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; how ever, they are most often associated with develop ing 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 (Panizzi et al., 2000).

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 be ing 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 se curity (FAO, 2013; ^{Gnanamanickam, 2009}). In neotropical rice fields, hemipterans are the pri mary pests (Schaefer & ^{Panizzi, 2000}), with the Pentatomidae family containing the most eco nomically 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 man agement (^{Didonet et al., 2001}; ^{Kruger & Burdyn, 2015}; ^{Pantoja et al., 1997}). These three species are significant because they generate large loss es in irrigated rice cultivation, reducing yields and causing the low quality of commercial rice (Pantoja et al., 1997, 2000; ^{Santana et al., 2018}).

The rice crops may represent important feed ing and mating sites of other stink bug species taxonomically related to Tibraca Stål (^{Barros et al., 2020}a); as is the case for Hypatropis in ermis (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 stud ies 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 ar eas of Argentina. As mentioned above, the oc currence 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 spe cies P. spinosa were reported for the first time in Argentina.

MATERIAL AND METHODS

The study was conducted in twelve commer cial 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 re gion (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 (reproduc tive 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 manu ally at each site in 250cm³ 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, 1984). All the speci mens 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. poeci lus 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 impor tance for the crop.

Key to the stink bug species, both pests and potential pests of rice, from Argentina

1- Anterolateral margins of pronotum straight and crenulated in anterior part; humeral an gles not developed..................................Hypatropis inermis (Fig. 1B)

1´- Anterolateral margins of pronotum sinuous to concave, not crenulated...............................2

2- Mandibular plates subequal to clypeus; anten nomere 2 longer than antennomere 1.............3

2´- Mandibular plates smaller than clypeus; clypeus robust and raised above mandibular plates; antennomere 2 shorter than antenno mere 1................................................................4

3- Apex of radial vein of corium with a large pale yellow callosity; body ferruginous to dark cas taneous, with one pair of yellow callosities on pronotum; if humeral angles are developed into a spine, then spine directed laterally......... ..................................Oebalus poecilus (Fig. 1D)

3´- Apex of radial vein of corium without callos ity; body castaneous, with one pair of small yel low spots, not callosities, on pronotum; if hu meral angles are developed into a spine, then spine directed anterolaterally............................ ........................Oebalus ypsilongriseus (Fig. 1E)

4- Large specimens (body length more than 11 mm); antennomere 4 cylindrical; femurs of metathoracic legs uniformly castaneous; con nexivum with dark castaneous macule on anterior angles....Tibraca limbativentris (Fig. 1F)

4´- Small specimens (body length less than 11 mm); antennomere 4 conical; femurs of me tathoracic legs with proximal part of light col oration and distal part dark; connexivum concolorous with abdomen....................................5

5- Humeral angles slightly developed................... ...................Glyphepomis adroguensis (Fig. 1A)

5´- Humeral angles forming an acute spine di rected anterolaterally......................................... .............................Paratibraca spinosa (Fig. 1C)

The species of Pentatomidae reported for the first time in Argentinean rice crops are present ed 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).

Glyphepomis adroguensis Berg(Fig. 1A)

Fig. 1 Species of Pentatomidae reported for the first time in Argentinean rice crops and currently stated pest species. (A) Glyphepomis adroguensis. (B) Hypatropis inermis. (C) Paratibraca spinosa. (D) Oebalus poecilus. (E) Oebalus ypsilongriseus. (F) Tibraca limbativentris. Scale: 1mm. 

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 hibernat ing on Paspalum quadrifarium Lamb. (Poaceae) (Kormilev & Pirán, 1952), and here it is reported on rice fields in the country for the first time.

The species was recorded during the tillering and flowering stages in plots of both rice variet ies in rice fields of Corrientes province (Fig. 2). Adults were found at the base of the plants be tween the stems.

Fig. 2 Presence of the species Glyphepomis adroguensis, Hypatropis inermis, and Paratibraca spinosa in target rice fields of northeastern Argentina. 

Material examined. Argentina. Corrientes: Empedrado (INTA), 29/XI/2017, Daniela Fuentes-Rodríguez leg., Tillering, manual sampling, 1 female; Empedrado (INTA), 9/II/2018, Daniela Fuentes-Rodríguez leg., Flowering, manual sampling, 4 males, 3 females; Berón de Astrada (Adeco1), 11/I/2018, Daniela Fuentes-Rodríguez leg., Tillering, manual sampling, 2 males, 1 fe male; Empedrado (Bomb2), 12/I/2018, Daniela Fuentes-Rodríguez leg., Tillering, entomological net, 1 female.

Hypatropis inermis (Stål)(Fig. 1B)

Hypatropis inermis is distributed in Suriname, Brazil, Uruguay and Argentina (^{Dellapé et al., 2022}). This species was report ed on rice and overwintering on Andropogon bicornis L. (Poaceae) in Brazil (^{Klein et al., 2013}; ^{Krinski et al., 2015}). While in Argentina, this is the first record of H. inermis on rice.

^{Krinski et al. (2015}) reported that rice might be an important feeding and mating host for this species in Brazil. Because of this, monitoring is recommended. The species was recorded during tillering and flowering in the two rice varieties sampled in rice fields of Corrientes province (Fig. 2). Also, the species were detected during post harvest hibernating on rice stubble.

Material examined. Argentina. Corrientes: Empedrado (Bomb), 12-VII-2017, Daniela Fuentes-Rodríguez leg., post-harvest, manual sampling, 1 male; Berón de Astrada (Cach1),

1-XI-2017, Daniela Fuentes-Rodríguez leg., Tillering, manual sampling, 2 males; Empedrado (INTA), 9-II-2018, Flowering, manual sampling, Daniela Fuentes-Rodríguez leg., 2 females; Berón de Astrada (Adeco), 14-VII-2017, Daniela Fuentes-Rodríguez leg., post-harvest, manual sampling, 1 male.

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.

Along with the genera Glyphepomis, Hypatropis Bergroth and Tibraca, among others, Paratibraca is part of the Mecocephala group, which has been widely studied for presenting many species that are important pests of rice and other crops (^{Rizzo, 1976}; Schaefer & ^{Panizzi, 2000}; Panizzi, 2015; ^{Barros et al., 2020}a, 2020b). Paratibraca spinosa has been collected on rice in several Brazilian states (^{Campos & Grazia, 1998}; Grazia et al., 2022), and the species is re ported here for the first time on rice crops in Argentina.

In Brazil, P. spinosa is considered a pest of rice because when T. limbativentris is found in low quantity, it can reach similar densities to this pest and cause high economic losses (^{Alves et al., 2012}). Because of this, monitoring is sug gested. The species was recorded in rice fields of Corrientes and Chaco provinces (Fig. 2) dur ing the tillering, flowering and ripening stages, mainly in plots of the Fortuna INTA variety. Also, the species were detected during postharvest hibernating on rice stubble. Adults were found at the base of the plants between the stems and were observed on rice stems in the typical feed ing position described for T. limbativentris, with the head pointed downward (^{Ferreira & Martins, 1984}).

Material examined. Argentina. Corrientes: General Paz (DonL), 5/IV/2018, Daniela Fuentes-Rodríguez leg., post-harvest, manual sampling, 1 male; General Paz (DonL), 30/I/2018, Daniela Fuentes-Rodríguez leg., Ripening, entomo logical net, 1 male; Ramada Paso, 4/VIII/2017, Daniela Fuentes-Rodríguez leg., post-har vest, manual sampling, 1 female; Empedrado (Bomb1), 31/I/2018, Daniela Fuentes-Rodríguez leg., Flowering, entomological net, 1 female; Empedrado (Bomb1), 16/II/2018, Daniela Fuentes-Rodríguez leg., Ripening, entomologi cal net, 1 female; Berón de Astrada, 22/II/2017, Solange Martínez leg., Flowering, 1 male; Chaco: Chaco (Gral. Mansilla) 7/II/2019, Daniela Fuentes-Rodríguez leg., Tillering, manual sampling, 1 male.

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.