Este trabajo fue realizado en dos habitats diferentes de maíz en Mexico, con el objetivo de determinar los parasitoides de huevos de dos importantes chicharritas plagas del maíz en este país. se empleó la siguiente metodología: plantas de maíz con similar número de huevos de D. maidis y D. elimatus fueron expuestos a los parasitoides. Ambas especies de chicharritas fueron parasitadas por Paracentrobia tapajosae Viggiani (Hymenoptera: Trichogrammatidae), Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Aphelinoidea semifuscipennis (Hymenoptera: Trichogrammatidae) y Pseudoligositalongifrangiata (Viggiani) (Hymenoptera: Trichogrammatidae). Todas las especies de parasitoidesque atacan a los huevos de D. elimatus son reportadas por primera vez. Además, en ambas especies de chicharritas se encontró un número similar de huevos parasitados y porcentaje de parasitismo, y los parasitoides encontrados llegaron a su estado adulto. La tasa total de parasitismo depende del tipo de hábitat; en el hábitat donde se cultiva maíz todo el año, una alta tasa de parasitismo fue encontrada, mientras que en el hábitat con maíz estacional, la tasa de parasitismo fue baja.Fil: Moya Raygoza, Gustavo. Universidad de Guadalajara; MéxicoFil: Renteria, Isabel. Universidad de Guadalajara; MéxicoFil: Luft Albarracin, Erica Beatriz. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Planta Piloto de Procesos Industriales Microbiologicos; ArgentinaFil: Virla, Eduardo Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucuman. Planta Piloto de Procesos Industriales Microbiologicos; Argentin

Luft Albarracin, Erica Beatriz

Moya Raygoza, Gustavo

Renteria, Isabel

Virla, Eduardo Gabriel

Florida Entomologist

English

Maize plants with similar numbers of Dalbulus maidis (DeLong & Wolcott) and Dalbulus elimatus (Ball) (Hemiptera: Cicadellidae) eggs were exposed to egg parasitoids in seasonal and perennial maize habitats. Both leafhopper species were parasitized by Paracentrobia tapajosae Viggiani (Hymenoptera: Trichogrammatidae), Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Aphelinoidea semifuscipennis Girault (Hymenoptera: Trichogrammatidae), and Pseudoligosita longifrangiata (Viggiani) (Hymenoptera: Trichogrammatidae). All parasitoids that attacked D. elimatus eggs are reported for the first time. Both leafhopper species showed similar number of parasitized eggs and similar percentages of parasitism. The parasitoids reached the adult stage. The levels of parasitism varied among the 2 habitats; a higher level of parasitism was observed in the perennial maize habitat compared with the seasonal maize habitat

Moya-Raygoza,  G.

Renteria C,  I.

Albarracin,  E.L.

Virla,  E.G.

Red Mexicana de Repositorios Institucionales

Egg parasitoids of the leafhoppers dalbulus maidis and dalbulus elimatus (Hemiptera: Cicadellidae) in two maize habitats

CONICET Digital

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers,academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.Egg Parasitoids of the Leafhoppers Dalbulus maidis and Dalbuluselimatus (Hemiptera: Cicadellidae) in Two Maize HabitatsAuthor(s): Gustavo Moya-Raygoza , Isabel Renteria C , Erica Luft Albarracin andEduardo G. VirlaSource: Florida Entomologist, 97(1):309-312. 2014.Published By: Florida Entomological SocietyURL: http://www.bioone.org/doi/full/10.1896/054.097.0148BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in thebiological, ecological, and environmental sciences. BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies, associations,museums, institutions, and presses.Your use of this PDF, the BioOne Web site, and all posted and associated contentindicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.Usage of BioOne content is strictly limited to personal, educational, and non-commercialuse. Commercial inquiries or rights and permissions requests should be directed to theindividual publisher as copyright holder. Scientific Notes 309EGG PARASITOIDS OF THE LEAFHOPPERS DALBULUS MAIDIS AND DALBULUS ELIMATUS (HEMIPTERA: CICADELLIDAE) IN TWO MAIZE HABITATSGustavo Moya-RayGoza¹,*, Isabel RenteRIa C¹, eRICa luft albaRRaCIn² and eduaRdo G. vIRla²¹Departamento de Botánica y Zoología, CUCBA, Universidad de Guadalajara, km 15.5 carretera Guadalajara-Nogales, Zapopan, C.P. 45110, Jalisco, Mexico²PROIMI-Biotecnologia, Div. Control Biológico, Av. Belgrano y Pje. Caseros (T4001 MVB),  San Miguel de Tucumán, Argentina*Corresponding author; E-mail: moyaraygoza@gmail.comDalbulus maidis (DeLong & Wolcott) and D. elimatus (Ball) (Hemiptera: Cicadellidae) are im-portant pest of maize (Zea mays L. ssp. mays) in Latin America. They are efficient vectors of the corn stunt spiroplasma (Spiroplasma kunkelii Whitcomb), maize bushy stunt phytoplasma (Candidatus Phytoplasma asteris), and Maize rayado fino virus (MRFV) (Nault 1980; Ebbert et al. 2001). Little is known about the natural enemies of these leafhoppers. Eggs of D. maidis are parasitized mainly by Mymaridae and Tricho-grammatidae wasps (Moya-Raygoza et al. 2012). Egg parasitoids are considered good tools for bio-logical control because they show higher parasit-ism rates than parasitoids of other leafhopper stages (Freytag 1985).It’s unknown whether egg parasitoids that at-tack D. maidis also attack D. elimatus. These sis-ter leafhopper species belong to different phyletic groups, showing differences in morphology, isoen-zymes, molecular characters, oviposition behav-ior, and allopatric distribution (Heady et al. 1985; Triplehorn & Nault 1985; Triplehorn et al. 1990; Dietrich et al. 1998). During the process of spe-ciation, D. maidis spread mainly in low (< 1,000 m asl) elevation maize habitats and D. elimatus spread mainly in high (> 1,000 m asl) elevation maize habitats (Triplehorn & Nault 1985).Previous surveys identified 6 egg parasitoid species of D. maidis in Jalisco, Mexico (Virla et al. 2009; Moya-Raygoza et al. 2012). However, no reports of D. elimatus egg parasitoids are avail-able. Moreover, little is known about levels of parasitism and the successful development of parasitoids on the 2 leafhoppers. The objective of this study was to identify the egg parasitoids and the parasitism rates of D. maidis and D. elima-tus in low and high elevation maize habitats in Jalisco, Mexico.Parasitoids were surveyed in 2 sites with con-trasting environmental conditions during the 2009 maize growing season. El Grullo (868 m asl; N 19° 47' W 104° 12') is a permanent maize habitat where maize is cultivated throughout the year. By contrast in Zapopan (1,650 m asl; N 20° 74' W 103° 30') maize is cultivated during the Jun through Sep-Oct season, which is characterized by high rainfall and high temperatures (Larsen et al. 1992). The experiments were conducted in pes-ticide-free cornfields at each of the 2 sites during the 2009 maize growing season. The presence of D. maidis and D. elimatus adults was confirmed at each sampling date by using a heavy sweep net (38 cm diam net ring) for 20 m over the foliage of maize; adult leafhoppers were identified using the taxonomic keys by Triplehorn & Nault (1985).Laboratory-reared, 2-week-old females of each Dalbulus species were allowed to oviposit on pot-ted ancho-pozolero maize plants at the 3 leaf stage. Five females of each Dalbulus species were confined separately in a leaf-cage for 72 h under laboratory conditions (25 ± 2 °C; 50% RH; 12:12 h L:D). The leaf-cage size was (4.0 × 5.5 × 2.0 cm with a small hole covered with fine mesh). After the oviposition period, the adult females were re-moved, the numbers of eggs on each maize leaf were counted, and the plants were immediately transported to the field sites. The transportation time to Zapopan was approximately 1 h and to El Grullo 3 h. A potted plant with eggs was consid-ered a single replicate. On each sampling date 20 plants per Dalbulus species were placed along the edge of one 1.5-2 ha cornfield in each site. New plants with fresh leafhopper eggs were exposed in each site on 29 Jun, 23 Jul, 20 Aug, and 12 Sep. The plants were placed in pairs, each pair having 1 plant infested separately with eggs of each of the Dalbulus species. The distance between each pair of plants was 5 m. The eggs were exposed to parasitoids in the cornfields for 4 days. Then the plants were retrieved and taken to the labora-tory, where the sections of the leaves with the egg masses were cut and transferred to Petri dishes lined with wet tissue paper. The dishes were cov-ered with clear plastic food wrap to avoid desic-cation and prevent the wasps from escaping. The egg masses were checked daily until emergence of leafhopper nymphs and/or adult wasps. The time from oviposition to egg-hatch at the local temper-ature is approximately 14-15 days (Nault 1990). Adult parasitoids were counted and preserved in 95% ethanol. The numbers of exposed and para-310 Florida Entomologist 97(1) March 2014sitized eggs of D. maidis and D. elimatus were compared using chi square goodness of fit tests. The levels of parasitism between Dalbulus spe-cies and habitats were compared using a Krus-kal-Wallis test and SPSS software (SPSS 11.5 for Windows, SPSS, Chicago, Illinois, USA).The parasitoids were identified using the keys by Triapitsyn (1999 & 2002) and Viggiani (1981), and by comparison with type specimens. Vouch-er specimens were deposited in the entomologi-cal collection of the University of Guadalajara, Mexico, and in the entomological collection of the Instituto y Fundación “Miguel Lillo”, San Miguel de Tucumán, Argentina (IMLA).Dalbulus maidis eggs were parasitized by Paracentrobia tapajosae Viggiani (Hymenoptera: Trichogrammatidae), Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Aphelinoi-dea semifuscipennis Girault (Hymenoptera: Trichogrammatidae) Girault, Pseudoligosita longifrangiata (Viggiani) (Hymenoptera: Tricho-grammatidae), and Oligosita desantisi Viggiani (Hymenoptera: Trichogrammatidae) in El Grullo site, and by P. tapajosae, P. longifrangiata, and A. breviphragma in the Zapopan site (Table 1). This is the first report of O. desantisi attacking D. maidis eggs in Mexico. In previous studies in the same sites the following parasitoids were found attacking D. maidis eggs: A. breviphrag-ma, A. semifuscipennis, Oligosita clarimaculosa (Girault), P. tapajosae, Polynema saga (Girault), and P. longifrangiata in El Grullo and A. brevi-phragma, A. semifuscipennis, O. clarimaculosa, and P. tapajosae in Zapopan (Virla et al. 2009; Moya-Raygoza et al. 2012).This is the first report of parasitoids attacking D. elimatus eggs. Eggs of D. elimatus were para-sitized by P. tapajosae, A. semifuscipennis, and P. longifrangiata in El Grullo and by P. tapajosae and A. breviphragma in Zapopan (Table 1).No evidence of host specificity was observed in the parasitoids as most species parasitized both D. maidis and D. elimatus. No significant differ-ences in the total number (c² = 0.97; df = 1; P = 0.32) and the percentages of (c² = 0.001; df = 1; P = 1.00) parasitized eggs of D. maidis and D. eli-matus were observed. All parasitoids developed and reached the adult stage on D. maidis and D. elimatus (Table 1). The overall parasitism level was higher for both D. maidis and D. elimatus in the permanent maize habitat (El Grullo), com-pared with seasonal maize habitat (Zapopan) (H= 40.48; df = 1; P = 0.001) (Fig. 1). Landis & Me-nalled (1998) and Landis et al. (2000) also found high levels of parasitism in permanent habitats attributed to the stability and higher diversity of these habitats. Results of this study are consis-tent with previous studies (Moya-Raygoza et al. 2012) showing low parasitism in D. maidis dur-ing 2 summer seasons in seasonal maize habitat, where parasitoids are exposed to more variable table 1. eGG paRasItoId speCIes of Dalbulus maiDis and Dalbulus elimatus In peRennIal and seasonal MaIze habItats. total nuMbeR of eMeRGed adult paRasItoIds aRe shown In paRenthesIs.Permanent maize habitat (El Grullo)Seasonal maize habitat (Zapopan)D. maidisD. elimatusD. maidisD. elimatusCollection dateNot sampledP. tapajosae (1)P. tapajosae (4) JuneP. longifrangiata (2)P. tapajosae (51) P. tapajosae (15) Not found JulyA. breviphragma (1)A. semifuscipennis (8) A.semifuscipennis (7) A. breviphragma (26) A.breviphragma(19) August P. tapajosae (20) P. tapajosae (26)P. tapajosae (132) P. tapajosae (100) P. tapajosae (14) P. tapajosae (13) SeptemberA. semifuscipennis (1) A. semifuscipennis (2) A. breviphragma (2) A. breviphragma (13)P. longifrangiata (3) P. longifrangiata (1)O. desantisi (1) Scientific Notes 311environmental conditions. A similar pattern of parasitism was found not only for D. maidis but also for D. elimatus. More studies to determine the specific abiotic factors that influence the par-asitism rates in permanent and seasonal maize habitats are needed.The research was supported by the Univer-sity of Guadalajara (Project P3e 2009; G. Moya-Raygoza) and by the scientific and technological cooperative agreement (no 0710) between Mexico (CONACYT) and Argentina (MINCYT).suMMaRyMaize plants with similar numbers of Dalbu-lus maidis (DeLong & Wolcott) and Dalbulus eli-matus (Ball) (Hemiptera: Cicadellidae) eggs were exposed to egg parasitoids in seasonal and peren-nial maize habitats. Both leafhopper species were parasitized by Paracentrobia tapajosae Viggiani (Hymenoptera: Trichogrammatidae), Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Aphelinoidea semifuscipennis Girault (Hymenop-tera: Trichogrammatidae), and Pseudoligosita longifrangiata (Viggiani) (Hymenoptera: Tricho-grammatidae). All parasitoids that attacked D. elimatus eggs are reported for the first time. Both leafhopper species showed similar number of par-asitized eggs and similar percentages of parasit-ism. The parasitoids reached the adult stage. The levels of parasitism varied among the 2 habitats; a higher level of parasitism was observed in the perennial maize habitat compared with the sea-sonal maize habitat.Key words: maize pests, egg parasitoids, leaf-hoppersResuMenPlantas de maíz con similar número de hue-vos de D. maidis y D. elimatus fueron expuestos a los parasitoides. Ambas especies de chicharritas fueron parasitadas por Paracentrobia tapajosae Viggiani (Hymenoptera: Trichogrammatidae), Anagrus breviphragma Soyka (Hymenoptera: Mymaridae), Aphelinoidea semifuscipennis (Hy-menoptera: Trichogrammatidae) y Pseudoligosita longifrangiata (Viggiani) (Hymenoptera: Tricho-grammatidae). Todas las especies de parasitoi-des que atacan a los huevos de D. elimatus son reportadas por primera vez. Además, en ambas especies de chicharritas se encontró un número similar de huevos parasitados y porcentaje de pa-rasitismo, y los parasitoides encontrados llegaron a su estado adulto. La tasa total de parasitismo depende del tipo de hábitat; en el hábitat donde se cultiva maíz todo el año, una alta tasa de pa-rasitismo fue encontrada, mientras que en el há-bitat con maíz estacional, la tasa de parasitismo fue baja.Pabras Clave: maize pests, egg parasitoids, leafhoppersRefeRenCes CIteddIetRICh, C. h., fItzGeRald, s. J., holMes, J. l., blaCk Iv, w. C., and nault, l. R. 1998. Reassess-ment of Dalbulus leafhopper (Homoptera: Cicadel-lidae) phylogeny based on mitochondrial DNA se-quences. Ann. Entomol. Soc. America 91: 590-597.ebbeRt, M. a., JeffeRs, d. p., haRRIson, n. a., and nault, l. R. 2001. Lack of specificity in the interac-tion between two maize stunting pathogens and field collected Dalbulus leafhoppers. Entomol. Exp. Appl. 101: 49-57.fReytaG, p. h. 1985. The insect parasites of leafhop-pers, and related groups, pp. 423-467 In L. R. Nault and J. G. Rodriquez [eds.], The Leafhoppers and Planthoppers. John Wiley and Sons Inc., New York, USA.heady, s. e., Madden, l. v., and nault, l. R. 1985. Oviposition behavior of Dalbulus leafhoppers (Ho-moptera: Cicadellidae). Ann. Entomol. Soc. America 78: 723-727.landIs, d., and Menalled, f. 1998. Ecological consid-erations in conservation of parasitoids in agricul-tural landscapes, pp. 101-121 In P. Barbosa [ed.], Fig. 1. Mean percentage of parasitism of Dalbulus maidis and Dalbulus elimatus eggs in a perennial maize habitat (El Grullo) and a seasonal maize habitat (Zapo-pan) in Jalisco, Mexico, during the 2009 maize growing season. Error bars represent the standard error. N.S. = not sampled.312 Florida Entomologist 97(1) March 2014Conservation Biological Control. Academic Press, San Diego, California, USA.landIs, d., stephen, d. w., and GuRR, G. M. 2000. Habitat management to conserve natural enemies of Arthropods pests in Agriculture. Annu. Rev. Ento-mol. 45: 175-201.laRsen, k. J, nault, l. R., and Moya-RayGoza, G. 1992. Overwintering biology of Dalbulus leafhoppers (Homoptera: Cicadellidae): Adult populations and drought hardiness. Environ. Entomol. 21: 566- 577.Moya-RayGoza, G., luft albaRRaCIn, e., and vIRla, e. G. 2012. Diversity of egg parasitoids attacking Dalbulus maidis (Hemiptera: Cicadellida) popula-tions at low and high elevations sites in Mexico and Argentina. Florida Entomol. 95: 105-112.nault, l. R. 1980. Maize bushy stunt and corn stunt: A comparison of disease symptoms, pathogen host range, and vectors. Phytopathology 70: 659-662.nault, l. R. 1990. Evolution of an insect pest: maize and the corn leafhopper, a case study. Maydica 35: 165-175.tRIapItsyn, s. v. 1999. A review of the species of Anagrus Haliday, 1833 (Hymenoptera: Mymaridae) collected by A. A. Obloblin in Argentina. Russian En-tomol. J. 8: 213-222.tRIapItsyn, s. v. 2002. Descriptive notes on a new and other little know species of Anagrus Haliday, 1833 (Hymenoptera: Mymaridae) from the new world tropics and subtropics. Entomotropica 17: 213-223.tRIplehoRn, b. w., and nault, l. R. 1985. Phylogenet-ic classification of the genus Dalbulus (Homoptera: Cicadellidae), and notes of the phylogeny of the Mac-rostelini. Ann. Entomol. Soc. America 78: 291-315.tRIplehoRn, b. w., shaMbauGh, G. f., haMIlton, d. f., and nault, l. R. 1990. Isoenzyme analisis of the genus Dalbulus (Homoptera: Cicadellidae). Ann. En-tomol. Soc. America 83: 694-704.vIGGIanI, G. 1981. Nearctic and Neotropical species of Oligosita Walker (Hymenoptera: Trichogramma-tidae). Boll. Lab. Entomol. Agraria Filippo Silvestri 38: 101-118.vIRla, e. G., luft albaRRaCIn, e., and Moya-Ray-Goza, G. 2009. Egg Parasitoids of Dalbulus maidis (Hemiptera: Cicadellidae) in Jalisco State, Mexico. Florida Entomol. 92: 508-510.

Egg Parasitoids of the Leafhoppers Dalbulus maidis and Dalbulus elimatus (Hemiptera: Cicadellidae) in Two Maize Habitats

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Egg Parasitoids of the Leafhoppers Dalbulus maidis and Dalbulus elimatus (Hemiptera: Cicadellidae) in Two Maize Habitats

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