Occurrence of some stink bug species (Hemiptera: Pentatomidae) associated with rice fields in Argentina

: Stink bugs (Hemiptera: Pentatomidae) are a group of about 5,000 species distributed worldwide, many of them phytophagous with economic implications as crop pests. Rice ( Oryza sativa L.) is one of the leading agricultural products for human consumption. In neotropical rice fields, hemipterans are the primary pests, with stink bugs being the worst affecting crop productivity, standing out the genus Tibraca Stål in terms of economic damage. In addition, rice crops may represent important feeding and mating sites for other stink bug species taxonomically related to Tibraca , which could play the role of potential pests, making it necessary to study the pentatomids associated with this crop in the Neotropics. This work aimed to report the presence of Glyphepomis adroguensis Berg, Hypatropis inermis (Stål) and Paratibraca spinosa (Campos & Grazia) associated with rice in the main rice-growing areas of Argentina. Material collected during 2017-2018 from commercial fields in north-eastern Argentina, the central rice-producing region, was identified. The rice variety on which the specimens were collected, crop status (growing season - post-harvest) and crop phenology were considered. As a result, the association of the mentioned species with rice in the provinces of Chaco and Corrientes, Argentina, is reported. Moreover, the genus Paratibraca Campos & Grazia and the species P. spinosa are reported for the first time in the country.


INTRODUCTION
Stink bugs (Hemiptera: Pentatomidae) are a worldwide distributed group that includes around 5000 species (Schuh & Weirauch, 2020), of which 279 are represented in Argentina (Dellapé, 2021). Except for asopines (predators), most stink bugs are phytophagous, feeding on non-cultivated and economically important cultivated plants. These insects can feed on leaves, stems, and roots; however, they are most often associated with developing seeds, fruits or growing shoots (McPherson, 2018;Panizzi et al., 2021). Therefore, they may have economic implications as agricultural pests, and many species of agricultural interest are mainly associated with rice and other grasses .
Rice (Oryza sativa L.) is one of the most important agricultural commodities produced for human consumption, providing 20% of the world's total vegetable calorie intake and being the primary nutritional source for more than half of the global population (Seck et al., 2012;Zeigler & Barclay, 2008). This cereal also provides a large number of calories per hectare cultivated, being a vital food resource within the plans developed to contribute to global food security (FAO, 2013;Gnanamanickam, 2009). In neotropical rice fields, hemipterans are the primary pests (Schaefer & Panizzi, 2000), with the Pentatomidae family containing the most economically important ones, such as the stink bugs Tibraca limbativentris Stål, Oebalus poecilus (Dallas) and O. ypsilongriseus (DeGeer), which are widely distributed in rice fields in the region and represent a serious challenge for pest management (Didonet et al., 2001;Kruger & Burdyn, 2015;Pantoja et al., 1997). These three species are significant because they generate large losses in irrigated rice cultivation, reducing yields and causing the low quality of commercial rice (Pantoja et al., 1997(Pantoja et al., , 2000Santana et al., 2018).
The rice crops may represent important feeding and mating sites of other stink bug species taxonomically related to Tibraca Stål (Barros et al., 2020a); as is the case for Hypatropis inermis (Stål), and several species of Paratibraca Campos & Grazia and Glyphepomis Berg in Brazil (Campos & Grazia, 1998;Pantoja et al., 2005;Farias et al., 2012;Klein et al., 2013;Krinski et al., 2015). According to Farias et al. (2012) and Krinski et al. (2015), further studies are needed to determine the presence of these species in rice and to assess whether they could be pests of this crop in the future.
This work aimed to report the presence of Hypatropis inermis, Glyphepomis adroguensis Berg and Paratibraca spinosa (Campos & Grazia) associated with rice in the main rice-growing areas of Argentina. As mentioned above, the occurrence of these species in rice fields is relevant due to their potential role as crop pests. On the other hand, the genus Paratibraca and the species P. spinosa were reported for the first time in Argentina.

MATERIAL AND METHODS
The study was conducted in twelve commercial rice fields in northeastern Argentina (Chaco and Corrientes provinces: 26°44'S to 27°50'S, 58°50'W to 57°20'W), the main rice-producing region (BCSF et al., 2021). The irrigation system in selected rice fields uses water extracted from the Paraná River, one of the largest river systems in the Neotropics, whose floodplain supports a vast drainage area that includes natural wetlands and rice paddies (Benzaquén et al., 2017;Neiff, 1996). The samplings were carried out during 2017-2018, throughout the whole rice growing season: tillering, stem elongation (vegetative phenology), flowering and ripening (reproductive phenology) (Degiovanni et al., 2004;Kruger & Burdyn, 2015). Also, qualitative post-harvest sampling of rice stubble was carried out in the same plots. The specimens were collected manually at each site in 250cm 3 containers, and using an entomological net. The rice cultivar planted in each studied area, Fortuna INTA (Doble Carolina rice variety, tall plants) and short variety IRGA 424 (long thin rice variety, lower plants), were also recorded.
All collected specimens were preserved in 96% ethanol, and hemipterans were separated from the other orders. Pentatomidae specimens were identified using appropriate keys and literature (Grazia & Schwertner, 2008;Rolston et al., 1980;Rolston & McDonald, 1981. All the specimens studied were deposited in the entomological collection of the Museo de La Plata, Buenos Aires, Argentina. Digital photographs were taken using a Leika EZ4 stereomicroscope, and images were processed with CorelDraw© X7 graphic suite software. The map was created with the Google Maps web mapping platform (https://www.google. com/maps) and edited with CorelDraw© X7.

RESULTS
The species of economic importance and main pests of rice fields are T. limbativentris, O. poecilus and O. ypsilongriseus (Dellapé et al., 2022;Kruger & Burdyn, 2015). However, in this work, we report the occurrence of three other stink bug phytophagous species in Argentine rice fields: Glyphepomis adroguensis, Hypatropis inermis, and Paratibraca spinosa, which are relevant given their role as potential rice pests in other countries such as Brazil (Fig. 1). The following key includes these six species of economic importance for the crop.
Key to the stink bug species, both pests and potential pests of rice, from Argentina  (Fig. 1C) The species of Pentatomidae reported for the first time in Argentinean rice crops are presented below. The authors undertake to notify the authorities of the Servicio Nacional de Sanidad y Calidad Agroalimentaria (SENASA), through the "SINAVIMO" network of the Dirección Nacional de Protección Vegetal -SENASA (DNPV). (Fig. 1A) This species is distributed in Brazil, Uruguay and Argentina (Dellapé, 2021;Dellapé et al., 2022). Along with other species of the genus, such as G. setigera Kormilev & Pirán and G. pelotensis Campos & Grazia, it has been reported on rice crops in Brazil (Campos & Grazia, 1998;Farias et al., 2012, Bianchi et al., 2016. While in Argentina, G. adroguensis was collected hibernating on Paspalum quadrifarium Lamb. (Poaceae) (Kormilev & Pirán, 1952), and here it is reported on rice fields in the country for the first time.

Paratibraca spinosa (Campos & Grazia)
( Fig. 1C) The genus Paratibraca is distributed in Central and South America (Grazia et al., 2022) and is reported for the first time in Argentina through this work.
Given the economic relevance of rice crops and the potential role of these three species of stink bugs as crop pests in neighboring countries such as Brazil, we recommend more exhaustive monitoring and field studies to determine these species' abundance in Argentinean rice fields and to assess whether they could be pests of this crop in the future.