A new species of Strepsitera Halictophagus naulti (Halictophagidae) that is parasitic in the corn leafhopper Dalbulus maidis (Delong and Wolcott) from the Mexican state of Morelos is described

Kathirithamby, J

Moya-Raygoza, G

Kathirithamby, Jeyaraney

Oxford University Research Archive

SYSTEMATICSHalictophagus naulti sp. n. (Strepsiptera: Halictophagidae),a New Species Parasitic in the Corn Leafhopper(Homoptera: Cicadellidae) from MexicoJEYARANEY KATHIRITHAMBY1 AND GUSTAVO MOYA-RAYGOZA2Ann. Entomol. Soc. Am. 93(5): 1039Ð1044 (2000)ABSTRACT A new species of Strepsiptera Halictophagus naulti (Halictophagidae) that is parasiticin the corn leafhopper Dalbulus maidis (Delong & Wolcott) from the Mexican state of Morelos isdescribed.KEY WORDS Halictophagus naulti, Dalbulus maidis, Strepsiptera, Halictophagidae, Homoptera,CicadellidaeTHE CORN LEAFHOPPER, Dalbulus maidis (Delong &Wolcott), is the most important leafhopper pest ofmaize in Latin America (Nault 1990). This speciestransmits three pathogens: the corn stunt spiroplasma(CSS), the maize bushy stunt phytoplasma (MBSP),and themaize rayadoÞnomaraÞvirus (MRFV)(Nault1980). The distribution of these pathogens coincideswith the distribution of the corn leafhopper, whichoccurs throughout the southern United States (Cali-fornia, Florida, and Texas) to Argentina, including theCaribbean Islands (Nault 1983). In addition, D.maidisis found at a wide range of elevations from sea level to3,200 m (Nault et al. 1979).Mesoamerica (throughout central Mexico to Nica-ragua) is considered the center of origin of D. maidis,and the 13 species of the genus Dalbulus have beencollected from maize and its closest relatives (teos-intes and gamagrasses Tripsacum) (Triplehorn andNault 1985, Nault 1990, Nault and Styer 1994). Dal-bulus gramalotes Triplehorn & Nault is the only spe-cies collectedoutsideMesoamerica (Nault 1990). Thisgeographic range is not only the center of origin forDalbulus spp. but also for their parasitoids (Moya-Raygoza and Trujillo-Arriaga 1993).To date, taxa of the parasitoids of D. maidis havebeen recorded from Mesoamerica. Adults of D. maidisare parasitized by the ßy Eudorylas (Metadorylas)absonditus Hardy (Diptera: Pipunculidae) in Texcocostate, Mexico (Vega et al. 1991), and by the waspGonatopus bartletti Olmi (Hymenoptera: Dryinidae)in four Mexican states: Jalisco (Moya-Raygoza andTrujillo-Arriaga 1993), Guanajuato, Mexico, andVeracruz (Vega and Barbosa 1990). In Nicaragua theeggs of D. maidis are parasitized by the wasps Anagrussp. (Hymenoptera: Mymaridae) and Paracentrobia sp.(Hymenoptera: Trichogrammatidae) (Gladstone etal. 1994). Furthermore, in Mesoamerica, Dalbulus eli-matus (Ball) is parasitized by E. (Metadorylas) abson-ditus (Vega et al. 1991) and Gonatopus flavipes Olmi,whereas D. quinquenotatus Delong & Nault is parasit-ized by the dryinids Gonatopus moyaraygozai OlmiandAnteon ciudadiOlmi (Moya-Raygoza andTrujillo-Arriaga 1993).Here we report a new species, Halictophagus naulti(Strepsiptera), parasitic on D. maidis that was col-lected from maize in July 1994 from Tlaltizapán, stateofMorelos,Mexico. The stylopized adultswere rearedindividually in maize plants to obtain adult H. naulti,from which three males and several females werecollected.Halictophagus has a cosmopolitan distribution andparasitizes four families of Homoptera (Kathi-rithamby 1989) and six subfamilies of Cicadellidae(Freytag 1985, Kathirithamby 1992a). Strepsipterahave shown potential for controlling leafhopper pestssuch asPerkinsiella vitiensisKirkaldy, 70%ofwhich areparasitized by Elenchoides perkinsi Pierce on sugarcane in Fiji (Clausen 1972). Riek (1975) described anewspeciesHalictophagus irwiniparasitic inD.distansL. from Natal, South Africa. These results suggest thatH. naulti might be used as biological control of D.maidis.Eleven species of Strepsiptera have been describedfrom Mexico (Table 1). Kifune and Brailovsky (1987)provided a list and keys to Strepsiptera of Mexico, andKathirithamby (1992b) provided an up-to-date list ofStrepsiptera from Mesoamerica.Halictophagus naulti sp. n.Adult Male (Fig. 9). Head width, 0.34Ð0.36 mm.Maxilla. Maxilla three times longer than mandibles(base, 0.03Ð0.05mm;palpi, 0.11Ð0.12mm)(Figs. 1 and12).1 Department of Zoology, South Parks Road, Oxford OX1 3PS, UK.2DepartamentodeBotanicayZoologia,C.U.C.B.A.,UniversidaddeGuadalajara, Km 15.5 Carretera Guadalajara-Nogales, Las Agujas,Zapopan, C.P. 45110, Apdo. Postal 139, Jalisco, Mexico.0013-8746/00/1039Ð1044$02.00/0 q 2000 Entomological Society of AmericaDownloaded from https://academic.oup.com/aesa/article-abstract/93/5/1039/9117 by Said Business School user on 09 September 2019Mandibles.Mandiblesdonotmeet incenter(lengthof mandibles, 0.04 mm) (Fig. 10).Antennae. Seven-segmented with ßabellum onIIIrd-VIth segments (IIIrd ßabellum; 0.22Ð0.23 mm;IVth ßabellum, 0.19Ð0.22mm;Vth ßabellum, 0.10mm;VIth ßabellum, 0.11 mm) (Figs. 2 and 10).Thorax. Scutum1prescutum, 0.14Ð0.16 mm; scute-llum, 0.10 mm. Postlumbium with two long indenta-tions, length at middle region, 0.06Ð0.07 mm. Postno-tum very long, 0.29Ð0.30 mm, and as long asscutum1prescutum, scutellum and postlumbium(Fig. 4).Wing. Sc, R1, and R2 prominent; R3 pale and longand a third longer than R2; R5 meets dent in marginof wing; MA two-thirds the length of CuA, CuPpresent. Length of wing (along its longest length),1.05Ð1.25 mm (Fig. 7).Abdomen. A cone-shaped projection present onVIIIth abdominal sternitewhich is darker in color thanthe rest of the sternites (Figs. 3, 5, and 11). Xth ab-dominal segment as long as IXth (length of VIIIthsternite, 0.07Ð0.09 mm; length of IXth abdominal ster-nite, 0.09Ð0.10 mm; length of Xth abdominal sternite,0.09 mm).Aedeagus. Aedeagus with a small curved apex (Fig.6).Male Cephalotheca. Unknown.Female. Pale yellow above and brown below theopening of the brood canal. The triangular sclerotizedcollar (within the host) (Kathirithamby 2000) is vis-ible through the transparent host cuticle. Opening ofbrood canal broad with semicircular upper margin(Fig. 8).Length of cephalothorax, 0.18Ð0.21 mm; width ofcephalothorax, 0.16Ð0.17 mm; length of brood canalopening, 0.10 mm; width of opening, 0.04Ð0.05 mm.Type Material. Holotype: ?, Tlaltizapán, Morelos,MEXICO, 23-VII-94 (G. Moya-Raygoza and W. Styer.Paratypes: 3 //, in host, Tlaltizapán, Morelos, Mex-ico, 31-VII-94 (G. Moya-Raygoza and W. Styer). 1 ?,Tlaltizapán, Morelos, Mexico, 23-VII-94 (G. Moya-Raygoza and W. Styer). 1 /, in host, Tlaltizapán,Morelos, Mexico, 31-VII-94 (G. Moya-Raygoza andTable 1. List of Strepsiptera from MéxicoTaxa Location HostFamily Corioxenidae Kinzelbach, 1971Subfamily Triozocerinae Kinzelbach, 1970Genus Triozocera Pierce, 1909maxicana Pierce, 1909 Veracruz* , Oaxaca Pangaeus bibineautus (Say)texana Pierce, 1911 (Hem: Cydnidae)tecpanensis Brailovsky & Márquez, 1974 Guerrero* Unknownvernalis Kifune & Brailovsky, 1987 Puebla* : Jalisco UnknownFamily Halictophagidae Perkins, 1905Subfamily Halictophaginae Perkins, 1905Genus Halictophagus Curtis, 1831acutus Bohart, 1943 Atzcapotzalco, D.F.* Draeculacephala mollipes (Say)D. minerva Ball (Hom: Cicadellidae)Family Elenchidae Perkins, 1905Subfamily Elenchinae Perkins, 1905Genua Elenchus Curtis, 1831koebelei Pierce, 1908 Northern District* Liburnia campestris Van Duzee.(Hom: Delphacidae)koebelei Pierce, 1908tenuicornis Baumert, 1959heidemanni Pierce, 1918heidemanni Pierce, 1918mexicanus (Pierce, 1961) Veracruz* (Sogata) Liburnai cubana(Crawford) (Hom: Delphacidae)butzei Brailvosky, 1981 Veracruz* unknownFamily Myrmecolacidae Saunders, 1872Genus Caenocholax Pierce, 1909fenyesi Pierce, 1909 Veracruz; Tabasco UnknownGenus Stichotrema Hofender 1910trilobulatum Brailovsky, 1974 Galeana* , Guerrero Unknownsyn. of S. beckeriOliveria & Kogan, 1959(Kinzelbach & Pohl, 1994)mexicanum Kifune & Brailovsky, 1987 Veracruz* UnknownFamily Stylopidae Kirby, 1813Genus Melittostylops Kinzelbach, 1971hesparapium Kinzelbach, 1971 Chihuahua* ; Baja California Hesperapis rhodocerata (Cockerell)H. leucura Cockerell (Hym. Melittidae)* , type locality.1040 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 5Downloaded from https://academic.oup.com/aesa/article-abstract/93/5/1039/9117 by Said Business School user on 09 September 2019W. Styer). All of the above are at the Hope Entomo-logicalCollections,OxfordUniversityMuseumofNat-ural History. 2 ??, Tlaltizapán, Morelos, Mexico,6-VII-94(G.Moya-RaygozaandW.Styer). 1/, inhost,Tláltizapan, Morelos, Mexico, 6-VII-94 (G. Moya-Ray-goza and W. Styer). The last two are in the ColecciónEntomológica, C.U.C.B.A., Universidad de Guadala-jara, Mexico.Etymology. The new species is named after L. R.Nault, whohas beenworking onDalbulus for 26 years.Diagnosis. The new species differs from male H.lopesi Oliveira and Kogan (1959) from Brazil by theshape of the apex of the aedeagus, which is onlyslightly curved, whereas in H. lopesi the apex is asmooth hook with an elongated point. It differs fromH. barberi (Pierce 1908) by the longer maxilla, thepostnotum, which is twice as long as scutum1prescutum, scutellum, and postlumbium, whereas inH. baberi postnotum as long as scutum 1 prescutum,scutellum, and postlumbium. It differs from male H.irwini by the shape and structure of the antennalsegments, particularly the longer ßabella of the IIIand IV segments; by the shape and structure of thecurved anterior margin of the scutellum, and theabsence of the very stout, broadly based spines onthe IX abdominal sternite. It differs from female H.irwini by the opening of the brood-canal, with itssemicircular upper margin, and the collar within thehost is a short triangular area, whereas in H. irwiniFigs. 1–6. (1) Maxilla. Scale bar 5 0. 2 mm. (2) Antennae. Scale bar 5 0. 2 mm. (3) Lateral view of abdominal segments.Scale bar 5 0. 2 mm. (4) Dorsal view of thorax. Scale bar 5 0. 3 mm. (5) Ventral view of VIII and IX abdominal segments.Scale bar 5 0. 2 mm. (6) Lateral view of IX abdominal segment with aedeagus. Scale bar 5 0. 2 mm.September 2000 KATHIRITHAMBY AND MOYA-RAYGOZA: A NEW SPECIES OF STREPSIPTERA 1041Downloaded from https://academic.oup.com/aesa/article-abstract/93/5/1039/9117 by Said Business School user on 09 September 2019the brood canal opening is subrounded and thecollar is very large and extends to IV abdominalsegment. It differs from male H. acutus Bohart(1943) by the absence of the spoon-shaped III an-tennal segment, and a longer indented posteriormargin of postlumbium; a longer projection in theVIII abdominal segment, only slightly curved apexof the aedegus. It differs from female H. acutus by acephalothorax that is as long as it is broad (in H.acutus it is longer than broad) and the shape of thebrood-canal opening.The male of the new species is distinguished fromall other Halictophagus by the triangular extension onthe VIII abdominal sternite and the two long inden-tations in the posterior margin of the postnotum.AcknowledgmentsWe thank W. E. Styer for the Þeld collections and L. R.Nault for the grant to enable G.M-R to collect the materialwith W. E. Styer; and to the British Council for support inpublishing this study.References CitedBaumert,D. 1959. MehrjährigeZuchteneinheimischer Strep-sipteren. 2. Imagines, Lebenszyklus, und Artbestimmungvon Elenchus tenuicornis Kirby. Zool. Beitr. 4: 343Ð409.Bohart, R.M. 1943. Newspecies ofHalictophaguswith a keyto the genus in North America (Strepsiptera, Halictoph-agidae). Ann. Entomol. Soc. Am. 36: 341Ð359.Brailovsky, H. 1974. 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Gonatopus barletti Olmi[Hymneoptera: Dryinidae] in México: a previous unre-ported parasitoid of the corn leafhopper Dalbulus maidis(Delong & Wolcott) and the Méxican corn leafhopperDalbulus elimatus (Ball) [Homoptera: Cicadellidae].Proc. Entomol. Soc. Wash. 92: 461Ð464.Vega, F. E., P. Barbosa, and A. P. Perez. 1991. Eudorylas(Metadorylas) sp. (Diptera: Pipunculidae). a previouslyunreported parasitoid of Dulbulus maidis (Delong &Wolcott) and Dalbulus elimatus (Ball) (Homoptera: Ci-cadellidae). Can. Entomol. 123: 241Ð242.Received for publication 16 November 1999; accepted 26May 2000.1044 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 5Downloaded from https://academic.oup.com/aesa/article-abstract/93/5/1039/9117 by Said Business School user on 09 September 2019

Halictophagus naulti sp. n. (Strepsiptera: Halictophagidae), a New Species Parasitic in the Corn Leafhopper (Homoptera: Cicadellidae) from Mexico

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