Abstract
Xylella fastidiosa Wells et al. is a xylem-borne bacterium that causes some of the most important plant diseases to woody plants such as citrus, olives, almonds and other cultures. This pathogen is mainly transmitted by sharpshooters, among which the tribe Cicadellini (Cicadellinae) includes the largest number of proven vectors. The correct identification of the vectors, along with biological and phenological information, are necessary to identify the key vectors involved in the spread of the bacterium and, consequently, establish control strategies and evaluate risks at a local or regional scale. However, lack of information on the Cicadellini from Argentina has delayed the implementation of control measures. Based on surveys conducted in the main citrus producing areas along with bibliographic data, this contribution provides the first list of Cicadellini species from Argentina that are potential vectors of X. fastidiosa; an identification key to these sharpshooters is provided. Twelve species were recorded from northeastern citrus groves, while from northwestern orchards, with previous information totally absent, 10 species were recorded. Eight species are shared by all producing regions, and five of them are proven vectors of X. fastidiosa (Bucephalogonia xanthophis (Berg), Dilobopterus costalimai Young, Macugonalia cavifrons (Stål), M. leucomelas (Walker), Sonesimia grossa (Signoret)). This contribution provides 22 new insect-plant relationships, information on their natural enemies, the geographic distribution of all species is broadened and the female genitalia of three proven vectors are described for the first time.
References
Bucci, E.M. (2018) Xylella fastidiosa, a new plant pathogen that threatens global farming: Ecology, molecular biology, search for remedies. Biochemical and Biophysical Research Communications, 502, 173–182. https://doi.org/10.1016/j.bbrc.2018.05.073
Carvalho, R., Lopes, M. & Rodrigues, L.G.N. (2015) Espécies de cigarrinhas em cultivo de café no município de Santa Teresa, Espírito Eanto, Brasil (Hemiptera, Cicadellidae, Cicadellinae). Papeis Avulsos de Zoologia, 55, 205–210. https://doi.org/10.1590/0031-1049.2015.55.13
Costa, N., Plata, M.I., Garrán, S.M. & Mika, R. (2009) XIII Jornadas Fitosanitarias Argentinas. s.n., Santiago del Estero, E021 pp.
De Coll, O., Remes Lenicov, A.M.M., Agostini, J. & Paradell, S. (2000) Insect Transmitted Procaryotes. Proceeding of the 14th Internacional Organization Citrus Virologists Conference (IOCV), Argentina, 2000, 216–222.
Defea, B. (2018) Biodiversidad de Cicadellini en las regiones norte y centro de la Argentina (Hemiptera: Cicadellidae). Tesis Doctoral, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, 295 pp.
Defea, B., Paradell, S. & Remes Lenicov, A.M.M. de (2017) The genus Plesiommata Provancher (Hemiptera: Cicadellidae) in Argentina. First detailed description of the female genitalia and comparisons with its Neotropical congeners. Austral Entomology, 55, 1–6. https://doi.org/10.1111/aen.12211
Dellapé, G. (2013) Cicadelinos potenciales vectores de patógenos en cultivos citrícolas del NE argentino. Estudios taxonómicos y moleculares (Insecta: Hemiptera: Cicadellidae). Tesis Doctoral, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, 227 pp. https://doi.org/10.35537/10915/31796
Dellapé, G., Bouvet, J.P. & Paradell, S. (2013) Diversity of Cicadomorpha (Hemiptera: Auchenorrhyncha) in Citrus Orchards in Northeastern Argentina. Florida Entomologist, 96, 1125–1134. https://doi.org/10.1653/024.096.0353
Dellapé, G. (2016) Description of the female terminalia of twelve species of Proconiini and a key to genera from Argentina. Zootaxa, 4117 (2), 211–225. https://doi.org/10.11646/zootaxa.4117.2.5
Dellapé, G., Paradell, S., Delfederico, L. & Semorile, L. (2016) The potential vectors of Xylella fastidiosa from Argentina: a study of leafhoppers and treehoppers (Hemiptera: Auchenorrhyncha) on citrus agroecosystems. Entomologia Experimentalis et Applicata, 2016, 1–12.
Froza, J.A. (2017) Levantamento de espécies de cigarrinhas (Hemiptera: Auchenorrhyncha) com ênfase em possíveis vetores de Xylella fastidiosa em pomares de oliveira na Serra da Mantiqueira. Mestra em Ciências. Área de concentração: Entomologia. Universidade de São Paulo Escola Superior de Agricultura “Luiz de Queiroz”, Piracicaba, 91 pp.
Fundecitrus (1999) Descobertos mais seis vetores de CVC. Revista Brasileira de Fruticultura, 94, 8–9. Available from: http://www.fundecitrus.com.br (access 20 December 2021)
Garita-Cambronero, J., Villalobos, W., Godoy, C. & Rivera, C. (2008). Diversidad de cicadélidos y clastoptéridos (Hemiptera) en tres zonas productoras de café afectadas por Xylella fastidiosa Wells et al. en Costa Rica. Neotropical Entomology. 37(4), 436–448.
Giustolin, T.A, Lopes, J.R.S., Querino, R.B., Cavichioli, R., Zanol, K., Azevedo-Fihlo, W. & Mendes, M. (2009) Diversidade de Hemiptera Auchenorrhyncha em citros, café e fragmento de floresta nativa do Estado de São Paulo. Neotropical Entomology, 38, 834–841. https://doi.org/10.1590/S1519-566X2009000600018
Haelterman, R.M., Tolocka, P.A., Roca, M.E., Guzmán, F.A., Fernández, F.D. & Otero, M.L. (2015) First presumptive diagnosis of Xylella fastidiosa causing Olive scorch in Argentina. Journal of Plant Pathology, 97 (2), 393. https://doi.org/104454/JPP.V97I2.023
Hickel, E., Jean-pierre, H., Ducroquet, H., Leite-junior, R. & Leite, R.M.V.B.C. (2001) Fauna de Homoptera: Auchenorrhyncha em pomares de ameixeira em Santa Catarina. Neotropical Entomology, 30, 725–729. https://doi.org/10.1590/S1519-566X2001000400032
Hill, B.G. (1970) Comparative morphological study of selected higher categories of leafhoppers (Homoptera: Cicadellidae). PhD thesis in Entomology, North Carolina State University, Raleigh, 186 pp.
Janse, J., Obradovic, A. (2010) Xylella fastidiosa: its biology, diagnosis, control and risks. European Journal of Plant Pathology, 92, 35–48. https://doi.org/10.4454/jpp.v92i1sup.2504
Krewer, G., Dutcher, J.D. & Chang, C.J. (2002) Imidacloprid 2F insecticide slow development of Pierce’s disease brunch grapes. Journal of Entomological Science, 37, 101–112. https://doi.org/10.18474/0749-8004-37.1.101
Leal, A. H., Creão-Duarte, A. J., & Mejdalani, G. (2016) Taxonomic review of Scopogonalia Young, 1977(Insecta: Hemiptera: Cicadellidae: Cicadellini) with description of six new species. Journal of Natural History. http://dx.doi.org/10.1080/00222933.2016.1166530.
Leite, R. & Nunes, L. (2003) Avanços nas pesquisas sobre Xylella fastidiosa do café no Brasil. In: Zambolim, L. (Ed.), Produção integrada de café. DFP, Viçosa, pp. 87–101.
Lopes, J.R.S., Daugherty, M.P. & Almeida, R.P. (2009) Context-dependent transmission of a generalist plant pathogen: host species and pathogen strain mediate insect vector competence. Entomologia Experimentalis et Applicata, 131, 216–224. https://doi.org/10.1111/j.1570-7458.2009.00847.x
Lopes, J.R.S. (2017) European Conference on Xylella fastidiosa 2017: finding answers to a global problem. Available from: https://www.efsa.europa.eu/sites/default/files/event/171113/171113-5.1_Lopes.pdf (accessed 15 November 2021)
Lopes, J.R.S. & Froza J.A. (2021) 3rd European Conference on Xylella fastidiosa and XF-ACTORS final meeting. Available from: https://www.efsa.europa.eu/es/events/event/3rd-european-conference-xylella-fastidiosa-and-xf-actors-final-meeting (accessed 30 December 2021)
Lozada P. (2010) Neotropical Cicadellinae (Hemiptera: Cicadellidae) in the Staatliches Museum für Naturkunde Stuttgart. Stuttgarter Beiträge zur Naturkunde A, (3), 103–110.
Luft Albarracin, E., Triapitsyn S.V. & Virla E.G. (2009) Annotated key to the genera of Mymaridae (Hymenoptera: Chalcidoidea) in Argentina. Zootaxa, 2129, 1–28. https://doi.org/10.11646/zootaxa.2129.1.1
Marucci, R.C., Giustolin, T.A., Miranda, M.P., Ferraz, P.C. & Lopes, J.R.S. (2001). Sharpshooter transmission of a coffee strain of Xylella fastidiosa to coffee seedlings. Fitopatologia Brasileira. 26, 277.
Marucci, R., Giustolin, T., Miranda, M., Miquelote, H., Almeida, R.P. & Lopes, J.R.S. (2003) Identification of a non-host plant of Xylella fastidiosa to rear healthy sharpshooter vectors. Scientia Agrícola, 60, 669–675. https://doi.org/10.1590/S0103-90162003000400010
Marucci, R., Lopes, J.R.S., Vendramim, J. & Corrente, J.E. (2004) Feeding site preference of Dilobopterus costalimai Young and Oncometopia facialis (Signoret) (Hemiptera: Cicadellidae) on citrus plants. Neotropical Entomology, 33, 759–768. https://doi.org/10.1590/S1519-566X2004000600014
Marucci, R., Lopes, J.R.S. & Cavichioli, R.R. (2008) Transmission Efficiency of Xylella fastidiosa by Sharpshooters (Hemiptera: Cicadellidae) in Coffee and Citrus. Journal of Economic Entomology, 101, 1114–1121. https://doi.org/10.1603/0022-0493(2008)101[1114:TEOXFB]2.0.CO;2
Mckamey, S.H. (2007) Taxonomic catalogue of the leafhoppers (Membracoidea). Part 1. Cicadellinae. American Entomological Institute, 78, 1–394.
Medler, J.T (1963) A Review of the genus Erythrogonia Melichar (Homoptera, Cicadellidae). Miscellaneous Publications of the Entomological Society of America, 4, 1–33.
Mejdalani, G. (1998) Morfologia externa dos Cicadellinae (Homoptera, Cicadellidae): comparacao entre Versigonalia ruficauda (Walker) (Cicadellini) e Tretogonia cribrata Melichar (Proconiini), com notas sobre outras especies e analise da terminologia. Revista Brasileira de Zoología, 15, 451–544. https://doi.org/10.1590/S0101-81751998000200015
Menegatti, A.C.O., Garcia, F. R. M. & Savaris, M. (2008) Análise faunística e flutuação populacional de cigarrinhas (Hemiptera, Cicadellidae) em pomar cítrico no município de Chapecó, Santa Catarina. Biotemas, 21 (1), 53–58.
Milanez, J., Parra, J. & Magri, D. (2001) Alternation of host plants as a survival mechanism of leafhoppers Dilobopterus costalimai and Oncometopia facialis (Hemiptera: Cicadellidae), vectors of the citrus variegated chlorosis (CVC). Scientia Agrícola, 58, 699–702. https://doi.org/10.1590/S0103-90162001000400008
Molina, R.O., Nunes W. M. C., Gonçalves, A.M.O., Corazza-Nunes, M.J., Zanutto, C. A., Yamamoto, A.Y. & Vargas, R.G. (2006) Ocorrência de cigarrinhas vetoras de Xylella fasidiosa em pomares cítricos do município de Loanda, no noroeste do Paraná. Laranja, 27, 243–250. https://doi.org/10.1590/S1516-89132010000300007
Morrone, J.J. (2001) Biogeografía de América Latina y el Caribe. Manuales y Tesis SEA, Zaragoza, 3, 1–148 pp.
Morrone, J.J. (2006) Biogeographic areas and transition zones of Latin America and the Caribbean islands based on panbiogeographic and cladistic. Analyses of the entomofauna. Annual Review of Entomology, 51, 467–494. https://doi.org/10.1146/annurev.ento.50.071803.130447
Navarro, F., Cuezzo, F., Goloboff, P., Szumik, C., Lizarralde de Grosso, M. & Quintana, M. (2009) Can insect data be used to infer areas of endemism? An example from the Yungas of Argentina. Revista Chilena de Historia Natural, 82, 507–522. https://doi.org/10.4067/S0716-078X2009000400006
Naumann, M. (2006) Atlas del gran chaco sudamericano. Sociedad Alemana de cooperación técnica (gtz). Erregé & asoc., Buenos Aires, 92 pp.
Nielson, M. (1965) A revision of the genus Cuerna (Homoptera, Cicadellidae). Bulletin of the US Department of Agriculture, 1318, 1–48.
Oman, P. (1949) The Nearctic leafhoppers (Homoptera: Cicadellidae). A generic classification and check list. Memoirs of the American Entomological Society, 3, 1–253.
Paradell, S. (1995) Especies argentinas de homópteros cicadélidos asociados al cultivo de maíz (Zea mays L.). Revista Facultad de Agronomía, Universidad Nacional La Plata, 71, 213–234. [http://sedici.unlp.edu.ar/handle/10915/117007]
Paradell, S.L, Virla, E.G, Logarzo, G.A. & Dellapé G. (2012) Proconiini Sharpshooters of Argentina, with notes on its distribution, host plants, and natural enemies. Journal of Insect Science, 12, 1–17. https://doi.org/10.1673/031.012.11601
Paradell, S., Defea, B., Dughetti, A., Zárate, A. & Remes Lenicov, A.M.M. de (2014a) Diversity of Auchenorrhyncha (Hemiptera: Cicadellidae: Delphacidae) associated with Vicia villosa in Southern Buenos Aires Province, Argentina. Florida Entomologist, 97, 674–684. https://doi.org/10.1653/024.097.0247
Paradell, S., Maciá, A., Asborno, M., Catalano, M., Brentassi, M.E., Varela, G., Dellapé, G., Defea, B., Foieri, A. & Marino de Remes Lenicov, A.M. (2014b) Diversity of leafhoppers (Hemiptera: Cicadellidae) in experimental rice lots and associated weeds in Buenos Aires province, Argentina. Studies on Neotropical Fauna and Environment, 49, 213–221. https://doi.org/10.1080/01650521.2014.962950
Paris, P., Tolotti, S., Peruzzo, L. & Azevedo Filho, W.S. (2012) Cigarrinhas (Cicadellidae: Cicadellinae) na cultura da canola no município de Vacaria, Rio Grande do Sul, Brasil. Cadernos de Pesquisa, 24, 14–22.
Purcell, A.H. (1989) Homopteran transmission of xylem-inhabiting bacteria. In: Purcell, A.H., Advances in disease vector research. Vol. 6. Springer, New York, pp. 243–266.
Rapicavoli, J., Ingel, B., Blanco-ulate, B., Cantu, D. & Roper, C. (2018) Xylella fastidiosa: an examination of a re-emerging plant pathogen. Molecular Plant Pathology, 19, 786–800. https://doi.org/10.1111/mpp.12585
Redak, R., Purcell, A., Lopes, J.R.S., Blua, M., Mizell, R.F. & Andersen, P. (2004) The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annual Review of Entomology, 49, 243–270. https://doi.org/10.1146/annurev.ento.49.061802.123403
Remes Lenicov, A.M.M. de, Paradell, S., Virla, E., Varela, G., Costamagna, A.C. & Mariani, R. (1997) VI Congreso Nacional de maíz. Proceedings I Sec. II Pergamino, Buenos Aires, 1997, pp. 58–69.
Remes Lenicov, A.M.M., Paradell, S., de Coll, O.R. & Agostini, J. (1999) Cicadelinos asociados a citrus afectados por Clorosis Variegada (CVC) en la República Argentina (Insecta: Homoptera: Cicadellidae). Revista Sociedad Entomológica Argentina, 58, 211–225. [https://www.biotaxa.org/RSEA/article/view/32607]
Remes Lenicov, A.M.M., Paradell, S. & Catalano, M. (2006) Hemípteros auquenorrincos perjudiciales al cultivo de sorgo en la Argentina (Insecta-Hemiptera). Revista de Investigaciones Agropecuarias INTA, 35 (2), 3–20.
Ringenberg, R. (2008) Análise faunística de cigarrinhas (Hemiptera: Cicadellidae) e flutuação populacional de potenciais vetores de Xylella fastidiosa em vinhedos nos estados do Rio Grande do Sul e Pernambuco, Brasil. Tesis doutorado, Universidade de São Paul, São Paul, 200 pp. https://doi.org/10.11606/T.11.2008.tde-24072008-125329
Saravia, R., Plata, G. & Gandarillas, A. (2014) Plagas y Enfermedades del Cultivo de Quinua. Fundación PROINPA, Cochabamba. [unknown pagination]
Severin, H.H.P. (1950) Spittle-insect vectors of Pierce’s disease virus. II. Life history and virus transmission. Hilgardia, 19, 357–382. https://doi.org/10.3733/hilg.v19n11p357
Silva, M., Meneguim, A., Paião, F.G., Meneguim, L., Canteri, M.G. & Leite, R.P. Jr. (2007) Infectividade Natural por Xylella fastidiosa Wells et al. de Cicadelíneos (Hemiptera: Cicadellidae) de Lavouras Cafeeiras do Paraná. Neotropical Entomology, 36, 274–281. https://doi.org/10.1590/S1519-566X2007000200015
Toledo, A., Virla, E., Humber, R.H., Paradell, S. & López Lastra, C. (2006) First record of Clonostachys rosea (Ascomycota: Hypocreales) as an entomopathogenic fungus of Oncometopia tucumana and Sonesimia grossa (Hemiptera: Cicadellidae) in Argentina. Journal of Invertebrate Pathology, 92, 7–10. https://doi.org/10.1016/j.jip.2005.10.005
Triapitsyn, S.V., Logarzo, G.A., De León, J.H. & Virla, E.G. (2008) A new Gonatocerus (Hymenoptera: Mymaridae) from Argentina, with taxonomic notes and molecular data on the G. tuberculifemur species complex. Zootaxa, 1949 (1), 1–29. https://doi.org/10.11646/zootaxa.1949.1.1
Young, D.A. (1968) Taxonomic study of the Cicadellinae (Homoptera: Cicadellidae), Part 1, Proconiini. Bulletin of the American Museum of Natural History, 261, 1–287. https://doi.org/10.5479/si.03629236.261.1
Young, D.A. (1977) Taxonomic study of the Cicadellinae (Homoptera: Cicadellidae). Part 2. New World Cicadellini and the genus Cicadella. Technical Bulletin of the North Carolina Agricultural Experiment Station 239, 1–1135.