The identity and recognition of African Tetrastichus species (Hymenoptera: Eulophidae) associated with fruit flies (Diptera: Tephritidae)

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1 The identity and recognition of African Tetrastichus species (Hymenoptera: Eulophidae) associated with fruit flies (Diptera: Tephritidae) J. LaSalle 1* & R.A. Wharton 2 1 Unit of Parasitoid Systematics, CABI Bioscience U.K. Centre (Ascot), Department of Biology, Imperial College at Silwood Park, Ascot, Berks, SL5 7PY, U.K. 2 Department of Entomology, Texas A&M University, College Station, Texas, 77843, U.S.A. INTRODUCTION The identity of the African fruit fly (Diptera: Tephritidae) parasitoids Tetrastichus giffardii Silvestri, T. giffardianus Silvestri, T. dacicida Silvestri and T. oxyurus Silvestri (Hymenoptera: Eulophidae) is discussed. Tetrastichus dacicida is synonymized with T. giffardii. Characters to recognize and differentiate Tetrastichus giffardii, T. giffardianus, and T. oxyurus are presented. Lectotypes are designated for all four of these species. Key words: Eulophidae, Tetrastichinae, Tetrastichus, fruit flies, Tephritidae, parasitoid. Fruit flies in the family Tephritidae are major pests in Africa and other parts of the world, and one of the most serious and widespread pests of edible fruits, Ceratitis capitata (Wiedemann) (medfly), is of African origin. African parasitoids, mostly opiine Braconidae and tetrastichine Eulophidae, have been used in numerous tephritid biological control programmes worldwide (Silvestri 1913b; Clausen et al. 1965; Clausen 1978; Steck et al. 1986). Most of these species were initially introduced from Africa to Hawaii, then redistributed from Hawaii to other parts of the world (Clausen 1978; Wharton 1989). At least four nominal species of Tetrastichus (Eulophidae) have been shipped to Hawaii since 1914 for tephritid biological control. Tetrastichus giffardianus Silvestri has subsequently been sent to at least eight other countries, and was the focus of a mass-rearing programme directed primarily against medfly in Brazil (Fonseca & Autuori 1940; Fonseca 1947). The status of the other species is largely unknown, in part because of the lack of adequate information on how to differentiate the species. Proper identification of parasitoids used in biological control is imperative, and the purpose of this paper is to resolve questions regarding the identity of the African Tetrastichus species attacking fruit flies and to provide a key to their identification. The ability to differentiate these species is particularly crucial to studies attempting to verify apparent differences in patterns of host utilization by the various eulophids that have been reared from tephritids. *Present address: CSIRO Entomology, G.P.O. Box 1700, Canberra, ACT, 2601, Australia. The only other tetrastichine recorded from fruit flies in Africa is Aceratoneuromyia indica Silvestri. This, and possibly other species of Aceratoneuromyia which might be present, are easily distinguishable from Tetrastichus species by the presence of three or more setae on the submarginal vein as opposed to a single seta in Tetrastichus (Figs 6, 7). Tetrastichines are commonly encountered in studies of the parasitoid fauna of tephritids in Africa, but native tetrastichines appear to be absent from the parasitoid community attacking New World tephritids. It is likely that additional species of Tetrastichus may be found parasitizing fruit flies in Africa. TAXONOMIC HISTORY The genus Tetrastichus as it was traditionally treated was one of the largest genera in the Chalcidoidea and contained the majority of species in the subfamily Tetrastichinae. However, this was not a natural classification and merely reflected the difficult taxonomy of this group of insects. Graham (1987) provided a reclassification of the European Tetrastichinae, in which he divided Tetrastichus into several smaller and more natural groups; this classification has since been followed by Bou ek (1988), Graham (1991) and LaSalle (1994). The genus Tetrastichus in its current sense is the third largest genus of Tetrastichinae, and occurs on all continents. Graham (1991) referred to a small group of species within Tetrastichus, which he called the murcia group (= subgenus Musciformia Kostjukov 1977). He stated that although African Entomology 10(2): (2002)

2 298 African Entomology Vol. 10, No. 2, 2002 having a rather characteristic habitus, the group is difficult to define. Species have relatively long setae on the vertex (their length that of the ocellar diameter), and moderately long to very long setae on the eyes ( the ocellar diameter). Other characters that help to define this group (taken from Graham s key) are: frons with oblong median area; mouth width at most only slightly greater (less than 1.3 times) than malar space; antenna with scape shorter than eye, its front edge with six or fewer setae; mesosoma with distinct engraved reticulation; setae on hind margin of pronotum and adnotaular setae relatively long and suberect; hind coxa more strongly and coarsely reticulate dorsally than elsewhere, usually more or less rugulose dorso-basally; gaster less than twice as long as broad, shorter than head plus mesosoma, with last tergite less than 1.7 times longer than broad; ovipositor sheaths reaching apex of last tergite. Graham (1991) placed five European species in the murcia group, T. murcia (Walker), T. dasyops Graham, T. atratulus (Nees), T. brachyopae Graham, T. solvae Graham, and mentioned that the African T. giffardii Silvestri and T. giffardianus also belong to this group. All species in this group appear to be parasitoids of Diptera. It is not clear that T. oxyurus belongs in this group, as the setae on its vertex and mesosoma are relatively short and not semi-erect. MATERIALS AND METHODS Lectotypes are designated for four species in this paper. These were chosen from material originally collected by Silvestri and stored in alcohol for over 80 years. The poor condition of the material and similarity of the species involved could lead to confusion over the identity of these species. In all cases, lectotypes were designated in order to maintain stability of usage for the names. Type material for this study is all from Silvestri material in the collection of the Dipartimento di Entomologia e Zoologia Agraria dell Università, Portici, Italy (DEZA). In many cases, not all the type material was found in DEZA. However, Silvestri routinely exchanged material with other dipterists and hymenopterists of the era. These included type specimens, although they were not always correctly labelled as such. Thus, it is not at all surprising that only parts of his series are at Portici. Nonetheless, it was decided to designate lectotypes in each case from among the original Silvestri material that was retained in DEZA. Other material was examined from The Natural History Museum, London (BMNH), the United States National Museum, Washington (USNM), the Bernice P. Bishop Museum, Honolulu (BPBM), and collections made as part of this study in Texas A&M University, College Station (TAMU) and the International Centre for Insect Physiology and Ecology, Nairobi, Kenya (ICIPE). Not all material examined is listed under each species, but new records are indicated. Terminology is taken from LaSalle Genus Tetrastichus Haliday, 1844 Diagnosis. Submarginal vein with one dorsal seta (with the exception of T. howardi, T. inferens which have two). Propodeum with a characteristic carina in the shape of an inverted Y just medial to the spiracle (Fig. 8); median panels of the propodeum generally reticulate. Outer surface of hind coxa usually with strong reticulations. Body usually black to dark or bright metallic, generally without light coloration. Key to female African Tetrastichus species associated with fruitflies 1. Gaster long, pointed apically, clearly more than 1.5 times as long as mesosoma (Fig. 2); hypopygium extending less than half the length of gaster, ovipositor greater than twothirds the length of gaster, last tergite longer than wide. Antenna without semi-erect setae, or with shorter setae (Fig. 3, cf. Figs 10, 11); antennal segments all distinctly longer than wide; setae on vertex between lateral ocellus and eye margin usually shorter than greatest width of ocellus (Fig. 1) T. oxyurus Gaster shorter, rounded apically, clearly less than 1.5 times as long as mesosoma (Fig. 5); hypopygium extending half or more the length of gaster; ovipositor less than twothirds the length of gaster; last tergite wider than long. Antenna with more distinct semi-erect setae (Figs 10, 11, cf. Fig. 3); at least some antennal segments quadrate to wider than long; setae on vertex between lateral ocellus and eye margin usually longer than greatest width of ocellus (Fig. 4) Speculum large, extending along anterior margin of wing to base of stigmal vein

3 LaSalle & Wharton: African Tetrastichus species associated with fruit flies 299 Figs 1 5. Differences of Tetrastichus oxyurus from T. giffardii and T. giffardianus T. oxyurus female: 1, head; 2, mesosoma and metasoma; 3, antenna, showing scape to club only T. giffardii female: 4, head; 5, mesosoma and metasoma. (Fig. 7). Basal vein mostly without setae, base of cubital vein mostly without setae, so that speculum is largely open behind. Paraspiracular carina usually not as distinct as in giffardii, with outer branch poorly defined (Fig. 9, cf. Fig. 8) T. giffardianus Speculum small, extending along anterior margin of wing much less than half the distance to the base of stigmal vein (Fig. 6). Basal and cubital veins complete; speculum completely closed behind. Paraspiracular carina distinct, with outer branch well defined (Fig. 8, cf. Fig. 9) T. giffardii Tetrastichus giffardii Silvestri, Figs 4 6, 8, Tetrastichus giffardii Silvestri, 1913a: Lectotype 9 [present designation] Nigeria, Olokemeji, 27.xi.1912, F. Silvestri, ex Ceratitis antisticta (DEZA). 49, 58 paralectotypes, same data as lectotype (DEZA). Tetrastichus dacicida Silvestri, 1915:

4 300 African Entomology Vol. 10, No. 2, 2002 Figs 6 9. Differences between Tetrastichus giffardii and T. giffardianus Forewings: 6, T. giffardii; 7, T. giffardianus Scutellum and propodeum: 8, T. giffardii; 9, T. giffardianus. Lectotype 9 [present designation] Cameroon, Victoria, i.1913, F. Silvestri, ex. Dacus bipartitus [= Dacus bivittatus] (DEZA). 28 paralectotypes, same data as lectotype (DEZA). Syn. n. Biology. From the following hosts (all Tephritidae): Bactrocera cucurbitae (Coquillett), Bactrocera dorsalis (Hendel), Ceratitis anonae Graham, Ceratitis antisticta Bezzi, Ceratitis capitata (Wiedemann), Ceratitis colae Silvestri, Ceratitis ditissima (Munro), Ceratitis giffardi Bezzi (probably a synonym of C. cosyrae: DeMeyer 1998), Ceratitis punctata (Wiedemann), Ceratitis rosa Karsch var. fasciventris, Ceratitis simi (Munro), Dacus bivittatus (Bigot), Trirhithrum coffeae Bezzi. Host information mainly taken from Noyes (1998, as either T. giffardii or T. dacicida), although nomenclature has been updated using Norrbom et al. (1998). Although both T. giffardii and T. giffardianus are widely polyphagous, one major pest species listed above, Ceratitis rosa and its variety fasciventris, is a definite host for T. giffardii, whereas we have not yet confirmed it as a host for T. giffardianus. Greathead (1972) reported that T. giffardii attacked fruit flies in Ugandan coffee, but did not act in a density dependent manner, and only reached detectable levels when host populations were high. The present study shows that this species can be fairly common in Kenyan squash. Tetrastichus giffardii is a gregarious, koinobiont endoparasitoid. Silvestri (1913b) stated that T. giffardii oviposited in the eggs or young larvae of their hosts. This is different from T. giffardianus, which prefers older larvae (4 7 days) for oviposition (Purcell et al. 1996). Several adults will emerge from each host puparium. Silvestri also

5 LaSalle & Wharton: African Tetrastichus species associated with fruit flies 301 Figs Variation in Tetrastichus giffardii , female antenna (note difference in relative size of first two funicular segments); 12 13, male antenna (note difference in relative size of first two funicular segments); 14 15, ventral sensory plaque on male scape. noted (1915) that the biology of T. dacicida was similar to that of T. giffardii. Distribution. Congo, Cameroon, Benin, Ghana, Kenya, Nigeria, Uganda (Noyes 1998). Imported into Hawaii against Bactrocera dorsalis, but without major impact (Clausen 1978). All recent records from Hawaii are of T. giffardianus, suggesting that T. giffardii may never have established there. Remarks. T. giffardii: Silvestri (1913a) did not mention how many specimens he used in the description of T. giffardii. However, he did state that between 15 and 34 individuals emerged from each Ceratitis or Dacus pupa, indicating that he had seen many specimens. The lectotype was selected from 10 specimens (59, 58) in the DEZA collection, so some type specimens are missing. T. dacicida: Silvestri (1915) made no mention of how many specimens he had when describing T. dacicida. The lectotype was selected from three specimens (19, 28) in the DEZA collection. The decision to synonymize T. dacicida with T. giffardii was not a simple one. Table 1 lists characters given by Silvestri (1915) to separate the two species, with comments on each character. Basically, none of the characters proved to be consistent and without variation. Examination of type material did not show characters that could be used, or even that were always consistent with Silvestri s observations on the difference; and field collected material could not be divided

6 302 African Entomology Vol. 10, No. 2, 2002 Table 1. Characters provided by Silvestri (1915) to distinguish Tetrastichus dacicida from T. giffardii. Sex T. dacicida T. giffardii Comments Female Funicular segments 2 and 3 longer than in T. giffardii. Funicular segments shorter than in T. dacicida. Subjective and variable. It is not clear just what Silvestri meant by shorter and longer as he did not give actual range measurements. Certainly this is variable in the material examined (Figs 10 11). Female Female Male Male Mesoscutum with more lateral setae [from the description seven short setae on each side]. A seta situated in base of wing near the base of the basal vein. This apparently refers to a basal seta in the cubital vein which is placed basal to junction of cubital vein and basal vein. Scape with ventral plaque longer, more or less divided. The first funicular segment shorter than the second. Mesoscutum with fewer lateral setae [from the redescription (Silvestri 1913b) three setae on each side]. Seta absent Scape with ventral plaque shorter, not divided. The first funicular segment longer than the second. Most T. giffardii examined have 3 4 adnotaular setae. None have seven, including the T. dacicida types. We have seen some series where this seta is generally present, and these specimens also tend to have F2 and F3 longer. However, the mesoscutum still has only 3 4 adnotaular setae, the male antenna does not display the T. dacicida characters, and the character is not consistent in the entire series. It is again not clear just what Silvestri meant by shorter and longer as he did not give actual range measurements. As to the division, this plaque is mostly undivided in all T. giffardii specimens (including the only male dacicida paralectotype which has antennae). A few specimens were examined in which this plaque is malformed and apparently in two parts. This appears to be just an occasional aberration, and not a valid species level character (Figs 14 15). This is variable, even in the series of five male T. giffardii paralectotypes, as at least one of them has F1 distinctly shorter than F2 (Figs 12 13). into groups, which would be indicative of species differences. Thus, we are synonymizing T. dacicida with T. giffardii. Tetrastichus giffardianus Silvestri, Figs 7, 9 Tetrastichus giffardianus Silvestri, 1915: Lectotype 9 [present designation] Benin (Dahomey), Cotonou, ii.1913, F. Silvestri, ex Ceratitis giffardi (DEZA). 29, 28 paralectotypes, same data as lectotype (DEZA). Biology. From the following hosts (all Tephritidae): Bactrocera cucurbitae (Coquillett), Bactrocera dorsalis (Hendel), Bactrocera latifrons (Hendel), Bactrocera passiflorae (Froggatt), Bactrocera tryoni (Froggatt), Bactrocera xanthodes (Broun), Ceratitis anonae Graham, Ceratitis capitata (Wiedemann), Ceratitis giffardi Bezzi (probably a synonym of C. cosyrae: DeMeyer 1998), Ceratitis punctata (Wiedemann), Dacus bivittatus (Bigot), Dacus ciliatus (Loew), Dacus demmerezi (Bezzi), Neoceratitis cyanescens (Bezzi), Trirhithrum nigrum (Graham). Host information mainly taken from Noyes (1998), although nomenclature has been updated using Norrbom et al. (1998). During the course of the present study, and through examination of the literature, this species has often been reared from collections of fruits from which several species of fruit flies have also emerged. Under these circumstances, precise host relationships could not be determined. Although several additional species of hosts have been implicated in this fashion, they were not included in the host lists. This species is a gregarious, koinobiont, larval pupal endoparasitoid (Clausen 1978; Ramadan & Wong 1990; Purcell et al. 1996). The parasitoid oviposits into mature host larvae, and the adults emerge from young pupae after the puparium is formed. Tetrastichus giffardianus has been used as a biological control agent against a variety of fruit flies in several countries (Clausen 1978; Purcell 1998). Because of its wide host range, it has recently been studied to see if it has a non-target effect on other fruit fly species. It was found not to parasitize any non-frugivorus tephritids in Hawaii (Purcell et al.

7 LaSalle & Wharton: African Tetrastichus species associated with fruit flies ; Duan & Messing 1998). Distribution. Benin, Cameroon, Egypt, Kenya, Nigeria, Sierra Leone, Tanzania. Introduced into the Réunion Islands; in the New World into Argentina, Brazil, Puerto Rico, U.S.A. (California); and in the Australia/Pacific region into Australia, Fiji, Hawaii, New Caledonia, Samoa, Vanuatu (Noyes 1998; Clausen 1978). Establishment was never documented in some of the areas of introduction (e.g. California), and its current status in all but Hawaii is unknown. Remarks. Silvestri (1915) made no mention of how many specimens he had when describing T. giffardianus; however, he did mention that this species was known from Nigeria and Benin (Dahomey). The lectotype was selected from five specimens (39, 28) from Benin in the DEZA collection, so some type material is missing. Tetrastichus oxyurus Silvestri, Figs 1 3 Tetrastichus oxyurus Silvestri, 1913b: Lectotype 9 [present designation] Nigeria, Olokemeji, F. Silvestri, ex Carpophthoromyia (as Ceratitis) tritea (DEZA). 29 paralectotypes, same data as lectotype (DEZA). Biology. This species was described from 10 specimens that emerged from a puparium of Carpophthoromyia tritea (Walker). Distribution. Kenya (new record), Nigeria. Remarks. Silvestri (1913b) described this species from 10 female specimens. The lectotype was selected from three female specimens in the DEZA collection, so some type specimens are missing. ACKNOWLEDGEMENTS We thank G. Viggiani and E. Guerrieri for kindly locating and loaning the Silvestri types. M. Purcell provided recently collected material from Hawaii and S. Kimani allowed us the opportunity to examine material acquired under ICIPE s African fruit fly initiative. Other curators who have loaned material or given access to their collections are: K. Arakaki (BPBM), J. Noyes (BMNH), M. Schauff (USNM). M. De Meyer and I. White supplied information on the tephritid host names. This work was supported in part by USDA/NRI grant No and the Texas Agricultural Experiment Station. REFERENCES BOU EK, Z Australasian Chalcidoidea (Hymenoptera). A Biosystematic Revision of Genera of Fourteen Families, with a Reclassification of Species. CAB International, Wallingford, U.K. CLAUSEN, C.P. (Ed.) Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. Agricultural Handbook No U.S. Department of Agriculture, Washington, D.C. CLAUSEN, C.P., CLANCY, D.W. & CHOCK, Q.C Biological control of the Oriental fruit fly (Dacus dorsalis Hendel) and other fruit flies in Hawaii. United States Department of Agriculture, Technical Bulletin 1322: DE MEYER, M Revision of the subgenus Ceratitis (Ceratalaspis) Hancock (Diptera: Tephritidae). Bulletin of Entomological Research 88: DUAN, J.J. & MESSING, R.H Effect of Tetrastichus giffardianus (Hymenoptera: Eulophidae) on nontarget flowerhead-feeding tephritids (Diptera: Tephritidae). Environmental Entomology 27: FONSECA, J.P Criação da vespinha africana no Instituto Biológico. O Biológico 13: FONSECA, J.P. & AUTUORI, M Processos de criação da Vespinha africana parasita da mosca do Mediterraneo. O Biológico 6: GRAHAM, M.W.R. DE V A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum (Natural History). Entomology Series 55: GRAHAM, M.W.R. DE V A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae): revision of the remaining genera. Memoirs of the American Entomological Institute 49: GREATHEAD, D.J Notes on coffee fruit-flies and their parasites at Kawanda (Uganda). Technical Bulletin of the Commonwealth Institute of Biological Control No. 15: LaSALLE, J North American genera of Tetrastichinae (Hymenoptera: Eulophidae). Journal of Natural History 28: NORRBOM, A.L., CARROLL, L.E., THOMPSON, F.C., WHITE, I.M. & FREIDBERG, A Systematic database of names. Myia 9: NOYES, J.S Catalogue of the Chalcidoidea of the World. Biodiversity Catalogue Database and Image Library CD-ROM Series. Expert Center for Taxonomic Identification, University of Amsterdam, Amsterdam. PURCELL, M.F Contribution of biological control to integrated pest management of tephritid fruit flies in the tropics and subtropics. Integrated Pest Management Reviews 3: PURCELL, M.F., DUAN, J.J. & MESSING, R.H Response of three hymenopteran parasitoids introduced for fruit fly control to a gall-forming tephritid, Procecidochares alani (Diptera: Tephritidae). Biological Control 9: PURCELL, M.F., VAN NIEUWENHOVEN, A. & BATCHELOR, M.A Bionomics of Tetrastichus

8 304 African Entomology Vol. 10, No. 2, 2002 giffardianus (Hymenoptera: Eulophidae): an endoparasitoid of tephritid fruit flies. Environmental Entomology 25: RAMADAN, M.M. & WONG, T.T.Y Biological observations on Tetrastichus giffardianus (Hymenoptera: Eulophidae), a gregarious endoparasitoid of the Mediterranean fruit fly and the Oriental fruit fly (Diptera: Tephritidae). Proceedings, Hawaiian Entomological Society 30: SILVESTRI, F. 1913a. Notizia preliminare di un Tetrastichus (Immenottero Calcidide) parassita di specie di Ceratitis e Dacus nell Africa occidentale. Reale Accademia dei Lincei 22: SILVESTRI, F. 1913b. Viaggio in Africa par cercare parassiti di mosche dei frutti. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d Agricoltura in Portici 8: SILVESTRI, F Descrizione di nuovi imenotteri calcididi africani. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d Agricoltura in Portici 9: STECK, G.J., GILSTRAP, F.E., WHARTON, R.A. & HART, W.G Braconid parasitoids of Tephritidae [Diptera] infesting coffee and other fruits in westcentral Africa. Entomophaga 31: WHARTON, R.A Classical biological control of fruit-infesting Tephritidae. In: Robinson, A.S. & Hooper, G. (Eds) Fruit Flies, Their Biology, Natural Enemies and Control World Crop Pests 3B. Elsevier, Amsterdam. Accepted 20 November 2001