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First Record of Diaphorina Citri (Hemiptera: Psyllidae) in Ecuador Infesting Urban Citrus and Orange Jasmine Trees J.F

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First Record of Diaphorina Citri (Hemiptera: Psyllidae) in Ecuador Infesting Urban Citrus and Orange Jasmine Trees J.F Journal of Insect Science RESEARCH First Record of Diaphorina citri (Hemiptera: Psyllidae) in Ecuador Infesting Urban Citrus and Orange Jasmine Trees J.F. Cornejo1 and E.J. Chica1,2 1Carrera de Ingenierı´a Agrı´cola y Biolo´gica, Escuela Superior Polite´cnica del Litoral, Campus Gustavo Galindo, Km. 30.5 vı´a perimetral, Apartado 09-01-5863, Guayaquil, Ecuador 2Corresponding author, e-mail: [email protected] Subject Editor: Todd Shelly J. Insect Sci. 14(298): 2014; DOI: 10.1093/jisesa/ieu160 ABSTRACT. Adults and nymphs of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), were collected in the Guayaquil, Samborondo´n, and Dura´n cantons in coastal Ecuador. Psyllids were found in high numbers in citrus (Citrus spp., Sapindales: Rutaceae) and orange jasmine (Murraya exotica [L.] Jack, Sapindales: Rutaceae) trees within the Guayaquil-Samborondon-Duran conur- bation; however, none was found during scoutings in the main citrus producing areas in coastal Ecuador. To the best of our knowledge, this is the first report of D. citri in Ecuador and the Pacific coastal plain of South America. Key Words: Asian citrus psyllid, citrus, Huanglongbing The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Results Psyllidae), is present in tropical and subtropical regions of Asia, the Psyllids were found in high numbers in the conurbation formed by middle-east and the Americas. The host range of D. citri is limited to the cities of Guayaquil, Samborondo´n, and Dura´n. No psyllids were several members of the Rutaceae family, including all commercial cit- found in the main citrus producing regions of Ecuador located in rus species (Halbert and Manjunath 2004). In their nymph and adult western slopes of the Andes and the Portoviejo, and Chone cantons stages, D. citri alone could be considered only a minor pest of commer- (Fig. 1). The first finding of D. citri occurred on 20 January 2013, cial citrus, however, D. citri is a vector for the three bacteria when numerous adults and nymphs were found in a M. exotica tree (‘Candidatus Liberibacter asiaticus’, ‘Candidatus Liberibacter growing along a sidewalk in Guayaquil (210028.1600S, americanus’, and ‘Candidatus Liberibacter africanus’) that cause the 7953054.3100W). After this finding, Agrocalidad, the national plant devastating Huanglongbing (HLB) disease in citrus (Bove´ 2006). protection and quarantine authority was alerted to confirm the identity Currently, HLB is the most serious threat to citriculture worldwide, and of the psyllids. As of November 2013, the range of D. citri remained because there is no known cure for HLB, control of the disease spread restricted to the Guayaquil-Samborondo´n-Dura´n conurbation without is mostly conducted through controlling D. citri populations and change in the level of infestation within the city. The identity of the using certified pathogen-free planting material. In America, D. citri is collected specimens was confirmed to be D. citri by Agrocalidad, present in the southern United States (USDA 2010), the Caribbean originally determined by Dr. Susan Halbert, Florida Department basin and central Ame´rica (Burckhardt and Martı´nez 1989, of Agriculture and Consumer Services, Gainesville, FL, USA Halbert and Nu´n˜ez 2004, Villalobos et al. 2005), most of the countries (Florida State Collection of Arthropods number E2013-882). in the Atlantic and Caribbean coast of South America (Da Costa In Guayaquil, Samborondo´n and Dura´n, D. citri was distributed Lima 1942, Cermeli et al. 2000, Augier et al. 2006) and the Andean widely with adults present in 61 out of the 80 trees sampled on these region of Colombia (ICA 2012). Neither HLB or D. citri have been locations. The number of adults per tree ranged from 7 to more than reported in the Pacific coastal plains of South America where most of 50 (Fig. 2). Both leaves and psyllids tested negative for HLB-causing the commercial citrus production of Ecuador, Peru, and Chile is bacteria by PCR. located. Materials and Methods Discussion A survey for HLB symptoms and D. citri was conducted from July We report for the first time the presence of D. citri in Ecuador. 2012 to May 2013 in the coastal plains of Ecuador. In total, 26 locations D. citri is a vector for the bacteria that cause HLB disease in citrus, cur- were visited. These locations were cities, towns, and citrus farms lo- rently a major threat for worldwide citriculture. D. citri was found only cated in the outskirts of these cities/towns. Psyllids were sampled strik- in the conurbation formed by the cities of Guayaquil, Samborondo´n, ing a branch (four branches per tree) of citrus (Citrus spp., Sapindales: and Dura´n in ornamental and domestic citrus and orange jasmine trees. Rutaceae) or orange jasmine (Murraya exotica [L.] Jack, Sapindales: The absence of psyllids in citrus producing areas 80–120 km away Rutaceae) trees over a white sheet of paper and examining whether from these cities as well as in the city of Milagro ( 30 km northeast), adults or nymphs fell from the struck branch. About 1,500 citrus/orange where orange jasmine is grown commercially, suggests that D. citri was jasmine trees from the 26 locations were sampled during the survey. introduced to Guayaquil. The widespread distribution of D. citri in When psyllids were found, a sample of at least 25 psyllids was collected Guayaquil-Samborondo´n-Dura´n and the relatively sparse distribution using a brush and conserved in ethanol. The collected psyllids and of potential D. citri hosts within these cities suggest that the dispersal of leaves from all locations were tested for HLB-causing bacteria by poly- the psyllids within these cities was aided by human movement of host merase chain reaction (PCR) as in Li et al. (2007). plants and/or transporting of municipal pruning debris from parks and VC The Author 2014. Published by Oxford University Press on behalf of the Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 JOURNAL OF INSECT SCIENCE VOLUME 14 Fig. 1. Distribution of Diaphorina citri in coastal Ecuador (July 2012 to May 2013). Circles represent the localities surveyed, gray circles mark places were Diaphorina citri adults were collected. Shaded areas represent the major citrus producing cantons in Ecuador. this rate was about three times faster (Halbert et al. 2008), suggesting that areas where M. exotica and citrus are commercially grown in Ecuador could be reached by D. citri in a relatively short time. Due to climatic conditions, irregular year-round flushing and deficient crop management practices, D. citri could become established and thrive in the citrus producing regions of Ecuador, increasing the risk of a rapid dissemination of HLB if infected material reaches the country. The presence of D. citri in the Guayaquil area also poses a threat for the Peruvian lemon and lime industries located in Northern Peru near the border with Ecuador, about 260 km south of Guayaquil. Continuous monitoring of populations and surveying are currently being conducted in Guayaquil-Samborondo´n-Dura´n and the main citrus producing regions. Acknowledgments We thank Imelda Fe´lix (Agrocalidad) for key exchanges of ideas during our survey and Marı´a Fernanda Ratti (CIBE) for her technical assistance during the PCR tests. We also thank Agrocalidad for their collaboration in the identification of the specimens collected and Centro de Investigaciones Biotecnolo´gicas del Ecuador (CIBE) at the Escuela Superior Polite´cnica del Litoral for its contribution to conduct Fig. 2. Histogram of the number of adult psyllids per tree in citrus the PCR tests. and Murraya exotica trees sampled in the Guayaquil-Samborondo´n- Dura´n conurbation between January and May 2013. Reference Cited Augier, L., G. Gastaminza, M. Lizondo, M. Argan˜araz, and E. Willink. medians. One year after the first finding of D. citri in Guayaquil, its 2006. Presencia de Diaphorina citri (Hemiptera: Psyllidae) en el Noroeste Argentino (NOA). Revista de la Sociedad Entomolo´gica Argentina 65: distribution remained restricted to the Guayaquil-Samborondo´n-Dura´n 67–68. conurbation. In Brazil, the range of D. citri increased at a rate of ap- Bove´, J. M. 2006. Huanglongbing: A destructive, newly-emerging, century-old proximately 20 km per year (Gottwald et al. 2007), whereas in Florida disease of citrus. J. Plant Pathol. 88: 7–37. 2014 CORNEJO AND CHICA: FIRST RECORD OF DIAPHORINA CITRI IN ECUADOR 3 Burckhardt, D., and M. Martinez. 1989. Note sur la pre´sence su Honduras Proceedings International. Research Conference on Huanglongbing. Plant d’un redoutable ennemi de`s citrus: Diaphorina citri Kuwayama [Hom. Management Network, December 2008, Orlando. (http://www.plantmanage Psylloidea Psyllidae]. Bull. Soc. Entomol. France 94: 65–66. mentnetwork.org/proceedings/irchlb/2008/presentations/IRCHLB.2.6.pdf) Cermeli, M., P. Morales, and F. Godoy. 2000. Presencia del psı´lido asia´tico de (accessed 31 October 2014). los cı´tricos Diaphorina citri Kuwayama (Hemiptera: Psyllidae) en ICA. 2012. Vigilancia oficial del psı´lido asia´tico de los cı´tricos, Diaphorina Venezuela. Bol. Entomol. Venez. 15: 235–243. citri Kuwayama (Hemiptera: Psyllidae) en Colombia. (http://www.ica.gov. Da Costa Lima, A. M. 1942. Insetos do Brazil: Homopteros. Escola Nacional co/Areas/Agricola/Servicios/Epidemiologia-agricola/HUANGLONGBING/ de Agronomı´a, Officinas de Obras do Jornal do Comercio, Rio de Janeiro, BOL_HLB_DIC_21_2012.aspx) (accessed 31 October 2014). Brasil. Li, W., J. S. Hartung, and L. Levy. 2007. Evaluation of DNA amplification Gottwald, T. R., J. V. Da Grac¸a, and R.
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