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Proconiini Sharpshooters of Argentina, with Notes on Its Distribution, Host Plants, and Natural Enemies

The American tribe Proconiini (Hemiptera: Cicadellidae: Cicadellinae) is one of the largest groups of xylem-feeding insects and includes the majority of the known vectors of xylem-born phytopathogenic organisms. The significance of the pathogens that this group transmits gives them an important role as pests, mostly for citrus fruit, grapes, and almonds. Knowledge of these Hemiptera in Argentina is insufficient and fragmentary. Thus one of the aims of this paper is to summarize the available information of the Proconiini sharpshooters in Argentina. In addition, 14 species are mentioned for the first time in the country, and new distributional data are given for 18 species. Thirty-four new associations between sharpshooters and host plants are recorded. New records of egg parasitoids are given for Dechacona missionum, Molomea consolida, M. lineiceps, and Tapajosa similis.


Introduction
The Proconiini tribe (Hemiptera: Cicadellidae: Cicadellinae) is characterized by posterior legs at rest with knees not attaining posterior proepimeral margins, male pygofer and plates both usually with numerous evenly dispersed microsetae and antennal ledges usually protuberant in dorsal aspect (Young 1968). The tribe includes 422 species in 58 genera (McKamey 2007;Wilson et al. 2009) and is restricted to the New World, with only Homalodisca vitripennis having an extra-American distribution, after recent invasion of many islands in the Pacific Ocean (Pilkington et al. 2005). The sharpshooters are one of the largest groups of xylem-feeding insects and include the majority of the known vectors of xylem-born phytopathogenic organisms (Rakitov and Dietrich 2001;Redak et al. 2004).
The bacterium Xylella fastidiosa Wells (Xanthomonadales: Xanthomonadaceae) is a growing threat in the Neotropical region. It has been found in Mexico, Costa Rica, Venezuela, Paraguay, Brazil, and Argentina, and a clear association between the xylemfeeding habit of sharpshooters and their ability to transmit the bacterium has been observed (Hopkins 1989;Redak et al. 2004). Most South American countries are under high occurrence risk of this dangerous disease (Dellapé et al. 2011).
The information on faunistic aspects of Proconiini in Latin America is almost nonexistent, particularly in Argentina. In addition, most of the knowledge on proconiine vectors is derived from studies done in countries of the Nearctic region. Relatively few transmission studies have been carried out in the Neotropic, where the majority of sharpshooter species occur (Redak et al. 2004;Silva et al. 2007;Marucci et al. 2008).
In Argentina, the Proconiini tribe is mainly distributed in the northern region (Young 1968;Remes Lenicov et al. 1999;Virla et al. 2008), and there is almost no information regarding this economically important group. Only for few species is there available data, and most of them provide only distributional records and/or species association with commercial crops (Costilla et al. 1972;Remes Lenicov and Tesón 1985;Paradell 1995;Remes Lenicov et al. 1997, 1999Virla et al. 2008).
To obtain a better understanding about this tribe in Argentina, this paper contributes new distributional records and/or host plants associations and parasitoids, and also summarizes the available data of the Proconiini sharpshooters in the country.

Materials and Methods
Three sources were used to achieve the objectives: (1) bibliographical data; (2) specimens housed in the most important entomological collections of Argentina: Instituto Miguel Lillo (IMLA), Museo de Ciencias Naturales de La Plata (MLP), Museo Argentino de Ciencias Naturales "Bernardino Rivadavia" (MACN); and (3) research conducted by the working group.
112 sites in 21 provinces of Argentina were surveyed between 22° S and 44° S ( Figure 1). Most of the sites were sampled by sweeping on diverse crops, its surrounding vegetation, and both anthropically-modified environments and pristine ones. In four occasions, Malaise traps and yellow pan traps were used as well (in Buenos Aires, Córdoba, and Rio Negro provinces). The specimens collected were preserved in 70% ethanol, and voucher specimens were deposited in the IMLA and MLP collections.
An extensive distribution list of all species studied was made using both our own data, bibliographic records, and data of the specimens deposited in the Argentinean collections. Sharpshooter species were grouped into biogeographical regions proposed by Morrone (2001Morrone ( , 2006. The Jaccard Index was used to identify the similarities between the biogeographic provinces (Moreno 2001).

Results
In the Argentinean territory, 40 species of Proconiini were found: 14 of them were reported for first time in Argentina, and 18 species had extended in geographic distribution. Also, new associations with host plants were found for six species of sharpshooters, and new records of parasitoid wasps for four species.
Below, 14 species of Proconiini recorded for the first time in Argentina are listed (Table 1, symbolized with an "A"):
The Proconiini, as other xylem feeding leafhoppers, are considered polyphagous and have evolved with many unusual adaptations, such as host switching, to maximize nutrient uptake (Mizell and Andersen 2001 Table 2. The knowledge about natural enemies of Proconiini in Argentina is insufficient. Sharpshooter species are attacked by egg predators (Dermaptera), entomopathogenic fungus (Ascomycota) Toledo et al. 2006), and several egg parasitoids belonging Trichogrammatidae and Mymaridae families (Hymenoptera). In recent times, investigations conducted to survey the egg parasitoids of the Proconiini sharpshooters resulted in a greater and more comprehensive understanding of egg parasitoid wasps; the majority of the representatives of this guild belong to Gonatocerus Nees (Mymaridae), a wellknown genus showing a certain degree of specificity at level-tribe, because most of its species attacks Cicadellini and Proconiini sharpshooters (Triapitsyn et al. 2010). New records of parasitoids were found for 10 species (25%). Information of known natural enemies and new data are summarized in Table 3.
In Argentina, all the species of sharpshooters were found in two zones to north of latitude 40º S: one strip that connects the northeast with the mid-east of the country, and another from the northwestern to the mid-west ( Figure  1). The most diverse genera (e.g., Aulacizes and Oncometopia) were found in both places. The eastern fringe includes the Paraná forest and was the most diverse; this is deeply linked to biogeographic systems of the Brazilian territory, which has the greatest diversity of Proconiini (Dellapé et al. 2011). All the studied sites where sharpshooters were found were grouped into the corresponding biogeographic provinces (sensu Morrone 2001Morrone , 2006 (Table 4).
Tapajosa Melichar, the most widely distributed genus, was found in all the biogeographic provinces (except in the Puna); both T. rubromarginata and T. doeringi were the species with southernmost distributional range ( Figure 2). Tapajosa rubromarginata was the most frequent and ubiquitous species, which was found in 70 localities of the Argentinean territory.
Three other genera were found in two biogeographic provinces: Acrogonia Stål (associated with jungle environments, both in Paraná and Yunga forest), Anacuerna Young (distributed in high elevations of Yunga and Puna), and Aulacizes Amyot and Serville (linked to forest environments and very humid localities of Chacoan subregion on the shore of the "Esteros de Iberá") ( Figure 4).
The genus Tretogonia Melichar ( Figure 5) was found in sites of the Chaco province, with T. notatifrons being its most widely distributed species. Oncometopia Young is the genus with more species and was mostly linked to forest sites ( Figure 5), but the species O. facialis and O. tucumana seemed to have more plasticity, occurring in four biogeographic provinces and a variable range of altitudes. Species of Molomea China were found in six different biogeographic provinces, with M. consolida having the widest range, as it was found to occur in 27 localities, from 60 to 2100 m a.s.l. (Figure 6).
Considering the 40 species of sharpshooters inhabiting the Argentinean territory, 19 of them (47.5%) were found only in the Paraná forest, and three species (7.5%) occurred only in the driest region of Chaco. The high elevation of Puna hosted only two species as well as Central Patagonia, where the specimens were collected in oasis located along river valleys.
The number of shared species between biogeographic provinces was low. The range of values of the Jaccard index varied between 0-1, representing complete dissimilarity between sampling for any taxon to a perfect match between sampling, respectively. The highest Jaccard index was obtained for adjacent provinces like "Prepuna-Yunga" (0.6), "Chaco-Pampa" (0.53), and "Prepuna-Monte" (0.5), while there were no shared species between "Puna-Pampa" and "Puna-Central Patagonia" (0), located very far from each other (Table 5). This is the most comprehensive compilation of information related to species of sharpshooters in Argentina. The need for knowledge of interrelationships of insect pests and their environment has been emphasized by several authors in order to develop effective management tactics. In this context, the information given in this study could be useful for those involved in vector-control related programs.

Acknowledgements
We thank the curators of IMLA, MLP, and MACN entomological collections, Dr. Pedro Lozada who provided data on specimens deposited in SMNS, the reviewers for helpful comments, and Lic. D.A. Barrasso for critically reading the manuscript. Gimena Dellapé is a CONICET fellowship holder.  (1): 57-60. * Bibliographic data of distribution; (A) New records for Argentina; (B) New record for province(s); (C) New locality/localities; ( Xf ) Vector species of Xylella fastidiosa according to Roberto et al. (1996) and Yamamoto et al. (2000).  Table 3. Summarized records of natural enemies of the Argentinean Proconiini sharpshooters (*).

Editor's note
(*) The data without references are new records. Table 4. Distribution of the Argentinean Proconiini sharpshooters into the biogeographic provinces (according to Morrone 2001Morrone , 2006. The range of elevation of the localities in which each species occurs is given.