J. HYM. RES. Vol. 13(2), 2004, pp. 243–249

A New Species of (: ): A Gall-inducing Pest on (Fabaceae)

IL-KWON KIM, GERARD DELVARE, AND JOHN LA SALLE (IKK, JLS) CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia; email: [email protected] (GD) CIRAD TA 40L, Campus International de Baillarguet-Csiro, 34398 Montpellier Cedex 5, France; email: [email protected]

Abstract.— Kim sp.n. is described from Singapore, Mauritius and Re´- union. This species forms galls on the leaves, stems, petioles and young shoots of Erythrina var- iegata and E. fusca in Singapore, on the leaves of E. indica in Mauritius, and on Erythrina sp. in Re´union. It can cause extensive damage to the trees. Key words.—Hymenoptera, Eulophidae, Quadrastichus, phytophagous, gall inducer, Singapore, Mauritius, Erythrina, Fabaceae

Species of Eulophidae are mainly para- 1988; Redak and Bethke 1995; Headrick et sitoids, but secondary phytophagy in the al. 1995); burwelli Schauff form of gall induction has arisen on many (Schauff and Garrison 2000); and Leptocybe occasions (Boucˇek 1988; La Salle 1994; invasa Fisher & La Salle (Mendel et al. Headrick et al. 1995; Mendel et al. 2004; 2004). Quadrastichus erythrinae Kim sp.n. La Salle 2004). Gall-inducing Eulophidae has recently achieved pest status in Sin- generally belong to two groups: Opheli- gapore, Mauritius and Re´union. Erythrina mini is an Australian lineage which con- trees have been grown in these areas for sists mainly of gall inducers on eucalypts, decades, and this species has never been but perhaps also on some other myrta- recorded from them. Although its exact ceous hosts (Boucˇek 1988; La Salle 2004); origin remains unknown, it is likely to and includes several in- represent another example of an invasive stances of gall induction, but it is ques- pest species. tionable that these represent a single evo- There are approximately 110 species of lutionary event (La Salle 2004). Genera of Erythrina around the world, mostly found Tetrastichinae where gall induction is in tropical regions (Mabberly 1987). Their known to occur include Quadrastichodella, beautiful red flowers have earned them Oncastichus, Epichrysocharis, Aprostocetus, the common name of coral trees, and Paragaleopsomyia, Ceratoneura, ‘Exurus’, made them a popular tree to be used in and Leptocybe (La Salle 2004; Mendel et al. landscaping in many tropical regions. 2004). Recently, a eulophid species was found Several species of tetrastichine gall in- from galls on Erythrina in Singapore and ducers have become invasive pests, partic- sent to one of us [JL]; at about the same ularly in the last decade, these include: time galls were found in Mauritius and Quadrastichodella nova Girault (Flock 1957, Re´union, with wasps being sent to another as Flockiella eucalypti; Timberlake 1957, as of us [GD]. Comparison of the two sam- Flockiella eucalypti; Boucˇek 1988); Oncasti- ples showed that there was a single, wide- chus goughi Headrick & LaSalle (Gough spread species involved. This wasp can 244 JOURNAL OF HYMENOPTERA RESEARCH cause severe damage to Erythrina trees, donesia; PPRI, Biosystematics Division, and has become a nuisance in these coun- Plant Protection Research Institute, Preto- tries. ria, South Africa; QMB, Queensland Mu- Records of gall-inducing wasps on Ery- seum, Brisbane, Australia; USNM, United thrina are not extensive. Annecke & Moran States National Museum of Natural His- (1982) reported on Erythrina galls in South tory, Washington, D.C., USA. Africa. Five species of chalcidoid wasps were reared from these galls, the most SYSTEMATICS common being a Eulophidae sp. and a Quadrastichus erythrinae Kim, sp.n. Eurytoma sp. (). At that time, (Figs 1–10) the Eurytoma was suspected as being the gall inducer. Recent examination of the Types. Holotype &: SINGAPORE, material (by Dr. G.L. Prinsloo) has shown 02.vi.2003, He Liansheng, reared from that there are two eulophid species pres- galls on Erythrina fusca (ANIC). ent, but neither of them are the same as Paratypes: 63&, 118(, Same data as Ho- Q. erythrinae. Because this species was lotype (28&, 83( ANIC; 5&, 5( each: found on Re´union and Mauritius, one of BMNH, CIRAD, CNC, MZB, PPRI, QMB, us [GD] compared this species with all USNM). species described by Risbec from Mada- Non-type material: MAURITIUS: Bras gascar; however, it did not agree with any d’Eau, 04.iv.2003, D. Ramkhelawon, vii.03, previously named species. ex. Erythrina indica leaves (12&, 14(, Quadrastichus erythrinae Kim represents ANIC); Quatre Bornes, 17.vii.2003, (S. Per- the first record of a gall inducer in the ge- malloo), ex. leaf galls on Erythrina indica ´ nus Quadrastichus. Species of Quadrastichus (3&, 5(, ANIC). LA REUNION: Saint- have a variety of biologies: many are par- Pierre, Bassin Plat, 06.xii.2000, G. Delvare asitoids of gall-inducing hosts, such as Ce- & A. Franck, ex. galls on Erythina sp. (33&, cidomyiidae (Diptera) and Cynipidae (Hy- 38( CIRAD); Saint-Benoıˆt, 24.ii.2003, S. menoptera); others are parasitoids of Bu- Quilici, ex. galls on Erythina sp., Ref. NЊ prestidae and Curculionidae (Coleoptera), RQ 4611 & Cirad 18009 (21&, 11( CIR- or Agromyzidae and Tephritidae (Dip- AD). tera); Q. sajoi (Szele´nyi) larvae are preda- Description tors of eriophyid mites within galls (Gra- ham 1991, La Salle 1994, Hansson and La Female Length 1.45–1.6 mm. Dark Salle 1996). brown with yellow markings. Head yel- Terminology used in this paper is taken low, except gena posteriorly brown. An- from Gibson (1997) and Graham (1987); tenna pale brown except scape posteriorly OOL, ocell–ocular distance; POL, post- pale. Pronotum dark brown. The mid lobe ocellar distance; MPS, multiporous plate of mesoscutum with a ‘‘V’’ shaped or in- sensilla. verted triangular dark brown area from Acronyms used in the text are as fol- anterior margin, the remainder yellow. lows. ANIC, Australian National Scapula yellow. Scutellum, axilla and dor- Collection, CSIRO Entomology, Canberra, sellum brown to light brown. Propodeum Australia; BMNH, The Natural History dark brown. Gaster brown. Fore and hind Museum, London, UK; CIRAD, Centre de coxae brown. Mid coxa almost pale. Fem- Coope´ration Internationale en Recherche ora mostly brown to light brown. Speci- Agronomique pour le De´veloppement; mens from Mauritius are generally darker CNC, Canadian National Insect Collec- than those from Singapore. tion, Ottawa, Ontario, Canada; MZB, Mu- Head (Figs 1–2). Ocellar triangle sur- seum Zoologicum Bogoriense, Bogor, In- rounded by groove; transverse groove ex- VOLUME 13, NUMBER 2, 2004 245

Figs. 1–6. Quadrastichus erythrinae sp. n.—1. Head, frontal view; 2. Head, dorsal view; 3. Head and thorax, lateral view; 4. Mesosoma, dorsal view; 5. Gaster, lateral view; 6. (Genitalia, dorsal view. 246 JOURNAL OF HYMENOPTERA RESEARCH tending from lateral ocellus to eye. POL basal vein, leaving the speculum partially 1.6–2.0 times longer than OOL. Frons with open behind; the speculum small. broad median area, but without median Gaster (Fig. 5). Slightly longer than the carina. Toruli situated at level of lower eye head plus mesosoma. Hypopygium ex- margin. Shallow groove present beneath tending 0.8–0.9 the length of gaster and torulus, extending slightly over half the reaching up to the posterior margin of G6. distance from torulus to clypeal margin. Ovipositor sheath not protruding, short in Gena slightly swollen and malar sulcus dorsal view. Cercus with 3 setae, the lon- only slightly curved, without triangular gest one slightly curved and about 1.3 as fovea below eyes. Clypeal margin biden- long as the others, which are subequal in tate. length. Antenna (Fig. 7) with one large anellus. Male. Length 1.0–1.15 mm. Pale colora- All funicular segments 1.3–1.6 times lon- tion white to pale yellow as opposed to ger than wide and each segment approx- yellow in female. Head and antenna pale. imately equal in length and width to the Pronotum dark brown (but in lateral view, others. However, under the microscope only upper half dark brown; lower half with slide-mounted antenna, each succes- yellow to white). Scutellum and dorsellum sive segment appears slightly wider than pale brown. Axilla pale. Propodeum dark previous one. Sensilla (MPS) slightly brown. Gaster in anterior half pale; re- shorter than length of funicular segment, mainder dark brown. Legs all pale. each sensilla reaching to the next funicular Antenna (Fig. 8) with 4 funicular seg- segment; 1–2 sensillae visible on each seg- ments; without the whorl of setae; F1 dis- ment in lateral view. Scape not extending tinctly shorter than the other segments above the vertex. and slightly transverse; about 1.4 wider Mesosoma (Figs 3–4). Median line on than long. Ventral plaque extending 0.4– the mid lobe of mesoscutum very weak to 0.5 length of scape and placed in apical absent but usually at least indicated in cer- half. tain angles and light; if indicated, it can be Gaster shorter than female. Genitalia seen superficially only in posterior half. (Fig. 6) elongate, with digitus about 0.4 Mid lobe of mesoscutum with 3 to 5 short length of the long, exserted aedagus. [Dor- adnotaular setae. Scutellum with distinct sally exposed parts of the genitalia were submedian lines and sublateral lines; 2 measured.] pairs of setae on scutellum (occasionally Etymology. The specific name erythrinae with an additional seta), anterior seta sit- comes from the genus name of the host uated well behind midlength of scutellum. plant. Precoxal suture distinct and extending Biology. Reared from galls on Erythrina about 0.7 length of mesopleuron. Propo- variegata L., E. fusca Lour. (ϭE. glauca deal spiracle relatively large, whole rim Willd.) and E. indica L. (Figs 11–12). Inside exposed. Propodeum without distinct me- the leaf galls there is usually only one dian carina or paraspiracular carina. Pro- wasp per cell, while in the swollen tissues podeal callus with 2 setae. of shoots, twigs and petioles more than Wing (Figs 9–10). Submarginal vein five individuals were observed. with 1 seta, situated slightly basal to the Distribution. Singapore, Mauritius, Re´- middle. Costal cell without setae. Post- union. It is not known if this wasp is na- marginal vein almost rudimentary; less tive to one of these regions or not. than 0.3 length of stigmal vein. Costal cell: marginal vein: stigmal vein: postmarginal Discussion vein ϭ 3.9–4.1: 2.8–3.1: 1.0: 0.1–0.3. Cubital This species fits the definition of Quad- line of setae not extending all the way to rastichus offered by Graham (1991): SMV VOLUME 13, NUMBER 2, 2004 247

Figs. 7–10. Quadrastichus erythrinae sp. n.—7. Antenna, &; 8. Antenna, (; 9. Forewing; 10. Submarginal vein.

Figs. 11–12. Galls on stems, petioles, and young shoots of Erythrina induced by Quadrastichus erythrinae. 248 JOURNAL OF HYMENOPTERA RESEARCH with 1 dorsal seta, antenna with all funic- fly from seed-like Eucalyptus galls in California. ular segments longer than wide and with Pan-Pacific Entomologist 33: 153–155. 1–3 anelli in female and gaster longer than Gibson, G. A. P. 1997. Morphology and Terminology. Pp. 16–44, in: Annotated Keys to the Genera of Ne- the head plus mesosoma. However, the arctic Chalcidoidea (Hymenoptera) (eds GAP Gib- species is distinct from all other Quadras- son, JT Huber & JB Woolley). National Research tichus on the basis of the long hypopy- Council Research Press. Ottawa, Ontario, Cana- gium. da. 794 pp. The only key to species of Quadrastichus Gough, N. 1988. Gall forming wasps on Geraldton of any region is Graham (1991) for Euro- wax. News Bulletin, Entomological Society of Queensland 15(10): 131–132. pean species. In this key, this species Graham, M. W. R. de V. 1987. A reclassification of the would run to the anysis-group of Q. anysis European Tetrastichinae (Hymenopter: Eulophi- (Walker), Q. citrinus (Thomson) and Q. dae), with a revision of certain genera. Bulletin of xanthosoma (Graham) as follows: body the British Museum (Natural Histroy) Entomology black and yellow as opposed to metallic series 55(1): 1–392. and without yellow markings; frons with Graham, M. W. R. de V. 1991. A reclassification of the European Tetrastichinae (Hymenoptera: Eulo- median area but without median carina; phidae): Revision of the Remaining Genera. gena slightly swollen, malar sulcus only Memoirs of the American Entomological Institute 49: slightly curved, malar sulcus without a 1–322. large subtriangular fovea just beneath eye. Hansson, C. and La Salle, J. 1996. Two new eulophid However, Quadrastichus erythrinae dif- parasitoids (Hymenoptera: Chalcidoidea: Eulo- fers from the anysis-group because: clypeal phidae) of Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). Oriental 30: 193–202. margin bidentate, scape not exeeding Headrick, D. H., La Salle, J., and Redak, R. A. 1995. above the vertex, apex of hypopygium ex- A new genus of Australian Tetrastichinae (Hy- tending distinctly beyond middle of gas- menoptera: Eulophidae): an introduced pest of ter. Males of the anysis-group have whorls Chamelaucium uncinatum (Myrtaceae) in Califor- of long setae on the funicular segments nia. Journal of Natural History 29: 1029–1036. (Graham, 1991; Reina & La Salle, 2004), La Salle, J. 1994. North American genera of Tetrasti- chinae (Hymenoptera: Eulophidae). Journal of however these are absent in Q. erythrinae. Natural History 28: 109–236. Additionally, the anysis-group appears to La Salle, J. 2004. Biology of gall inducers and evolu- be restricted to leafminer hosts. tion of gall induction in Chalcidoidea (Hyme- noptera: Eulophidae, Eurytomidae, Pteromali- ACKNOWLEDGMENTS dae, Tanaostigmatidae, Torymidae). Pp. 507–537, in: Raman, A., Schaeffer, C. W. & Withers, T. M. We are grateful to He Liansheng (Agri-Food & Vet- (eds), Biology, ecology, and evolution of gall-induc- erinary Authority of Singapore) for providing speci- ing . Science Publishers, Inc., USA. 823 mens and information about the biology of Q. ery- pp (2 vols). thrinae, and S.I. Seewooruthun (Ministry of Agricul- Mabberly, D. J. 1987. The Plant-Book. A portable dictio- ture, Mauritius) for sending us samples of Q. erythri- nary of the higher plants. Cambridge University nae. Gerhard Prinsloo, Plant Protection Research Press, Cambridge. 707 pp. Institute, Pretoria, offered advice and helpful com- Mendel, Z., Protasov, A., Fisher, N., and La Salle, J. ments. A. Franck, from CIRAD Re´union made the 2004. The and natural history of Lep- photographs of the infested Erythrina. tocybe invasa (Hymenoptera: Eulophidae) gen & sp. nov., an invasive gall inducer on Eucalyptus. LITERATURE CITED Australian Journal of Entomology 43: 101–113. Annecke, D. P. and Moran, V. C. 1982. Insects and Redak, R. A. and Bethke, J. A. 1995. Detection and Mites of Cultivated Plants in South Africa. Butter- seasonal occurrence of gall-forming wasps (Hy- worth. Durban and Pretoria. 383 pp. menoptera: Eulophidae) on Geraldton wax plant. Boucˇek, Z. 1988. Australasian Chalcidoidea (Hymenop- Journal of Economic Entomology 88(2): 387–392. tera): A Biosystematic Revision of Genera of Fourteen Reina, P. and La Salle, J. 2004. Two new species of Families, with a Reclassification of Species. CAB In- Quadrastichus Girault (Hymenoptera: Eulophi- ternational, Wallingford, U.K. 832 pp. dae), parasitoids of the leafminers Phyllocnistis ci- Flock, R. A. 1957. Biological notes on a new chalcid- trella Stainton (Lepidoptera: Gracillariidae) and VOLUME 13, NUMBER 2, 2004 249

Liriomyza trifolii (Burgess) (Diptera: Agromyzi- placement of the genus. Journal of Hymenoptera dae). Journal of Hymenoptera Research 13: 108–119. Research 9: 176–181. Schauff, M. E. and Garrison, R. 2000. An introduced Timberlake, P. H. 1957. A new entedontine chalcid- species of Epichrysocharis (Hymenoptera: Eulo- fly from seed capsules of eucaplyptus in Califor- phidae) producing galls on Eucalyptus in Califor- nia (Hymenoptera: Eulophidae). Pan-Pacific En- nia with notes on the described species and tomologist 33: 109–110.