sizes smaller than or at leastat the very bottom range of that which ichneumonoids(e.g. Miracinae or Cheloninae–Adeliini) have thusfar achieved. Ichneumonids described to date are, ingeneral, larger bodied than braconids (see Fig. 15.6),and this may correlate with some differences in hostutilisation, since only braconids can attack small insecthosts such as psocids, aphids, plant bugs and tinybeetles (Capek 1970).

It seems to me a very great shame that manytraditional areas of study, such as those on comparativeembryology and detailed descriptions of natural his-tory, have suffered a serious decline in recent years andeffectively have ceased in most Western universities.For a long time they have been largely restricted to

workers in parts of the world, such as the former Sovietblock countries, where access to more trendy modernmethods and thought were perhaps restricted. Thismeans that many important descriptions of biologycome from before World War II and sometimes beforeWorld War I. And although many of these are of highquality, they often deal with species serendipitously, aswell as under unfamiliar names that have been lost insynonymy and therefore may require some detectivework. However, these are the only sources of detailedbiology for some groups.

A great deal of what we know about the biologiesof various groups comes from efforts to use them forbiological control (e.g. Wharton 1984). As a conse-quence, we know far more about some subfamiliesthan we do about others and obviously we know moreabout taxa that are readily easily brought into culture,which means that the host nearly always has to beeasy to culture too, or at least easy to find and collect.There are a surprisingly large number of subfamilies forwhich we know absolutely nothing about the biology,not even the order of hosts that they attack or whetherthey are ecto- or endoparasitoids. Some of them includefairly common and frequently collected species.

Now that we have the powerful tool that modernphylogenetics provides, we are in desperate need ofmore such studies to help test hypotheses about theadaptive natures of particular character states within acomparative framework. Although it is possible in somecases to go out and obtain the necessary taxa, there is ageneral mismatch of people skills. Many excellent phys-iologists and molecular geneticists carry out their workon taxa of real or potential economic importance and aconsiderable amount of their research receives fundingbecause of this. By their nature, the hosts of potentialbiocontrol insects are generally easy to obtain andculture, although admittedly wood-borers may posemore of a logistic issue than say grass-feeding aphidsor cotton-feeding moths. The parasitoids that aretherefore best investigated are those which attack thesehosts with the consequence that much work has beencarried out on a relatively small subset of taxa, aphidi-ine and microgastrine braconids and campoplegineichneumonids being prime examples. Many of thelaboratory researchers would love to obtain some otherparasitoid taxa into culture to study, but this involvessetting up host cultures, obtaining the parasitoids andworking out rearing techniques, all probably withless funding available. Although there are numerous

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Introduction 5

exceptions, many laboratory-based experimentalistsoften do not have the field entomological or naturalhistory backgrounds to facilitate the finding of some ofthe other taxa.

The other side of the skills mismatch is that there are,at least in many ‘Western’ and East Asian countries,excellent natural historians who are good at and enjoygoing into the field in search of insects and rearingthem, but they often do not necessarily know whatmore detailed pieces of information about an insect’sbiology are missing. Added to this is the problem thatmany taxonomically interesting taxa, which mightwell have particularly interesting biologies and asso-ciated physiology, biochemistry, etc., are simply rare,very local in distribution or attack hosts that are verydifficult to obtain or bring into culture. There aremultiple examples of all of these.

One of the aspects that really needs to be revisited, assoon as sufficient independent molecular phylogeniesbecome available, is all the hypothesised evolutionarytransitions and trends that have been based on purelymorphological phylogenetic estimates. It is surprisinghow often the networks obtained from morphologicaland molecular analyses are similar, which is good,but the rooting is extremely different. Such differentresults may reflect either that the outgroups (if used)are too distant to provide much meaningful evidenceof true ancestry or even that workers had a soft spot foran elegant biological story. It was certainly commonpractice in early cladistics studies to ignore charactersthat the worker ‘knew’ to be homoplastic. Currentlyavailable molecular data have provided a considerablenumber of new insights and reasonably well-supportedbig pictures for both families, but there are still manyareas of the evolutionary tree where there is a realshortage of resolution and several taxa whose place-ments are far from certain. Quite possibly much ofthe radiation at subfamily level occurred subsequentto the Cretaceous period – there are few Cretaceousfossils that can be assigned to modern subfamilies withconfidence, especially within the Ichneumonidae, yetthe Eocene (53 to 33.7 Mya) fossil record containsmany species that are fairly certainly recognisable tomodern subfamilies and sometimes possibly to a genus.

The large size of both families mean that thereare inevitably many scientific names which may seemdaunting or confusing to beginners. Even when dealingwith the relatively small number of frequently culturedspecies there are still many of them to get to grips with.

I think it is certain that the nomenclatural aspect ofwork on this group has been off-putting, not aidedby the fact that some workers have employed alter-native systems [see Chapter 13, section Henry Townes(1913–90) and his idiosyncratic nomenclature, althoughit is not just Townes’ work where confusion can arise].

It is always difficult in a book such as this to decidewhether to start with morphology, biology or taxon-omy. I have opted for the first, but in order to be able tomake some sense of the features, it is necessary to referto some aspects of each of the others in this section.I have therefore included below very brief outlines ofsome of the important biological concepts and system-atics to facilitate understanding. I have also chosen toarrange things in rather a small number of chapters,each consequently with a fairly broad remit. Never-theless, some topics have had to be shoe-horned in atplaces where they might seem slightly incongruous.It also seemed logical to include a few physiologicalaspects within more broadly morphological sectionssince the understanding of the morphology is some-times intimately linked with other processes. As thiswill be used mainly as a reference book, some facts arerepeated in two or more places. I hope that in the end,the structure more or less makes sense.

LIFE HISTORY

There are two important terms to be learnt here. Thefairly obvious difference between parasitoids which(generally) lay their eggs within a host and whoselarvae develop internally surrounded by wet host tis-sues, i.e. endoparasitoids, and those that lay eggsexternally and whose larvae complete feeding from theoutside, surrounded by air, i.e. endoparasitoids.

A second important distinction, – indeed, in manyrespects possibly more important – is between para-sitoids whose hosts do not develop further after beingparasitised, referred to as idiobionts, and those par-asitoids whose hosts continue feeding and usuallymoulting after the parasitoid has oviposited (usually)in them, which are called koinobionts.

Ecto- and endoparasitism and idiobiont/koinobiontstrategies both explain a great deal about other life his-tory features and they are strongly correlated, althoughasymmetrically. Most koinobionts are endoparasitoids,but idiobionts can be either ecto- or endoparasitic, butendoparasitic idiobionts are almost entirely, within

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6 Donald L. J. Quicke

the Ichneumonoidea, parasitoids of host pupae andcomplete their development therein.

SYSTEMATICS

Necessarily, many subfamilies and genera have to bementioned, and typically members of the same subfam-ily show very similar biologies and members of generaeven more so, although there are some exceptions.Both Braconidae and Ichneumonidae include a largeclade whose members are all koinobionts and, withthe exception of the Tryphoninae within the Ichneu-monidae, endoparasitoids. In both families, the sistergroup to the entirely koinobiont clade is a predomi-nantly idiobiont ectoparasitoid lineage with numerousindependent transitions to endoparasitism and koino-biosis. In the Braconidae, members of this lineageare called cyclostomes (see Fig. 2.1b) in reference totheir mouthpart morphology, although some membersof the cyclostome lineage have secondarily becomenon-cyclostomes. When I use the term ‘cyclostome’

in this book, unless specified otherwise, I am referringto the lineage rather than the condition. There is noequivalent term within the Ichneumonidae, althoughthe biologically equivalent lineage of (predominantly)koinobiont endoparasitoids is dominated by a groupinformally referred to as the ophioniformes. The end-ing ‘-formes’ is used throughout to indicate groupingsof subfamilies that are believed to be monophyletic andusually have relatively consistent biologies.

Many readers will not know where a given taxonbelongs, either within the above larger framework or towhat subfamily it belongs. I have therefore very largelyspecified this as I go along, despite its clumsiness,because in that way the reader might most readilysearch for further information on other members ofgroup of interest.

ENDNOTE

1. Over 60,000 species names have been published so some19,000 are synonyms.

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Part I

Morphology and Biology

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Chapter 2

ADULT EXTERNAL

MORPHOLOGY

The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology, First Edition. Donald L. J. Quicke.© 2015 John Wiley & Sons, Ltd. Published 2015 by John Wiley & Sons, Ltd.

9

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T he pupal and adult bodies of apocritan (i.e.wasp-waisted taxa) Hymenoptera are dividedinto three tagmata, head, mesosoma and meta-

soma. The mesosoma comprises the three thoracicsegments in addition to the first abdominal segment, inother words, the narrow waist that defines the apocritais located between the first and second abdominalsegments. The first abdominal segment at the posteriorof the mesosoma is called the propodeum. The reasonfor the waist being there rather than between thethorax and abdomen is that in flying species, one ofthe large thoracic muscles associated with flight isattached to a posteriorly directed internal phragma ofthe metathorax. Readers should be aware that in the19th century, this was not always recognised and sosome works refer to the propodeum erroneously as themetathorax, which can be confusing, especially withdescriptions of colour patterns.

Karlsson and Ronquist (2012) provide an excellentguide to the skeletal anatomy of two exemplar bra-conids, both members of the Opiinae, which deals withboth external and internal chitinous structures. Thiswork updates and, because of the use of scanning elec-tron microscopy (SEM), is in greater detail than Alam’sstudies of the braconine, Stenobracon deesae (Alam,1954, 1955). It serves as a basis for the terminologyused here and also is almost entirely applicable to theIchneumonidae.

HEAD

The head bears three pairs of multi-articulateappendages and also a pair of mandibles, eyes andthree ocelli. Males tend to have larger eyes thanfemales and the eyes and ocelli of crepuscular andnocturnal taxa, such as those showing the ophionoidfacies, are usually relatively larger than those of relateddiurnal species. A few taxa that live largely concealedin termite nests can have very reduced eyes.

In the Ichneumonoidea, the head is virtually alwaysorthognathous, with the line between the ocelli andmandibles being more or less perpendicular to thelong axis of the body. The main exception is the defi-nitely prognathous Masoninae (see Fig. 12.73). Thetop of the head comprises, from posterior to anterior,the occiput [which is often margined anteriorly witha carina (for occipital carina, see Figs 12.12e and12.26)], the vertex, which is the dorsal part behindand somewhat lateral to the ocellar triangle, and the

frons (that part between the ocelli and the antennalsockets). Presence, partial absence or complete absenceof the occipital carina are often important charac-ters in braconid identification. The three ocelli areusually on a distinctly differentiated, roughly triangu-lar raised zone referred to as the stemmaticum. Thefront of the head (Fig. 2.1) from antennal sockets tothe mandible insertion is comprised of the face and,below this, the clypeus, the two regions usually beingclearly demarked by a carina or groove, although ina few groups (notably campoplegine and metopiineichneumonids) they are effectively completely unitedin a uniform shield. At the border between clypeusand face are a pair of pits [anterior tentorial pits (Fig.2.1a)], that are the external manifestation of a pairof internal cuticular protuberances (tentorial arms)which, together with posterior equivalents, form aninternal supporting skeleton for the brain and phar-ynx. One of the most important features in braconidsystematics involves the clypeus. In the majority ofspecies in the cyclostome lineage, the lower part of theclypeus (called the hypoclypeus) is reflexed posteriorlyand usually forms a dorsally convex arch exposing thelabrum, which is, again usually, convex and glabrous(Fig. 2.1b). In the non-cyclostome lineage of braconidsand nearly all ichneumonids, the labrum is hiddenand, if exposed, clearly setose. Its partial exposure isalso an important feature in the Ichneumonidae. Thedorsal, clypeal margin of the hypoclypeal depressionin cyclostome braconids usually bears a pair of clus-ters of small bristles, which are presumably sensillae(hypoclypeal hair brushes). The lower anterior clypealmargin nearly always bears a transverse row of strongsetae and in the Ichneumonidae, in particular, theirdistribution and regularity of spacing are often animportant taxonomic characters.

Between the ventral part of the compound eye andthe base of the mandible articulation is a region calledthe malar space. Various measurements such as therelative lengths and widths of these parts are oftenimportant in species recognition, although there hasnot been complete consistency in how various mea-sures are taken and care should be taken to understandwhat a particular author means by their use of themeasurements or ratios they employ.

The top of the head comprises the frons, locatedbetween the three ocelli and the antennal sockets,and the occiput, that part which lies behind the ocelli.The back of the head is often completely or partiallymargined by a carina, the occipital carina, and this

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Adult external morphology 11

Scapus

Torulus (antennal socket)

Face

Dorsal margin of clypeus(Epistomal groove)

Clypeus

Hypoclypeus recessed belowdorsal part of clypeus

LabrumMandibleGlossa

Labial palp

Maxillary palp

Temple

(a)

(b)

Face

Anterior tentorial pit

Clypeus

Malar suture

Mandible

Galea

Fig. 2.1 Parts of head in frontal aspect. (a) Phanerotoma behriae (Cheloninae), a non-cyclostome braconid showing lack ofimpressed space between lower margin of clypeus and mandibles. (Source: Reproduced by permission of Rebecca Kittel.) (b)Acrisis sp. (Rhyssalinae), a cyclostome braconid showing hypoclypeal depression and concave, glabrous labrum.

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12 Donald L. J. Quicke

is often of considerable taxonomic importance. Theregion where the head attaches to the prothorax(occipital foramen) is margined by the post-occipitalcarina, and the hypostomal carina runs from there toclose to the base of the mandibles, sometimes fusingpart of the way with the lowest part of the occipitalcarina. Details of the arrangement and developmentof the occipital and the hypostomal carinae have beensurveyed in the Braconidae by Tobias and Potapova(1982).

Ichneumonoid mandibles are typically bidentate,which is a synapomorphy for the superfamily, but anumber of taxa show either the secondary develop-ment of one or more extra teeth, most notably in theAlysiinae and Diplazontinae, or sometimes the reduc-tion to one so they are effectively unidentate. Little isknown about the distribution or function of mandibu-lar glands, but those of rhyssine ichneumonids havebeen described by Davies and Madden (1985) andappear to be associated with release of volatiles thatattract males (both by females and by males), andShaumar (1966) illustrated the mandibular gland inhis detailed study of the anatomy of Pimpla rufipes (asinstigator).

The antennae of ichneumonoids comprise two basalsegments, a rather large and usually bulbous sca-pus, followed immediately by a smaller pedicellus,although in some orthocentrines and hormiines thetwo structures are approximately similar in size. Thefollowing segments, which are almost always filiformwith many segments, are referred to as the flagellum.No ichneumonoids have strongly clubbed antennaebut they are slightly apically expanded in a few generasuch as Brachycyrtus (Brachycyrtinae) (see Fig. 13.32)and Hellwigia (Ophioninae), and in a few rare instancesthe scapus and basal flagellar segments may be highlymodified and raptorial (e.g. the euphorine braconidStreblocera; see Fig. 12.57).

The number of antennal segments is variable andthere are typically more in larger bodied wasps. Thelargest braconines and doryctines may have more than100 flagellomeres, although more typical numbersare between 20 and 60. A few genera have reducednumbers of antennal segments [down to about 12–14flagellar segments in the ichneumonids Adelognathus(Adelognathinae) and Pygmaeolus (Tersilochinae, for-merly Phrudinae) or 12 in miracine braconids and9–12 in cedriine braconids (Pambolinae)]. Nearly allcommonly encountered taxa have 15 or more flag-ellomeres. In the Microgastrinae, these often have

two rings of placoid sensilla with a weak constrictionbetween them, which can make them look superficiallyas if they have more segments than they do. Occasion-ally, the number of flagellar segments is fixed withina larger grouping, as in the braconid Microgastrinae(16 flagellomeres, with one exception) and Miracinae(12 flagellomeres in both sexes).

ANTENNAL SENSILLA

Numerous morphological studies, predominantlyusing SEM, have been carried out on the sensilla ofichneumonoids, predominantly on members of theBraconidae. Although all antennae have a variety ofsensilla types, very little progress has been made interms of identifying the individual roles of the differenttypes. They fall into several morpho-categories, varioustypes of setiform sensilla called sensilla trichodea, vari-ous types of sensilla basiconica, short sensilla coeloconicaand elongate multiporous plate sensilla also calledsensilla placodea or placode sensilla, the last being by farthe most conspicuous and best studied.

The sensilla placodea often give the flagellomeres alongitudinally striated appearance and are sometimesreferred to as rhinaria in reference to their likely olfac-tory function. They may occupy nearly the entirelength of the flagellar segment or form two rings, onebasally and one apically (notably in microgastrinebraconids) or they may be arranged more irregularly.The sensilla placodea of ichneumonoids differ fromthose of chalcidoids in that they have the neural orificeentering it at its midlength rather than at the basal endand the tip of the sensillum is not free and protruding.The opening typically occupies about 25–60% of thelength of the entire sensillum, but in most cyclostomebraconids it is much smaller, only 15–20% (Barlin& Vinson 1981, Basibuyuk & Quicke 1999a). In theBraconidae, aphidiines (Borden et al. 1978b), a fewMesostoinae and the euphorine genus Cosmophoruslack the internal sensilla floor more or less completelyand therefore the neural opening extends the entirelength of the sensillum. What the significance is ofthese variations in size of the hole in the basal plateis can only be speculated upon. Maybe it is somehowrelated to the number of separate neurones innervat-ing the placode and thus their relative discriminatoryability?

The ultrastructure of placode sensilla has beendescribed in detail for the pimpline ichneumonids