First record of Diaphorina citri (Hemiptera: Psyllidae) in Ecuador infesting urban citrus and orange jasmine trees.

Adults and nymphs of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), were collected in the Guayaquil, Samborondón, and Durán 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 conurbation; 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.

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is present in tropical and subtropical regions of Asia, the middle-east and the Americas. The host range of D. citri is limited to several members of the Rutaceae family, including all commercial citrus species ( Halbert and Manjunath 2004 ). In their nymph and adult stages, D. citri alone could be considered only a minor pest of commercial citrus, however, D. citri is a vector for the three bacteria (‘ Candidatus Liberibacter asiaticus’, ‘ Candidatus Liberibacter americanus’, and ‘ Candidatus Liberibacter africanus’) that cause the devastating Huanglongbing (HLB) disease in citrus ( Bové 2006 ). Currently, HLB is the most serious threat to citriculture worldwide, and because there is no known cure for HLB, control of the disease spread is mostly conducted through controlling D. citri populations and using certified pathogen-free planting material. In America, D. citri is present in the southern United States ( USDA 2010 ), the Caribbean basin and central América ( Burckhardt and Martínez 1989 , Halbert and Núñez 2004 , Villalobos et al ), most of the countries in the Atlantic and Caribbean coast of South America ( Da Costa Lima 1942 , Cermeli et al , Augier et al ) and the Andean region of Colombia ( ICA 2012 ). Neither HLB or D. citri have been reported in the Pacific coastal plains of South America where most of the commercial citrus production of Ecuador, Peru, and Chile is located.

Materials and Methods

A survey for HLB symptoms and D. citri was conducted from July 2012 to May 2013 in the coastal plains of Ecuador. In total, 26 locations were visited. These locations were cities, towns, and citrus farms located in the outskirts of these cities/towns. Psyllids were sampled striking a branch (four branches per tree) of citrus ( Citrus spp., Sapindales: Rutaceae) or orange jasmine ( Murraya exotica [L.] Jack, Sapindales: Rutaceae) trees over a white sheet of paper and examining whether adults or nymphs fell from the struck branch. About 1,500 citrus/orange jasmine trees from the 26 locations were sampled during the survey. When psyllids were found, a sample of at least 25 psyllids was collected using a brush and conserved in ethanol. The collected psyllids and leaves from all locations were tested for HLB-causing bacteria by polymerase chain reaction (PCR) as in Li et al. (2007) .

Results

Psyllids were found in high numbers in the conurbation formed by the cities of Guayaquil, Samborondón, and Durán. No psyllids were found in the main citrus producing regions of Ecuador located in western slopes of the Andes and the Portoviejo, and Chone cantons ( Fig. 1 ). The first finding of D. citri occurred on 20 January 2013, when numerous adults and nymphs were found in a M. exotica tree growing along a sidewalk in Guayaquil (2°10′28.16″S, 79°53′54.31″W). After this finding, Agrocalidad, the national plant protection and quarantine authority was alerted to confirm the identity of the psyllids. As of November 2013, the range of D. citri remained restricted to the Guayaquil-Samborondón-Durán conurbation without change in the level of infestation within the city. The identity of the collected specimens was confirmed to be D. citri by Agrocalidad, originally determined by Dr. Susan Halbert, Florida Department of Agriculture and Consumer Services, Gainesville, FL, USA (Florida State Collection of Arthropods number E2013-882). In Guayaquil, Samborondón and Durán, D. citri was distributed widely with adults present in 61 out of the 80 trees sampled on these locations. The number of adults per tree ranged from 7 to more than 50 ( Fig. 2 ). Both leaves and psyllids tested negative for HLB-causing bacteria by PCR.

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.

Fig. 2.

Histogram of the number of adult psyllids per tree in citrus and Murraya exotica trees sampled in the Guayaquil-Samborondón-Durán conurbation between January and May 2013.

Discussion

We report for the first time the presence of D. citri in Ecuador. D. citri is a vector for the bacteria that cause HLB disease in citrus, currently a major threat for worldwide citriculture. D. citri was found only in the conurbation formed by the cities of Guayaquil, Samborondón, and Durán in ornamental and domestic citrus and orange jasmine trees. The absence of psyllids in citrus producing areas 80–120 km away from these cities as well as in the city of Milagro ( ∼ 30 km northeast), where orange jasmine is grown commercially, suggests that D. citri was introduced to Guayaquil. The widespread distribution of D. citri in Guayaquil-Samborondón-Durán and the relatively sparse distribution of potential D. citri hosts within these cities suggest that the dispersal of the psyllids within these cities was aided by human movement of host plants and/or transporting of municipal pruning debris from parks and medians. One year after the first finding of D. citri in Guayaquil, its distribution remained restricted to the Guayaquil-Samborondón-Durán conurbation. In Brazil, the range of D. citri increased at a rate of approximately 20 km per year ( Gottwald et al. 2007 ), whereas in Florida 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-Samborondón-Durán and the main citrus producing regions.