The exotic wasp Megastigmus transvaalensis (Hymenoptera: Torymidae): first record and damage on the Brazilian peppertree, Schinus terebinthifolius drupes, in São Paulo, Brazil

An Acad Bras Cienc aabc Anais da Academia Brasileira de Ciências An. Acad. Bras. Ciênc. 0001-3765 1678-2690 Academia Brasileira de Ciências RESUMO Este trabalho registra o primeiro relato de Megastigmustransvaalensis Hussey (Hymenoptera: Torymidae) em drupas de aroeira-vermelha brasileira, Schinusterebinthifolius Raddi (Anacardiaceae), em Sorocaba, estado de São Paulo, Brasil. Essa vespa é uma espécie invasora e foi encontrada danifi cando drupas de S.terebinthifolius em áreas urbanas (35,0±15,8%), florestas nativas (21,5±10,2%) e áreas de restauração (15,8±8,4%). A bioecologia e os danos causados por M.transvaalensis em drupas de S. terebinthifolius justifi cam mais estudos visando o manejo dessa vespa fi tófaga. Megastigmus transvaalensis tem um potencial de ser disseminado por todo Brasil e representa uma ameaça para a regeneração natural de S. terebinthifolius em florestas nativas e áreas de recomposição e restauração ecológica do país. INTRODUCTION Brazilian peppertree, Schinus terebinthifolius Raddi (Anacardiaceae), native to Brazil, Paraguay and Argentina (Ewel et al. 1982), is a pioneer plant (Lenzi and Orth 2004a) of tropical and subtropical regions (McKay et al. 2009). This species has been introduced in more than 20 countries (Morton 1978, Mytinger and Williamson 1987) and is considered invasive in USA (Ewel 1986, Habeck 1995). In Brazil, S. terebinthifolius occurs from the coast to inland areas at altitudes up to 2000 feet in the state of Pernambuco and in southern Brazil (Joly 1979, Lenzi and Orth 2004a). This dioecious plant, pollinated by Diptera and Hymenoptera (Lenzi and Orth 2004b), can adapt to different areas reaching up to 5-6 meters in height (Lenzi and Orth 2004a) in the sandy and clayey soils of the Atlantic Forest. Furthermore, it grows in the sandbank soils (Cesário and Gaglianone 2008, Lenzi and Orth 2004b) and regenerating regions, fringes of the forests, cities, swamps and pastures (Ewe and Sternberg 2002, Tassin et al. 2007). Schinusterebinthifolius tolerates extreme conditions of humidity, shaded environments and saline conditions (Cuda et al. 2005) with rapid growth and allelopathic compounds (Morgan and Overholt 2005) in locations where other species present less growth (Donnelly et al. 2008). This plant is regarded as invasive in many countries; however, in Brazil it is recommended for land reclamation (José et al. 2005) due to its pioneering behavior, attractiveness to birds (Panetta and McKee 1997, Hight et al. 2002, D'Avila et al. 2010) and good development in less fertile soils (Souza et al. 2001). A phytophagous wasp was first noted in 2012 damaging the S. terebinthifolius drupes in the Sorocaba municipality (23°30'S and 47°25'W) in the state of São Paulo State, Brazil. During the dry season, from July-August 2014, three branches with drupes were collected using pruning shears at the lower third of each one of the 25 trees of this plant in three zones: a native semidecidual seasonal forest, a restored site and an urban forest (Table I), and stored in paper bags. Hundreds of S. terebinthifolius drupes were randomly sampled from the three branches per tree and placed in 500 ml transparent plastic containers with lids, and maintained at 25 °C with white light along 16 h to force the hatching of insects. After that, the number of emergence holes on the drupes and the number of adult insects were counted utilizing a stereoscopic microscope with 10 fold magnification (Figs. 1 and 2). A Kruskall-Wallis analysis and Tukey's test (P≤0.05) were performed to compare drupe damages (DD) among trees and sites. The phytophagous wasps were identified as Megastigmus transvaalensisHussey 1956 (Hymenoptera: Torymidae) by Dr. Paul Hanson of the University of Costa Rica, University City, School of Biology, San Pedro, Costa Rica. TABLE I Number (N°), location of trees (Geog. coord.) and percentage of Schinus terebinthifolius drupes damaged (%DD) (mean ± SD) by Megastigmus transvaalensis (Hymenoptera: Torymidae) in the semidecidual seasonal natural forests (Forest), restoration areas (Restoration) and urban areas (Afforestation) in Sorocaba, São Paulo, Brazil. N° Geog. coord. %DD Forest 1 23°35.20'S 47°31.12'W 35 2 23°35.21'S 47°31.13'W 28 3 23°35.20'S 47°31.14'W 21 4 23°35.21'S 47°31.15'W 31 5 23°35.14'S 47°30.99'W 23 6 23°35.15'S 47°31.31'W 12 7 23°34.97'S 47°31.31'W 1 8 23°35.12'S 47°31.48'W 29 9 23°34.99'S 47°31.62'W 21 10 23°35.00'S 47°31.61'W 14 Mean ± SD (%) 21.5 ± (10.2) Restoration 11 23°21.94'S 47°28.65'W 9 12 23°21.95'S 47°28.66'W 12 13 23°21.96'S 47°28.66'W 14 14 23°21.92'S 47°28.56'W 20 15 23°21.90'S 47°28.60'W 5 16 23°21.95'S 47°28.45'W 29 17 23°21.97'S 47°28.42'W 12 18 23°22.14'S 47°27.78'W 13 19 23°22.12'S 47°27.84'W 31 20 23°22.07'S 47°27.99'W 13 Mean ± SD (%) 15.8 ± (8.4) Afforestation 21 23°31.77'S 47°28.11'W 55 22 23°31.58'S 47°28.16'W 44 23 23°31.48'S 47°28.12'W 36 24 23°31.43'S 47°28.05'W 26 25 23°31.43'S 47°28.03'W 14 Mean ± SD (%) 35.0 ± (15.8) CV% Trees Mean ± SD 21.9 ± (12.6) 57.5 (%) Sites 15.6 Mean ± SD 24.1 ± (3.4) (%) Figure 1 -Megastigmus transvaalensis (Hymenoptera: Torymidae) adults emerged from Schinus terebinthifolius drupes. Side view of a male ( a ) and female ( b ). Scale bars in millimeters. Although Schinus spp. are native South American tree species, the wasp M. transvaalensis is presumed to originate from South Africa (Scheffer and Grissell 2003). It was also reported from the Canary Islands (Grissell 1979), Mauritius and USA (Habeck et al. 1989), Argentina (Wheeler et al. 2001), state of Paraná, Brazil (Perioto 1999), Southern Europe (Continental France and Corsica, Portugal and Continental Spain) and North Africa (Morocco) (Roques and Skrzypczynska 2003). Actually, the seed chalcid is capable of developing and reproducing on plants in the genera Rhus and Schinus. The host range includes at least three Rhus spp. in South Africa of which Rhus laevigata L. and R. angustifolia L. (Hussey 1956, Grissell 1979, Yoshioka and Markin 1991), and Schinus molle L. and S. terebinthifolius, which are both native to South America (Hussey 1956, Habeck et al. 1989). Adults of Megastigmus transvaalensis are yellowish-brown in color, with males and females measuring 2.3 to 2.9 mm and 3.1 to 3.4 mm in length, respectively (Fig. 1). Female ovipositor reaches about half of the body length (Hussey 1956). In most Megastigmus species, egg incubation period is short, the fi rst-instar larvae hatching after four to fi ve days. The larvae then develop through fi ve successive instars to pupae, which are often capable of prolonged diapause (Milliron 1949). Wasps lay more than one egg per S. terebinthifolius drupe but larvae are cannibalistics and after several months, we observed that only an adult emerges from each S. terebinthifolius drupe, leaving a quite circular exit hole (Fig. 2). Megastigmus transvaalensis damaged 1-55% of S. terebinthifolius drupes collected per tree in the state of São Paulo, Brazil with greater variation than that reported in Florida, USA, where 31% and 76% of them were damaged in the winter and spring, respectively (Wheeler et al. 2001) and 80% in Hawaii (Hight et al. 2003). Furthermore, damage largely varied among trees (cv= 57.5%) and sites (cv= 15.6%) (Table I). Drupe damage also differed significantly between zones (Kruskall-Wallis test; H= 6.927; P= 0.031). Following Tukey test, it appeared that damage did not differ between urban areas (35.0±15.8%) and natural forests (21.5±10.2%) but restoration areas (15.8±8.4%) were signifi cantly less attacked than urban areas (Table I). The observed number of damaged caused by M. transvaalensis to the S. terebinthifolius drupes is only an indicator, and the damage may be more important if empty seeds are considered and therefore, requires further study in Brazil. Monitoring of this wasp is necessary for proper population management to lessen the damage it causes to the S. terebinthifolius drupes and others Anacardiaceae species. Figure 2 - Undamaged Schinus terebinthifolius (Anacardiaceae) drupes ( a ) and drupe with the circular exit hole ( b ) of Megastigmus transvaalensis (Hymenoptera: Torymidae) adults. Scale bars in millimeters aCknowledgmenTS To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for fi nancial support. The authors express sincere thanks to Dr. Paul Hanson from the Universidad de Costa Rica Ciudad Universitaria, Escuela de Biologia, San Pedro, Costa Rica for assistance in identifi cation of the species studied. Global Edico Services corrected and edited the English of this manuscript. References CESÁRIO LF AND GAGLIANONE MC. 2008. 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