Synopsis of the parasitic wasps Bephrata (Hymenoptera: Chalcidoidea, Eurytomidae) in Brazil

ABSTRACT. This study is focused on the parasitic wasps Bephrata Cameron, 1884 (Hymenoptera, Eurytomidae), a small and poorly represented genus in entomological collections. Herein we report new geographical records to Bephrata bahiae (Ashmead, 1904), B. bouceki Gates & Hanson, 2009, B. cultriformis (Ashmead, 1894), B. leptogaster Gates & Hanson, 2009, B. lorraineae Gates & Hanson, 2009, B. ruficollis Cameron 1884 and B. ticos Gates & Hanson, 2009. Except for B. bahiae, B. chica Gates & Hanson, 2009 and B. christeri Gates & Hanson, 2009, all other studied species were recorded for the first time to Brazil. Additionally, we provide maps with the geographical distribution of the studied species based on the new records and literature data, and an identification key for the species recorded in Brazil. With these new records there are currently nine species of Bephrata known in Brazil.

Parasitic wasps, an especially diverse and dominant group of insects in the Neotropic, are a fascinating, taxonomically challenging and one of the most abundant groups of terrestrial natural enemies available (Munro et al., 2011;Heraty et al., 2013;Murray & Heraty, 2019).
Bephrata Cameron, 1884 (Eurytominae) is a predominantly Neotropical chalcid wasp group and currently includes 22 species, of which 19 occur in the Neotropical Region and three have been recorded for Brazil: B. bahiae (Ashmead, 1904) in the coastal tablelands of Atlantic Forest from state of Bahia and, B. chica Gates &Hanson, 2009 andB. christeri Gates &Hanson, 2009, both in the Amazonian basin from state of Amazonas (Gates & Hanson, 2009;Noyes, 2019;Perioto, 2022).Furthermore, an unidentified species of Bephrata is mentioned for Pantanal biome in Mato Grosso do Sul state (Shimbori et al., 2017).
The knowledge about the Brazilian fauna of Bephrata and its distribution is still far from complete.Therefore, the new distribution records presented here are important for a better understanding the actual richness and distribution range of this genus of parasitic wasps.
The consistency of anatomical data with the Hymenoptera Anatomy Ontology project (Yoder et al., 2010;Seltmann et al., 2012) was determined using the proofing tool available through the Hymenoptera Glossary (HAO, 2019).
Images were taken using a digital camera attached to a stereomicroscope and specimens illuminated with high diffuse dome illumination.Focus stacking of images was done using the software Helicon Focus (version 5.3).The figures were prepared using Adobe Photoshop (version 11.0).Species distributions were assembled in a dataset and incorporated into distribution maps.Geographic coordinates of the species records, if not present in labels, were taken from Google Earth software (https://www.google.com/earth/), and the maps were generated using the web software SimpleMappr (Shorthouse, 2010).
Abbreviations for Brazilian states are as follows: AC, Acre; AM, Amazonas; BA, Bahia; ES, Espírito Santo; MG, Minas Gerais; PE, Pernambuco; PR, Paraná; RJ, Rio de Janeiro; RN, Rio Grande do Norte; RO, Rondônia; RR, Roraima; and SP, São Paulo.Identification.According to Gates & Hanson (2009), B. bahiae is recognized for presenting the dorsal-posterior part of head with yellow area between occiput and ocellar area; mesoscutum and mesoscutellum pale yellow or orange yellow; center of pronotum with very narrow, longitudinal black line; procoxa with sinuous groove on anterior surface and metatibia black, at least in part.The specimen collected in Descalvado (SP) has the pronotum completely yellow, without longitudinal black line.

Bephrata Cameron, 1884
Discussion.Bephrata bahiae has been found previously in Costa Rica and Colombia and, in Brazil, has been recorded in state of Bahia (Gates & Hanson, 2009;Noyes, 2019).The new distributional records, in five Brazilian states (RN, MG, ES, RJ and SP) represent a significant increase of the distribution range in Brazil and indicate that this species can develop in different biomes such as Brazilian savannah, Atlantic rainforest and Caatinga.Gates & Hanson, 2009 (Figs 3, 4) Discussion.Only seven specimens of B. bouceki are known, all of them from the Amazon rainforest.B. bouceki has been found previously in Colombia, Equador and Peru (Gates & Hanson, 2009;Noyes, 2019).Now it is reported for the first time for Brazil, in Amazonas and Rondônia states.This new record extends the geographical distribution of B. bouceki about 1,800 km to the southeast from the type locality at Sucumbíos, Equador, 1,200 km to the southeast from Amazonas, Colombia and 800 km from Madre de Dios, Peru, the previous records.Discussion.Gates & Hanson (2009, p. 40), when describing Bephrata chica, stated that this species "can be distinguished by its black hind legs (except for the tarsi)".However, when analyzing the holotype's image, we verified that the hind leg of this specimen has coxa and femur almost entirely colored of yellowish brown, brown tibia, and yellowish tarsi.

Bephrata christeri Gates & Hanson
Discussion.Bephrata cultriformis was previously found in Mexico, Costa Rica, Dominica, St Vincent & Grenadines,Venezuela, Ecuador and Peru (Gates & Hanson, 2009;Noyes, 2019).Now it is reported for the first time for Brazil in Amazon rainforest area in the Acre and Amazonas states.Gates & Hanson, 2009 (Figs 11, 12) New records.Amajari (RR), Uruçuca (BA), and Ubatuba (SP) (Fig. 12).Identification.According to Gates & Hanson (2009), B. leptogaster is recognized by the extremelly elongate gaster (6× as long as high), specially in females.In addition, this species presents the procoxa with a sinuous groove on anterior surface, the lower face yellow (except for small black spot in the middle), the mesosoma with dorsum completely black, the fore wing without dark spot and with veins very thin, and the metatibia mainly black.In males, the mesoscutum and mesoscutellum presents transverse wrinkles and the pronotum is sligthly concave dorsally.

Bephrata leptogaster
Discussion.Bephrata leptogaster was previously found in Venezuela, Colombia, Ecuador and Peru (Gates & Hanson, 2009;Noyes, 2019) and now this species is reported for the first time for Brazil in the Amazon rainforest, in Roraima state, and in the Atlantic rainforest, in Bahia and São Paulo states.The female specimen from Uruçuca (BA) presents the lower face mostly darkened (from brown to black, except by the yellow margins), much larger than the small spot in the middle of lower face pointed by Gates & Hanson (2009).However, the former female agrees with the remaining features of original description of B. leptogaster and the male agrees with the whole description.Identification.According to Gates & Hanson (2009), B. ruficollis is recognized for presenting the metatibia completely yellow and is the only species in which the clava is white (pale yellow in some specimens here studied), differing from the other brown/black flagellomeres.
Discussion.Bephrata ruficollis was previously found in Costa Rica, Panama, Venezuela, and Ecuador (Gates & Hanson, 2009;Noyes, 2019).Now the species is reported for the first time for Brazil in Amazon rainforest in the state of Acre and Amazonas, and in Atlantic rainforest in the state of Espírito Santo, about 2.600 and 5.300 km southeast, respectively, from the type locality.Gates & Hanson, 2009 (Figs 18, 19) New record.Recife (PE) (Fig. 19).Examined material.1 female."Brasil, PE, Recife, Pq. dos Dois Irmãos, 08°00'37"S 34°56'31"W, varredura veg., 22/IV/2002, S.T.P. Amarante e eq., cols.", 1 female (LRRP #20709).Identification.According Gates & Hanson (2009) B. ticos is recognized for presenting the head yellow except black from scrobe to back of head and a small spot below eye; mesoscutum and mesoscutellum mostly yellow or orange yellow (sometimes with a thin, longitudinal, black line in middle); center of pronotum with wide black spot; mesoscutellum orange (reddish) yellow and procoxa with sinuous groove on anterior surface and metatibia black (dark brown in some specimens here studied), at least in part.

Bephrata ticos
Discussion.Bephrata ticos was previously found in Costa Rica (Gates & Hanson, 2009;Noyes, 2019).Now the species is reported for the first time for Brazil in Atlantic rainforest area in the state of Pernambuco, about 5.800 km southeast from the type locality.

DISCUSSION
Until now, the knowledge about Bephrata in Brazil was restricted to the occurrence of three species: B. bahiae, B. chica and B. christeri (Perioto, 2022).With the addition of B. bouceki, B. cultriformis, B. leptogaster, B. lorraineae, B. ruficollis and B. ticos to the Brazilian fauna, we expanded the knowledge of the group to nine species occurring in the country.
Furthermore, it is important to highlight the record of B. lorraineae for Fernando de Noronha archipelago.This archipelago is entirely volcanic in origin and has never been connected to the mainland and the main island area of Fernando de Noronha is 16.9 km 2 (Lopes & Ulbrich, 2015).
There is no evidence of the natural occurrence of orchids in the Fernando de Noronha archipelago and certainly the orchids that exist there today were introduced for the purposes of landscaping and decoration of hotels and inns.The archipelago is separated from the mainland by about 550 km.Such facts lead us to believe that B. lorraineae was introduced into the archipelago in orchid plants containing parasitized Tettigoniidae eggs.More studies are needed to support the hypothesis raised here.
, and collection expeditions carried out by N. W. Perioto and R. I. R. Lara in 2018 and 2019 in areas of Brazilian savanna at Parque Nacional da Chapada dos Veadeiros, in Goiás state and at Parque Nacional Grande Sertões Veredas, in Minas Gerais state, Brazil.The holotypes of B. chica, B. christeri and B. lorraineae Gates & Hanson, 2009 deposited in the Smithsonian National Museum of Natural History (USNM) were studied through photographs available in https://collections.nmnh.si.edu/search/ento/.