Geographical Distribution of Schizotetranychus Hindustanicus and Associated Mites in Roraima, Brazil
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Neotrop Entomol https://doi.org/10.1007/s13744-019-00704-6 SCIENTIFIC NOTE Geographical Distribution of Schizotetranychus hindustanicus and Associated Mites in Roraima, Brazil 1 2 3 3 4 1 3 FL FIGUEIRÊDO ,EGFIDELIS ,RSPEREIRA ,JCSANTOS ,MNEGRINI ,DCOLIVEIRA ,GJMORAES 1Instituto Federal de Educação, Ciência e Tecnologia de Roraima, Boa Vista, Brasil 2Embrapa Roraima, Boa Vista, Brasil 3Escola Superior de Agricultura “Luiz de Queiroz”, Univ de São Paulo, Piracicaba, Brasil 4Univ Federal de Roraima, Boa Vista, Brasil Keywords Abstract Quarantine pest, Citrus spp., Hindustan The Hindustan citrus mite, Schizotetranychus hindustanicus Hirst (Acari: citrus mite, Amblyseius aerialis Tetranychidae), is a quarantine pest present in the state of Roraima, Correspondence Brazil. This mite, which was described in India in 1924, was reported in EG Fidelis, Embrapa Roraima, Boa 2002 in Venezuela and spread to Roraima, where it was reported in 2008, Vista, Brasil; [email protected] and to Colombia, where it was reported in 2010. Its possible spread to Edited by Pedro Takao Yamamoto – ESALQ/ other regions of Brazil is a threat to Brazilian citriculture. This study reports USP the current distribution of S. hindustanicus and potential predators of this Received 21 February 2019 and accepted 1 pest and other mites associated with citrus in Roraima. A survey was July 2019 conducted in August and September 2015 in the 15 municipalities of the state. In each municipality, orchards and citrus plants in backyards and * Sociedade Entomológica do Brasil 2019 public areas along highways and in urban areas were sampled. Samples of leaves and fruits were collected to identify the mite and its natural ene- mies. Schizotetranychus hindustanicus was found in all 15 municipalities in the state of Roraima. In total, 308 associated mites were found, with S. hindustanicus being the most abundant phytophagous mite, followed by Brevipalpus yothersi Baker. Amblyseius aerialis (Muma) was the most abundant predator, followed by Iphiseiodes zuluagai Denmark and Muma and Euseius concordis (Chant). The broad dispersal of S. hindustanicus in Roraima increases the risks of this pest reaching the main citrus-producing regions in Brazil. Introduction The characteristic sign of the incidence of S. hindustanicus is the formation of whitish erinea of 1 to 3 mm in diameter, The Hindustan citrus mite, Schizotetranychus hindustanicus forming webs on the leaves and fruits (Navia & Marsaro Jr Hirst (Acari: Tetranychidae), was described from specimens 2010). The different developmental stages of the mite, which collected from citrus trees in India in 1924 (Hirst 1924). For discolor the plant tissue while feeding, are found under these more than 80 years, this mite was known only from this webs. The erinea initially appear along the ribs on the adaxial region, where it has never been reported as a pest. In surface of leaves and then spread to the entire adaxial and 2002, this mite was reported in Venezuela (Quirós and abaxial leaf surfaces and to the surface of the fruits. The Geraud-Pouey 2002); in 2008, in Boa Vista, Roraima, Brazil attacked citrus leaves and fruits become silvery and hard- (Navia & Marsaro Jr 2010); and, in 2010, in northern ened (Quirós & Geraud-Poney 2002, Navia & Marsaro Jr Colombia (Mesa-Cobo 2010). In 2010, it was also reported 2010). in Iran (Sheikholeslam-Zadeh & Sadeghi-Nameghi 2010). In In Venezuela and Roraima, high infestations of all cases, the incidence was observed in citrus. S. hindustanicus have been observed (Quirós & Geraud- Figueirêdo et al Poney 2002, Navia & Marsaro Jr 2010), causing a reduction in Material and Methods the commercial value of the fruit due to esthetic damage, although a negative effect on fruit production cannot be A survey was conducted between August and September ruled out. In Venezuela, the mite has been reported infesting 2015 in all the 15 municipalities of the state of Roraima: Tahiti lemon, lime, tangerine, lemon, and sweet orange Alto Alegre, Amajari, Boa Vista, Bonfim, Cantá, Caracaraí, (Quirós & Dorado 2005, Nienstaedt and Marcano 2009). In Caroebe, Iracema, Mucajaí, Normandia, Pacaraima, Brazil, S. hindustanicus hasbeenobservedinTahitilemon, Rorainópolis, São João da Baliza, São Luís, and Uiramutã. Rangpur lime, Ponkan mandarin, Valencia orange, and The main citrus orchards in the main producing regions of Murcott tangor (Navia & Marsaro Jr 2010). In India, the mite each municipality were inspected. The farms sampled were also has been reported infesting coconut, acacia, neem, chi- indicated by the technicians of Secretary of Agriculture, naberry, and sorghum (Cherian 1931;Gupta&Gupta1994; Livestock and Food Supply (SEAPA-RR) of each municipality. Migeon & Dorkeld 2018). Although infestations of The area of orchards ranged from 0.5 to 10 ha, of citrus S. hindustanicus have only been observed in citrus in South varieties. Citrus plants in backyards or public areas along America (Ferragut et al 2013), in experiments conducted in main highways and in urban areas were also sampled. Roraima, the mite had developed in neem plants for some In each field, producers were shown photos of attacked generations after artificial infestation (Fantine 2011). plants and asked about the presence of plants showing evi- In Brazil, S. hindustanicus presently is considered a quar- dence of S. hindustanicus. Ten plants, distributed across the antine pest (A2), reported thus far only in the state of whole orchard in zig-zag sampling pattern, were inspected. Roraima. In a survey conducted in 2010, the mite was found All plants indicated by the producers showing possible evi- only in the municipalities of Boa Vista, Bonfim, and Cantá dence of mite attack were also sampled. The following data (Fantine 2011). The recommended legislative measures to were collected for each collection point: geographical coordi- avoid the spread of this mite to other Brazilian states are nates, planted area, number of plants, variety or varieties, age washing, brushing, and waxing of fruits destined for sale in of plants, and use of acaricides. Ten leaves and ten fruits were pest-free states, as well as a ban on the transit of seedlings collected from each plant, whether or not it had been attacked. from infested areas (Mapa 2012). The dissemination of this The collected leaves and fruits were placed in paper bags, mite in Brazil could cause serious impacts to citriculture due labeled, and then packed in plastic bags. Samples were to damages, increase production costs with pest control, and placed in a Styrofoam box, and at the end of the daily collec- possibly impose phytosanitary barriers to the international tions, they were sent to the Laboratory of Entomology of trade of fresh fruits. Embrapa Roraima, where they were inspected under a ste- Brazil is one of the world’s largest producers of citrus reomicroscope (× 40 magnification). Those mites found were and the largest exporter of orange juice. The annual mounted on microscope slides using Hoyer’s medium and Brazilian production of citrus fruits reached 14 million then were sent to the Acarology Laboratory of the Luiz de tons in 2017 (IBGE 2018). The export of orange juice in Queiroz College of Agriculture, University of São Paulo, for that year was more than one million tons, corresponding species identification. to US$1.8 billion (Citros-BR 2018). In addition, the export of fresh lemons and oranges has increased, with that of Tahiti lemon corresponding to more than 60,000 (Boteon Results 2007) and that of orange to more than 27,000 (Citrus-BR 2018) tons per year. The largest citrus production is con- Distribution of S. hindustanicus centrated in the southeastern region, with approximately 85% of the national production, with São Paulo being the Schizotetranychus hindustanicus was found in all the 15 mu- largest producer (IBGE 2018). Therefore, phytosanitary nicipalities of the state of Roraima (Fig 1A), although it was measures that prevent the introduction of this mite to not found at all collection points (Table 1). In Amajari, the these areas are necessary. mite was found in nine of the 11 sampled points at all points Ecological information on S. hindustanicus is scarce, and along the RR-203 highway and in the urban area (Fig 1B). In the true dispersal potential of this mite in Brazil is unknown. Pacaraima, the mite was found in 14 of the 30 sampled Although Roraima is responsible for only approximately points (Table 1). In this municipality, S. hindustanicus was 0.05% of the national citrus production (IBGE 2018), citrus not found in the urban area (seat) but was found in Vila cultivation has been expanding in recent years, and fruits São Marcos, on the margin of highway BR 174, and in the have been sold in Amazonas, increasing the risks of dissem- villages of Surumu and Contão (Fig 1B). In Uiramutã, ination. The objective of this study was to evaluate the dis- S. hindustanicus was found only at one out of 23 sampled tribution of S. hindustanicus in citrus in Roraima and to iden- points, close to the border with Guyana. In Normandia, the tify other mites associated with this species. mite was also well dispersed, being found at 24 of the 29 Schizotetranychus hindustanicus and Associated Mites in Roraima Fig 1 Spatial distribution of Schizotetranychus hindustanicus in Roraima (A), municipalities of the northern (B), central (C), and southern (D)regionsof the state. sampled points, including at the seat of the municipality and In the south of the state, S. hindustanicus was widely along roads (Table 1 and Fig 1B). The northern region of dispersed in Caracaraí and was found in some citrus- Roraima has no commercial citrus orchards, only small pro- producing areas in the other municipalities (Fig 1D). In 2015, ducers who have fewer than 20 fruit trees and occasionally the mite was possibly beginning to disperse into this region. sell the fruits in local markets. According to IBGE (2018), the highest citrus production in In the central region of Roraima, S.