“Sy. ISSN 0968-0454 eS wa | Bulletin of _ The Natural History Museum Entomology Series S)2 THE NATURAL HISTORY MUSEUM VOLUME 63 NUMBER 1 23 JUNE 1994 The Bulletin of The Natural History Museum (formerly: Bulletin of the British Museum (Natural History) ), instituted in 1949, is issued in four scientific series, Botany, Entomology, Geology (incorporating Mineralogy) and Zoology. The Entomology Series is produced under the editorship of the Keeper of Entomology: Dr R.P. Lane Editor of Bulletin: Dr P.C. Barnard Papers in the Bulletin are primarily the results of research carried out on the unique and ever-growing collections of the Museum, both by the scientific staff and by specialists from elsewhere who make use of the Museum’s resources. Many of the papers are works of reference that will remain indispensable for years to come. All papers submitted for publication are subjected to external peer review before acceptance. 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(Ent.) 63(1):1-136 Issued 23 June 1994 A revision of the Indo-Pacific species of Ooencyrtus (Hymenoptera: Encyrtidae), parasitoids of the immature stages of economically important insect species (mainly Hemiptera and Lepidoptera) D.-W. HUANG & J.S. NOYES* Institute of Zoology, Chinese Academy of Sciences, Beijing, P.R. China *Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD CONTENTS i) 100) OC) COMB MOSER ER CE Eer CREEL LE cher Coa Oc, Cone Ce SCR Em Se Pee Cene tte cok eaaaray Seen! MIEN CXL GIN OIA tates cee cin ag Elo See ose adn Vos v Spe epinaebiwinc nua ed Sem sesiadd aus vp ss aGacs Spas ac 2 ESIOIOB VOLO OEIE VTS, SOD: weet snag ani had Sooo Oeiscinn sna Sethe nisina nds ac Aaine oan sepia nacde ts siodsion 2 SVNOPSIS/OLMOSTSIOL INGO-PACIIC SPECIES 5.0.0 cansacninienaen sige ce ducodeh ustarsgescdeecasen sancti 4 Use of Ooenayrius im biologicalcontrol )..... «ape. sic hove bie RES « cZNe mMmRichile « tuck to's duos tau bie 1 SVSLERI ATIC SECHOR Ms. saaqadae teas stepece dougie oven deebaeap «Rein cbphaeneierinemeiaitummmarrones «teewee 8 GOCHGY FS PASM GAG atee, cts > ove oMeev ae. Stckedh scene. Sede. (aaa anes cas 10 PRUDTSVIATIONS USCOMENIEKE S.occcncgaccceqdenecnt ance cciadncacinaapetegedecccacerescoseecesqseives 11 Key to’Orientall species of Ooencyrius (females)? 22-5... .tncs.ccsdenaee-sesceet-seseasene. 11 IRE VIC WIOL SPICOIGS o onn ccs cr caattla ar ever o's a0 canieinseatlgee a aaa ts oditiois Sansee uatata aa deck aus ates 16 FE XCUIGECSPECIES as. .enasccessantcciecseesses series ciacaiaabbtuinelaae’s «lest ilepasabenibansptcit eeuceaniats 83 IRELETONEES Sra stem scene tenes testis onerts sees nanehbLiaasechits ode « teeweitae aa setiepiatenach- ee 84 ELS try ALORA Sena ate settee ice eee rere wins vc sede deete sow Seats ammctincis Joes osebesth «Bais vam 88 MNGEX toSClEN te NAMES: Mage. see ach. dosece acu caepaadaceceeworeteimtevsateadewardaccvteccasaeea 134 Synopsis. This revision treats 70 species of the genus Ooencyrtus found in the Indo-Pacific region, including south China, but excluding Australia and New Zealand. One new generic and 7 new specific synonymies are proposed, 49 species are described as new ‘and 11 lectotypes are designated. Each species is characterized by a diagnosis and/or full species description, its known distribution and hosts are reviewed, and a key is provided to the females. * Correspondence to Dr J.S. Noyes © The Natural History Museum, 1994 2 INTRODUCTION The genus Ooencyrtus is of particular interest because it is widespread and species-rich in all geographic regions and its species parasitise diverse hosts and host stages. Many species para- sitise immature stages of pest species and thus have potential value as biological control agents. Some species also act as minor pests by parasitis- ing eggs of butterflies being reared for commer- cial purposes in Malaysia and Thailand. This interest is reflected by the relatively large amount of material of the genus that is received by the identification services of the The Natural History Museum and International Institute of Entomology from the Indo-Pacific region. Unfortunately, identification is difficult because the taxonomy of the genus in this part of the world is inadequate. This revision was under- taken as a first step towards improving this situation and it is perhaps not surprising that of the 70 species treated here, more than two-thirds are described as new. BIOLOGY OF OOENCYRTUS Host range The majority of species are parasitoids of the eggs of Hemiptera or Lepidoptera, but species are known that attack the prepupae of Lepi- doptera, braconid primary parasitoids of cater- pillars (Lepidoptera), immature stages of Dryinidae attacking auchenorrhynchous Homoptera, nymphal stages of Aphididae (Homoptera), immature stages of Syrphidae (Diptera) or Coccinellidae (Coleoptera) feeding on aphids, or the pupae of Chloropidae (Diptera). Host specificity The degree of host specificity is not known with any certainty. Some species appear to act only as solitary parasitoids of lepidopterous eggs laid in batches, such as pinicolus which parasitises the eggs of Lymantriidae and Lasiocampidae (see Trjapitzin, 1989). Other species may be parasi- toids of the eggs of Heteroptera or Lepidoptera which are laid in batches, e.g. pityocampae which will parasitize the eggs of Lasiocampidae, Not- odontidae (Lepidoptera) as well as Coreidae and Pentatomidae (Hemiptera), although the same species has also been recorded as a parasitoid of D.-W.HUANG AND J.S. NOYES the solitary eggs of Sphingidae (Battisti et al., 1988). At least one species is known to be a gregarious parasitoid of the solitary eggs of but- terflies, e.g. papilionis (see p. 79). Two species are known to attack different stages of hosts in different orders. Ooencyrtus kuvanae, has been recorded both as a primary solitary parasitoid of the eggs of gypsy moth (Lymantria dispar) and as a gregarious hyperparasitoid of the prepupal and pupal stages of the moth’s braconid primary parasitoid. Muesebeck & Dohanian (1927) found that female kuvanae from field-collected gypsy moth eggs would oviposit into the immature stages of Apanteles melanoscelus within their cocoons after they had emerged from the gypsy moth caterpillar. Up to 17 individuals subse- quently issuing from a single braconid host. The same species of Ooencyrtus has also been recorded as a primary parasitoid of Anastatus bifasciatus Fonscolombe in gypsy moth eggs (Howard & Fiske, 1911), although Crossman (1925) stated that he knew of only one such case in 14 years of working with these species. Ooen- cyrtus submetallicus (Howard) is best known as a primary parasitoid of the heteropterous eggs, but it has also been recorded as a parasitoid of the pupae of a chloropid dipteran (Legner & Bay, 1965a,b). Ovary development Adult females emerge from the host with unde- veloped ovaries and the preoviposition period may vary from 1.5 to nearly four days depending on temperature (Tracy & Nechols, 1988). Mating Mating has been described in detail only for kuvanae (Brown, 1984). Females may mate sev- eral times, but if they participate in a post-mating ritual they will mate only once. The post-mating ritual involves the pair facing each other and the male touching the female with his antennae, fore legs and head. The female touches the male with her mouthparts at this time. Newly emerged, mating females may be swarmed over by males if populations are large. Mating males appear to clean the female with their mouthparts, they may also try to mate with a female before her wings are fully expanded. Host finding and oviposition Evidence suggests that, in at least two species (fecundus and pityocampae), female adult parasi- toids are attracted to chemicals or odours pro- REVISION OF INDO-PACIFIC SPECIES OF OOENCYRTUS 3 duced by the adult female host (Laraichi & Voegelé, 1975; Battisti, 1989). This may be the result of the parasitoid being conditioned by encountering suitable freshly laid eggs after the mass emergence of a suitable host species (Bat- tisti, 1989). Oviposition may take some time depending upon the experience of the parasitoid. In kuvanae experienced females may take only five minutes to deposit an egg after the initial encounter whilst inexperienced females may take nearly twice as long (Lee & Lee, 1989), whilst in gregarious species oviposition may take nearly an hour per single host, e.g. johnsoni (Maple, 1937). Host feeding, by the adult parasitoid, has been observed in at least two species (Kuvanae, Lee & Lee, 1989; johnsoni, Maple, 1937) and is almost certainly common throughout the genus. Fecundity The species of host egg can influence fecundity (Laraichi, 1978a). Host density does not affect fecundity but lower host density increases the rate of superparasitism in solitary parasitoids (Laraichi, 1978b). The maximum overall fecun- dity may be as high as 200 (Crossman, 1925). In species that parasitise egg clusters the number of eggs deposited by the parasitoid will be limited to the number of mature eggs present in the ova- ries, in nezarae this averages about 17 (Takasu & Hirose, 1991). In kuvanae this normally results in a lower percentage parasitism of larger egg masses resulting from egg limitation (Weseloh, 1972; Williams ef al., 1990). Percentage parasit- ism in kuvanae may be as high as 80%, but is generally around 10-40%. The substrate on which the host eggs are laid may affect rate of parasitism. In kKuvanae, the eggs of its host on red maple (smooth bark) have a higher rate of para- sitism than those on oak (rough bark) (Bellinger et al., 1988). Immature stages After oviposition the egg stalk remains protrud- ing through the chorion of the host egg. The larva remains attached to its egg shell for the first three instars and is metapneustic (Maple, 1937), being able to utilise atmospheric air directly through the protruding part of the egg (Maple, 1937). The number of larval instars recorded varies from three (Gerling et al., 1976 in trin- idadensis; Matteson, 1981 in utetheisae; Cross- man, 1925 in kuvanae), four (Maple, 1937 in Johnsoni; Laraichi, 1977 in fecundus, nigerrimus and telenomicida) to five (Parker, 1933 in kuva- nae; Takasu & Hirose, 1989 in nezarae). The true number of instars is probably four or five since these counts are based on the mandibles of the exuviae of previous instars which remain attached to the anal shield of the final instar larva. Development time In both kuvanae and anasae development from egg to adult takes about 18-35 days depending on temperature (Muesebeck & Dohanian, 1927; Tracy & Nechols, 1987). In manii no develop- ment of immatures occurs if the temperature is over 32.5°C (Rahim et al., 1991). O kuvanae has 4 or 5 generations per year in more northerly parts of the USA (Crossman, 1925) and up to 7 generations per year in Italy (Prota, 1966) and overwinters as an adult. Adult longevity In manii longevity of both sexes decreases with an increase in temperature, males will live 4 to 1.2 days with temperatures of 15—36°C whilst females live from 10-1.7 days at the same tem- peratures. In general, longevity increases with an increase in humidity, with optimum at 50-70% RH (Rahim ef al., 1991). This is also reflected by longevity and fecundity of the same species dur- ing different seasons, the highest fecundity (37 eggs/female) being noted in April and the lowest (0.8 eggs/female) being noted in January and February (Yadav & Chaudhary, 1984). In some species day length may effect reproduction and longevity. For instance, in kuvanae longer day length results in more progeny but lower longev- ity (Weseloh, 1986). Sex ratio and sex determination The sex ratio varies from about to 1:1 to 4:1 in favour of females (johnsoni Maple, 1937). In anasae the proportion of females increases with number of hosts parasitized (Tracy & Nechols, 1987). Sex ratio may also be influenced by tem- perature. For instance, in fecundus (Laraichi, 1978c) all progeny are female if the ovipositing female is subjected to temperatures of 30°C but all progeny are male if the ovipositing female is subjected to a temperature of 35°C (Laraichi, 1978c). In O. submetallicus similar temperatures produce similar results with hermaphrodite mosaics being produced if the developing prog- eny are subjected to intermediate temperatures (Wilson, 1962; Wilson & Woolcock, 1960). This suggests that the sex of the offspring may be under the control of a microorganism similar to 4 that found in some species of Trichogramma (see Stouthamer et al., 1990; Stouthamer, 1990, 1991). However, Kamay (in Brown, 1984) reported that if developing kuvanae were exposed to temperatures of around 35°C this D.-W.HUANG AND J.S. NOYES resulted in a higher proportion of females, possi- bly because of higher male mortality. Seasonal fluctuations of temperature influence the sex ratio of manii (Yadav & Chaudhary, 1984). SYNOPSIS OF HOSTS OF INDO-PACIFIC SPECIES [] extralimital records * probably incorrect host association ! laboratory reared (H) hyperparasitoid All reared from eggs except those prefixed by (L) — from larvae, and (P) — from prepupae or pupae. HOST Unknown eggs COLEOPTERA Chrysomelidae Plesispa reichei Chapius Podontia quatuordecimpunctata (Linnaeus) Podontia quatuordecimpunctata (Linnaeus) Coccinellidae (P)indet. DIPTERA Syrphidae (P)Allograpta exotica (Wiedemann) (L)Dideopsis pura (Curran) (L)[Ischiodon scutellaris (Fabricius) (L)[Ischiodon aegyptius Wied (Wiedemann) (L)Paragus auritus Stuckenberg HEMIPTERA indet family Heteroptera Alydidae Leptocorisa sp. Leptocorisa acuta Thunberg [Mirperus jaculus (Thunberg) Piezodorus hybneri (Fabricius) Riptortus sp. Riptortus sp. [Riptortus dentipes (Fabricius) Coreidae Amblypelta sp. Amblypelta cocophaga China Amblypelta lutescens Distant Amblypelta papuensis Brown [Anoplocnemis curvipes (Fabricius) PARASITOID (Ooencyrtus sp.) ceres pindarus corbetti podontiae guamensis * guamensis guamensis guamensis] guamensis]} guamensis ferrierei utetheisae utetheisae utetheisae] utetheisae cybele utetheisae utetheisae] caurus ilion caurus utetheisae caurus utetheisae] REVISION OF INDO-PACIFIC SPECIES OF OOENCYRTUS [Clavigralla elongata Signoret [Clavigralla tomentosicollis Stal Dasynus kalshoveni Blote Dasynus piperis China [Gonocerus acutangulatus Goeze [Gonocerus juniperi Herich-Schaeffer Mictis profana (Fabricius) [Pseudotheraptus wayi Brown Pentatomidae indet. [Brachynema germarii (Kolenati) [Dolycoris penicillatus Horvath Eocanthecona furcellata (Wolff) Nezara viridula (Linnaeus) Plataspidae Brachyplatys pacificus (Dallas) Cratoplatys sp. Scutelleridae [Eurygaster integriceps Puton [Aelia sp. Tessaratomidae Tessaratoma papillosa (Drury) Tessaratoma javanica (Thunberg) Pycanum ponderosum Stal Homoptera indet. family Lophopidae Pyrilla spp. Pyrilla perpusilla Walker Aphididae (L)indet. LEPIDOPTERA indet. indet. indet. (P)indet. leafmining family Agonoxenidae (L)Agonoxena pyrogramma Meyrick Arctiidae [Utetheisa pulchella (Linnaeus) Bombycidae Rondotia menciana Moore Crambidae Chilo terenellus Pagenstecher Danaidae Danaus chrysippus (Linnaeus) Euploea core (Cramer) Tirumala limniace (Cramer) Epipyropidae (P)Epiricania melanoleuca (Fletcher) Gracillariidae (P)Acrocercops globulifera Meyrick (P)Conopomorpha cramerella (Snellen) utetheisae| utetheisae| icarus utetheisae 'telenomicida] telenomicida] utetheisae utetheisae| lucens telenomicida] telenomicida] iulus uletheisae pacificus ceres telenomicida] telenomicida] phongi phongi phongi midas mani mani pallidipes * phongi * Javanicus utetheisae ool shakespearei utetheisae hercle papilionis papilionis papilionis papilionis 6 Heliconiidae Heliconius charitonius (Linnaeus) Hesperiidae Erionota thrax (Linnaeus) Hasora sp. Lasiocampidae Dendrolimus sp. Dendrolimus kikuchii Matsumura Dendrolimus spectabilis Butler Malacosoma americana Malacosoma neustria tartacea Motschulsky Taragama repanda Hubner Lymantriidae Aroa cometaris Butler Euproctis chrysorrhoea (Linnaeus) Hemerocampa leucostigma Abbot & Smith Hemerocampa definata Packard [Lymantria dispar (Linnaeus) [Lymantria fumida Butler Lymantria xylina Swinhoe [Nygmia phaeorrhoea Donovan [Stilpnotia salicis Linnaeus Noctuidae Achaea janata (Linnaeus) (L)Exelastis atomosa (Walsingham) Othreis fullonia (Clerck) Othreis fullonia (Clerck) (L)Mythimna unipuncta (Haworth) Notodontidae Clostera cupreata (Butler) Stauropus lichenina Butler Turnaca acuta (Walker) Nymphalidae Ariadne ariadne (Linnaeus) Caligo memnon (Felder) Hypolimnas bolina Linnaeus Kallima sp. Phalanta phalantha (Drury) Junonia lemonias (Linnaeus) Tanaecia julii Bougainville Papilionidae Troides helena Linnaeus Papilio sp. Papilio sp. Papilio aegeus Donovan Papilio agamemnon (Linnaeus) Papilio citri (?lapsus for demoleus Papilio demoleus Linnaeus Papilio helenus Linnaeus Papilio memnon Linnaeus Papilio polytes Linnaeus Papilio rumanzovia Eschscholtz Pieridae (L)Delias sp. Eurema sp. Hebomoia glaucippe (Linnaeus) Saturniidae D.-W.HUANG AND J.S. NOYES papilionis pallidipes papilionis endymion endymion kuvanae !kuvanae kuvanae !telenomicida papilionis !kuvanae !kuvanae 'kuvanae kuvanae]| kuvanae] ?kuvanae kuvanae]| kuvanae]| lucens guamensis crassulus papilionis guamensis lucina boreas macula papilionis pallidipes papilionis papilionis papilionis papilionis papilionis papilionis papilionis plautus papilionis papilionis plautus papilionis papilionis paplionis papilionis papilionis larvarum larvarum hera REVISION OF INDO-PACIFIC SPECIES OF OOENCYRTUS 7 Attacus atlas Fabricius phoebi Callosamia promethea Drury !kuvanae Cricula sp. Javanicus Cricula elaezia Jordan dione [Eriogyna pyretorum Westwood kuvanae]| Hemileuca maia Drury !kuvanae Hemileuca oliviae Churchill !kuvanae Sphingidae indet. endymion Amorpha populi austanti Staudinger 'telenomicida Cephonodes hylas (Linnaeus) papilionis ?Gnathothlibas erotus eras (Boisduval) sphingidarum Hippotion celerio (Linnaeus) crassulus NEUROPTERA Myrmeleontidae indet. ixion USE OF OOENCYRTUS IN IZAS Instiute of Zoology, Chinese Academy of Sciences, Beijing, P.R. China BIOLOGICAL CONTROL MARI Malaysian Agricultural Research and Development Institute, Kuala Lumpur, Although species of Ooencyrtus undoubtedly Malays MNHN Museum National d’Histoire Naturelle, play an important role in the regulation of the populations of many insect species worldwide, they have not proven to be of great value in pest control. Their use in classical biological control programmes is summarised in Table 1. Perhaps the best documented example is that of Ooencyr- tus kuvanae for the control of the gypsy moth (Lymantria dispar) in North America and Europe. Brown (1984) comments that although affording some control, the species is unlikely to be of much benefit by itself, although it probably causes a post outbreak collapse which in turn increases the length of the interval between out- breaks. A further species, Ooencyrtus fecundus Fer- riére & Voegelé, may be of some benefit if used by means of inundative releases against het- eropterous pests of wheat in North Africa (Larai- chi & Voegelé, 1975). DEPOSITORIES BMNH The Natural History Museum, London, England BPBM Bernice P. Bishop Museum, Hawaii CNC Canadian National Collection, Ottawa, Canada IARI Indian Agriculture Research Institute, New Delhi, India IEE Institito di Entomologia Espanol, Madrid, Spain IRSN Institute Royal des Sciences Naturelles de Belgique, Brussels, Belgium Paris, France MZB Museum Zoologicum Bogoriense, Bogor, Indonesia ORSTOM Office de la Recherche Scientifique et Technique Outre-Mer, Paris, France PPRI Plant Protection Research Institute, Preto- ria, South Africa QMB Queensland Museum, Brisbane, Australia TAMU Texas A&M University, Texas, USA USNM United States National Museum, Washing- ton, D.C., USA ZAMU Zoology Department, Aligarh Muslim Uni- versity, Aligarh, India ZISP Zoological Institute, St Petersberg, Russia ACKNOWLEDGEMENTS We thank The Royal Society which provided the senior author the opportunity to study at The Natural History Museum in London. Many thanks to Mr David Foster of The Royal Society, who gave the senior author consistent help dur- ing his stay in UK. The Natural History Museum made its collections, facilities and libraries avail- able to us for the project. The senior author’s host institution, Institute of Zoology, Chinese Academy of Sciences permitted him one year off. We also thank Nigel Wyatt, Jeremy Holloway, Gary Stonedahl, Phil Ackery, Mike Shaffer and Mick Webb for checking host names, and thanks especially to John LaSalle for his valuable com- ments concerning the manuscript. Finally we are grateful to Dr M. Schauff (USNM), Dr G. 8 D.-W.HUANG AND J.S. NOYES Table 1 A summary of the use of Ooencyrtus spp. in classical biological control programmes worldwide (Abbreviations: NE — not established; NR — not released; ? — no subsequent information; SC — successful control; P — partial control; E — established but no further information available; NC — established but no significant control achieved). Target pest species HEMIPTERA Amblypelta cocophaga Amblypelta theobromae Anasa tristis Eurygaster integriceps Murgantia histrionica Nezara viridula Pseudotheraptus wayi Soybean stink bugs LEPIDOPTERA Ascotis selenaria Calpodes ethlius Conopomorpha cramerella Erionota thrax Hemerocampa leucostigma Hemileuca oliviae Lymantria dispar Othreis fullonia Nishida (BPBM), Dr J.-L. Nieves Aldrey (IEE), Trjapitzin (ZISP), Dr G.L. Prinsloo Dil: — Introduced Ooencyrtus sp.; country; year; result; source —sp.; Solomon Is; 1937-38; NE; Phillips (1941) — malayensis (?= utetheisae, misident.); Solomon Is; 1937-38; NE; Phillips (1941) — malayensis (?= utetheisae, misident.); Papua New Guinea; 71974; ?; Young (1982) — malayensis (?= utetheisae, misident.); USA (Massachusetts); 1981; ?; Coulson et al. (1988) — fecundus; USSR; ?; NR; Izhevskiy (1988) — nigerrimus; USSR; ?; NR; Izhevskiy (1988) — telenomicida; USSR; ?; NR; Izhevskiy (1988) —johnsoni; Bermuda; 1953; NE; Bennett & Hughes (1959) — johnsoni; Hawaii; 1940; E; Clausen in Clausen (1978) —johnsoni; Australia; 1953; NR; Wilson (1960) — malayensis (?= utetheisae, misident.); USA (Massachusetts); 1981; ?; Coulson et al. (1988) — submetallicus; Australia; 1952-57; NE; Wilson (1960) — submetallicus; Hawaii; 1962; NE; Davis (1964), Waterhouse & Norris (1987) — submetallicus; USA (Florida); 1973; ?; CIBC (1974) — trinidadensis; Hawaii; 1962; NE; Davis (1964), Waterhouse & Norris (1987) — sp. (?= utetheisae); Zanzibar; 1959; ?; Greathead (1971) — sp. (?= utetheisae); Kenya; 1959; ?; Greathead (1971) — nezarae; Brazil; 1983-1985; ?; Kobayashi & Cosenza (1987) — ennomophagus; Israel; 1977; NR; Wysoki (1979) — sp. (= calpodicus); Bermuda; 1953, 1962-63; NC; Cock (1985) — sp. (= calpodicus); St Vincent; 1950-51; E; Cock (1985) — sp. (= ooii); Malaysia (Sabah); 1987; NE; CIBC (1988, 1989, 1990) — pallidipes; Hawaii; 1973; SC; Mau, et al. (1980) — pallidipes; Mauritius: 1971-72; P; Waterhouse & Norris (1989) — kuvanae; USA; 1917, 1921; NE; Dowden (1962) — kuvanae; USA (New Mexico); 1913-16; NE; Clausen (1956) — kuvanae; Algeria; 1925-26, 1931; E; Lepigre (1932), Clausen (1978) — kuvanae; Canada (Ontario); 1976; E; Brown (1984) — kuvanae; Czechoslovakia; 1922; E; Clausen (1978) — kuvanae; Morocco; 1924-26; E; Brown (1984), Clausen (1978) — kuvanae; Portugal; 1932; E; Brown (1984), Clausen (1978) — kuvanae; Spain; 1923-27; E; Brown (1984), Clausen (1978) — kuvanae; USA; 1908-28, 1967-1971, 1981; E; Brown (1984), Peck (1963), Clausen (1956, 1978), Coulson et al. (1988) — kuvanae; CIS; 1987; ?; Volkov & Mirohova (1990) — kuvanae; Yugoslavia; ?1960; ?; Brown we) — sp. (?= papilionis),; American Samoa; ? ; 2; Waterhouse & Norris (1987) — sp. (?= papilionis); Western Samoa; ?; °°: - Waterhouse & Norris (1987) SYSTEMATIC SECTION (PPRI), Dr G. Gibson (CNC), Dr P. Dessart (IRSN) and Mr E.C. Dahms (QMB) for the loan or gift of material. OOENCYRTUS Ashmead Ooencyrtus Ashmead, 1900: 381. Type species: Encyrtus clisiocampae Ashmead, by original designation. Echthrodryinus Perkins, 1906: 252. Type species: REVISION OF INDO-PACIFIC SPECIES OF OOENCYRTUS 9 Echthrodryinus destructor Perkins, by mono- typy. Synonymy with Ooencyrtus by Noyes & Hayat, 1984. Ectopiognatha Perkins, 1906: 254. Type species: Ectopiognatha minor Perkins, by designation of Gahan & Fagan, 1923: 49. Syn.nov. Schedius Howard, 1910: 2. Type species: Sche- dius kuvanae Howard, by original designation. Synonymy with Ooencyrtus by Ferriére, 1931. Tetracnemella Girault, 1915: 170. Type species: Tetracnemella australiensis Girault, by original designation. Synonymy with Ooencyrtus by Noyes & Hayat, 1984. Xesmatia Timberlake, 1920: 424. Type species: Xesmatia flavipes Timberlake, by original des- ignation. Synonymy with Ooencyrtus by Noyes & Hayat, 1984. Pseudolitomastix Risbec, 1954: 1068. Type spe- cies: Litomastix creona Risbec. Synonymy with Ooencyrtus by Annecke & Mynhardt, 1973. Comments on generic synonymy Species previously combined with the genus Ectopiognatha can be separated from Ooencyrtus by the quadridentate mandibles and a broadened and flattened scape. However, one of the species included in this revision (leander sp.n.) is extremely close in general structure to both spe- cies included in Ectopiognatha except that it has a cylindrical scape. In addition, several described species of Ooencyrtus have a scape which is distinctly broadened. The biology of Ectopiog- natha spp. (parasitoids of the eggs of Hemiptera) falls within the range of that found in Ooencyrtus (see below) and, therefore, we have no hesita- tion in treating the two genera as synonymous. Noyes and Hayat (1984) treated Echthrodryi- nus as a synonym of Ooencyrtus whilst Gordh & Trjapitzin (1978) and later Trjapitzin (1989) have treated it as valid. It is not possible to separate the two genera on morphological grounds and the only possible basis for continuing to treat them as distinct is that the included species have different biologies. Ooencyrtus could be restricted to primary parasitoids (or perhaps hyperparasitoids) of the eggs of various insects, whilst Echthrodryinus could include primary parasitoids or hyperparasitoids of the larvae or prepupal stages of certain holometabolous insects, e.g. Dryinidae, Braconidae and Gracilla- riidae. However, one species, Ooencyrtus kuva- nae, has been recorded both as a primary parasitoid of the eggs of gypsy moth (Lymantria dispar) and as a hyperparasitoid of the prepupal and pupal stages of the braconid Apanteles mel- anoscelus in their cocoons after they emerge from their gypsy moth caterpillar host (see below). Recent work (Noyes, 1985 and Prinsloo, 1987) has shown that the host range of Ooencyr- tus spp. is much more diverse than had previ- ously been thought, many species being noted as parasitic on nymphs of Aphididae (Hemiptera) and Syrphidae (Diptera), even to the extent where specimens that attack dipterous or coleopterous larvae are morphologically indistin- guishable from those that attack heteropterous eggs (see Noyes, 1985). In view of this, we are continuing to treat Echthrodryinus as synony- mous with Ooencyrtus. Generic diagnosis In the most comprehensive classification of the Encyrtidae currently available, Trjapitzin (1973, 1989) includes Ooencyrtus in the Encyrtinae, tribe Microteryini, subtribe Ooencyrtina. Unfor- tunately, this classification does not provide any meaningful diagnoses for the tribes or subtribes. We are therefore hopeful that the following diagnosis will enable species to be assigned cor- rectly to Ooencyrtus: Robust, squat species, never conspicuously slender and elongate; thorax with posterior margin of mesoscutum weakly to strongly con- vex medially and overlying axillae centrally so that when thorax is in normal resting position axillae appear to be widely separated; mesopleuron posteriorly expanded so that it touches base of gaster, or nearly so, and com- pletely conceals the metapleuron and propo- deum from lateral view immediately above the hind coxae; forewing with marginal vein punc- tiform or not much longer than broad, Species of Ooencyrtus can be most easily con- fused with Trichomasthus, Helegonatopus and Psyllaephagus. Both Helegonatopus and Psyl- laephagus have the mesopleuron normal, not expanded posteriorly and not touching the base of the gaster so that in lateral view the metapleu- ron and propodeum are not obscured and touch the hind coxae. Species of Trichomasthus are generally much larger, usually being about 1.5 mm long, the marginal vein of the forewing is normally several times longer than broad, and all species are parasitoids of scale insects (Coc- coidea). Superficially, the placement of the genus within the tribe Microteryini may appear some- what questionable, especially on _ biological grounds. Morphologically, it is possibly to see an evolutionary trend from a Microterys-like or Trichomasthus-like ancestor, some species of Microterys and Trichomasthus being quite similar 10 structurally and, as stated above, it can be some- times quite difficult to separate Ooencyrtus from Trichomasthus. If it is hypothesized that the plesiomorphic host association for the tribe is scale insects (Homoptera; Coccoidea) (see Trjapitzin, 1989) then it would be possible to envisage a switch from parasitising insects with hard a scale covering and a host immune system, to parasitising the eggs of other insects which have a hard outer shell and no immune system. A further switch to hyperparasitism of Braconidae or Dryinidae, or parasitism of the immature stages of holometabolous insects (Diptera and Lepidoptera) is much more difficult to envisage, but at least two species are known to parasitise both hemipterous or lepidopterous eggs and the prepupae or pupae of holometabolous insects, i.e. kuvanae (Muesebeck & Dohanian, 1927) and submetallicus (see Noyes, 1985). Systematic relationships within the genus The relationships within Ooencyrtus are unclear and we do not attempt to provide any sort of formal classificatory framework within the genus by proposing subgeneric categories. However, probable assemblages of closely related species within the genus are highlighted in the comments sections of the appropriate species. Identification of species The following works should be consulted as aids to the identification of species from outside the Oriental region: Peck (1963) and Gordh (1979) for North America; Noyes (1985) and De Santis (1988) for South America; Trjapitzin (1989) for the Palaearctic; Prinsloo (1987) for Africa. Previous work dealing with the species within the Indo-Pacific area has not much value, either because of inadequate coverage of the species, or because it relies on poor characters whilst over- looking important diagnostic features. The only key available (Trjapitzin et al., 1978) is based almost entirely on inadequate original descrip- tions and is therefore of little use. Although we describe males of each species when they are available, they are excluded from the key to species. Males are often difficult to identify because they do not present many fea- tures and are unknown for most of the species included here. However, the presence of males in a reared series may help to confirm the separa- tion of some closely related species, e.g. sphingi- darum and papilionis. During the course of this work we have found D.-W.HUANG AND J.S. NOYES the following characters especially helpful in identifying species: Mandibles — several basic types, a) with one tooth and a broad straight, sometimes minutely denticulate truncation (Figs 10, 18, 139, 188, 204, 333, etc.), b) with one tooth and a broad, slightly convex, minutely denticulate truncation (Figs 303), ¢) one tooth and a distinctly emarginate truncation, or with two teeth and a truncation (Figs 75, 143, 150, etc.), d) tridentate (Fig. 69, 91, 268, etc.), all teeth subequal, e) one or two teeth and an oblique minutely denticulate trunca- tion, (Fig. 240), f) three acute, unequal teeth (Fig. 176), or g) four teeth (Fig. 46). Clava — a) clava with apex rounded and sensory area at extreme apex only (Figs 42, 47, 51, etc.) b) clava with sutures transverse and parallel, apex obliquely truncate and sensory area enlarged (Figs 9, 104, 196, etc.), or c) clava with sutures oblique, apex obliquely truncate and sensory area enlarged (Figs 16, 22, 28, 193, etc). Eyes — a) conspicuously hairy, or b) almost naked. Ocelli — relative distance of ocelli from occipital margin in terms of their own diameters. Antennal toruli — relative distance below eyes or above mouth margin in terms of their own lengths. Interantennal prominence — coloration purple or metallic green or blue green, etc. Scutellum — relative depth and type of sculpture in relation to mesoscutum. Forewing — relative density and distribution of setae on both dorsal and ventral surfaces of basal cell and on ventral surface of costal cell; linea clava closed or open; relative length of marginal and postmarginal veins in relation to stigmal. Legs — the coloration of coxae, femora and tibia seems to be reliable although there may be a slight amount of variation in the intensity of any brown areas on the femora and tibia. The colora- tion of the fore and hind coxae may vary from yellow to largely brown in some species. Gaster — the relative length may be unreliable because it may depend on the preservation tech- niques used. In air dried specimens the gaster collapses and may thus be relatively shorter than in Critical Point Dried specimens where the gaster remains inflated (see Gordh & Hall, 1976). The shape of the last tergite (apically rounded, truncate or medially invaginated) may be useful as well as the shape of the hypopygium (rectangular, triangular, with long or short ante- rior lateral projection, relative size of posterior incision, distribution and relative density of setae). REVISION OF INDO-PACIFIC SPECIES OF OOENCYRTUS Ovipositor — other than the usual characters such as relative length of the gonostyli or overall length of the ovipositor in relation to the mid tibia we have found that the shape of the proxi- mal part of the second valvifer can be extremely useful (e.g. compare upper parts of Figs 225 and 226). The length of the ovipositor is here taken as the combined length of the second valvifer together with the third valvula (gonostylus). Abbreviations used in text Fl, F2, etc.— First funicle segments, second OOL POL funicle segment, etc. — Ocular-ocellar line, or the shortest distance between each _ posterior ocellus and the adjacent eye margin. — Posterior ocellar line, or the short- est distance between the two poste- rior ocelli. Key to Oriental species of Ooencyrtus (females) 1 2(1) 3(2) At least one pair of coxae black or brown, concolorous with mesopleuron; gaster entirely black or brown without any yellow or orange areas All coxae yellow (occasionally fore coxae slightly infuscate); gaster frequently yellow or orange in part, although often entirely black or brown All coxae and femora conspicuously black or brown (rarely femora yellow with inconspicu- ous brown markings but if so then clava has a broad, slightly oblique apical truncation, the funicle segments are quadrate or transverse, the scape is subcylindrical (Fig. 9) and the scutellum has relatively shallow sculpture basally (Fig. 12)) Not all coxae and femora black or brown, at least some of them yellow (clava usually with apex rounded but if with a distinct, slightly oblique apical truncation, then either some funicle segments are clearly longer than broad, or the scape is strongly flattened and only about 2.5 times as long as broad (Fig. 104), or the scutellum has deep punctate-sculpture basally (asin) Fig. 109))) once seme seorceccer anc 20 Antenna (Figs 1, 9, 16, 22, 28, 34) with clava robust and with a large sensory apical area which gives it a distinct transversely or obliquely truncate appearance Antenna (Figs 37, 42, 47, 51, 54, 59, 64, 67, 68, 76, 83) with clava normally comparatively slen- der and with only a small apical sensory area 6(4) 7(6) 8(7) 9(5) 11 which gives it a rounded or even pointed appearance Sensory part of clava less than one third length Of Clava (BIGS | AO) con actedismmscsocuceasseuhace 5 Sensory part of clava more than one-third length of clava (Figs 16, 22, 28, 34) Mesoscutum with numerous silvery setae; scutellum conspicuously reticulate throughout (Fig. 2); [fore-tibia of male characteristic (Fig. 7)) Pe eer tee een a guamensis (p. 16) Mesoscutum without silvery setae; posterior half of scutellum smooth (Fig. 12) ... acca (p. 17) Antenna with first funicle segment at least 1.5 times as long as broad and at least a little longer than sixth (Fig. 16) ..... phongi (p. 18) First funicle segment not, or hardly, longer than broad and shorter than sixth (Figs 22, 28,34) . 7 Frontovertex more than one-fifth head width; gaster apically acute with ovipositor exserted, the exserted part about as long as mid tibial spur; mandibles tridentate ........ acus (p. 19) Frontovertex less than one-fifth head width; gaster apically truncate with ovipositor more or less hidden; mandibles with one small tooth and a very broad truncation .................... 8 Scutellum with apical one-third smooth and Venysshin yivees ccscnwes: eee tetas caurus (p. 21) Reticulate sculpture of scutellum extending almost to posterior margin with only a very narrow smooth and shiny marginal strip- jc Pe A RT tial Mate Rath same lucens (p. 22) Forewing with linea calva closed posteriorly (Figs 38, 40); antenna with all funicle segments longer than broad (Fig. 37) ...............065 10 Either linea calva open posteriorly (Figs 44, 48, 53, 55, 60, 65, 70, 77) or antenna with some segments quadrate or transverse (Figs 42, 83) Flagellum bicolorous, funicle segments brown or testaceous, clava yellow .. minerva (p. 22) Flagellum unicolorous ........... icarus (p. 23) Scutellum anteriorly with shallow, indistinct sculpture, the posterior part smooth; fron- tovertex at least one-third head width (Figs 43, 45); mandibles (Fig. 46) with four teeth; ovi- positor exserted, the exserted part at least one-quarter as long as gaster ................. 12 Scutellum with conspicuous, raised, regular reticulations, only margin narrowly and some- times apex smooth (Figs 71, 80); frontovertex 12 12(11) 13(11) 14(13) 15(13) 16(15) 17(16) 18(17) normally distinctly less than one-third head width; mandibles tridentate (Figs 56, 74, 85) or with one or two teeth and a truncation (Figs 69, 75); ovipositor not exserted, but if so then exserted part less than one-fifth length of PASCER) «gape «qa ee = nae sicbtpeletee oracmectomeesisciee 13 Antenna (Fig. 42) with F1l—4 subequal and clearly smaller than F5-6, clava as long as F3-6; exserted part of ovipositor half to one- third gaster length ............... adonis (p. 24) Antenna (Fig. 47) with Fl the smallest and much smaller than F2-6 which are subequal in size, clava about as long as F4—6; exserted part of ovipositor about one-quarter as long as gaster site aplsiiapinae mace tact on aeneemenenene = aeneas (p. 25) Visible part of ovipositor sheaths white, yellow or amber and extending past apex of last tergite, although occasionally hardly so ... 14 Visible part of ovipositor sheaths brown to dark brown, frequently not extending past APEXTOMlASHILELBICS Hessen .peee see tereeee sere eae. 115) Reticulate sculpture of scutellum relatively shallow and hardly deeper than that on mesos- cutum, especially in apical half or so; mid femur and tibia hardly marked with brown, almost completely yellow; eye with conspicu- ous translucent setae ............ phoebi (p. 26) Reticulate sculpture of scutellum clearly deeper than that on mesoscutum except on sides an extreme apex; mid femur and tibia mostly dark brown; eye almost naked, with setae very short and inconspicuous kuvanae (p. 26) Scutellum uniformly bright green and with deep, more or less regular reticulate sculpture; mandibles with three acute teeth . dis (p. 27) Scutellum green only at sides and apex, other- wise blue, purple or coppery and relatively dull with sculpture elongate-reticulate or striate towards sides; mandibles with one or two teeth and a truncation (Figs 69, 75) Frontovertex about one-third head width (Fig. PD) \etrsa artis 30 -Bo IIE OSS a eOE ESBS hercle (p. 28) Frontovertex not more than one-quarter head width (Fig. 74, 85) Clava relatively short, only about as long as F4-6 combined (Fig. 64) ...... corbetti (p. 29) Clava at least as long as F3-6 combined ... 18 Mid and hind tibiae completely yellow, with- out a brown subbasal ring . podontiae (p. 30) Mid and hind tibiae each with a narrow brown subbasal:ring “MA Lee a A ae 19 19(18) 20(2) 21(20) 22(20) 23(22) 24(23) 25(24) 26(25) D.-W.HUANG AND J.S. NOYES Eye as broad as long or broader; antennae (Fig. 76) with F1—2 subequal in size and smaller than F3-6 ............. pindarus (p. 30) Eye distinctly longer than broad; antennae (Fig. 83) with F1-3 subequal in size and con- spicuously smaller than F4-6 . plautus (p. 31) Scutellum entirely smooth and shiny except for a small sculptured triangular area posterior to axillae, this extending less than half way along scutellum (Fig. 105); hypopygium reaching apex of gaster; gaster almost always with extensive yellow areas™ airee.n- eas ereeeeeeee ee 21 Scutellum more extensively sculptured with sculpture discernible in apical half (Figs 106, 109, 146); hypopygium never reaching apex, generally not reaching two-thirds along gaster; gaster without any yellow areas ............. 23 Forewing with a transverse fuscous band from marginal vein (Fig. 90); all coxae black- DEOWI we etn ves doceucreaee seach daphne (p. 33) Forewing completely hyaline (Figs 98, 99); at least hind coxae yellow ........ flavipes (p. 34) All coxae black or dark-brown Fore-coxae yellow Scape strongly broadened and flattened, only about 2.5 times as long as broad; antennae strongly clavate with club extremely large (Fig. 104) ieee eee dione (p. 34) Scape subcylindrical, at least about 4 times as long as broad; antenna not strongly clavate and with club of normal proportions, not conspicu- ously enlarged (Figs 108, 113, 120, 125, 126, 1295134): 140591425: 148): Sores eee eer 24 Forewing with a median fuscous band (Fig. 107); antennae white except for radicle . dryas (p. 35) Forewing hyaline; antennae testaceous or browns not white”