Relicthemisia, a new subgenus of the oil-collecting bee genus Centris Fabricius, 1804 with notes on distribution and host plants of C. xanthomelaena Moure & Castro, 2001 (Hymenoptera: Apidae)

Centris xanthomelaena Moure & Castro, 2001 is a relict species, endemic to northeastern Brazil and broadly recorded within the semiarid region of Caatinga xerophilous open vegetation. It was originally included in the subgenus Paracentris Cameron, 1903 but posteriorly interpreted as remotely related to it or to the subgenus Centris s. str. Fabricius, 1804. In this paper it is proposed to recognize this species as the single member of the monotypic Relicthemisia, a new subgenus which belongs to the ‘Centris group’, one of the main internal lineages of the genus. The proposition of this new subgenus is based on both, morphological and molecular data which indicate its long history as a distinct lineage. Distribution records, floral hosts as well as photographs of both sexes of C. xanthomelaena are also provided.


Introduction
have been described in it, with Paracentris Cameron, 1903 being one of the most diverse, both in number of species and morphology (Vivallo 2020). According to the distribution pattern of the species of this subgenus, sensu Zanella (2002), it corresponds to a group with amphitropical distribution, with a large number of species occurring in North and South America, being practically absent in Central America (Michener 1979). The complete taxonomic revision of the species of Paracentris was published by Vivallo (2020), following the interpretation of Zanella (2002) who carried out a phylogenetic analysis using morphological data of a large part of the taxa present in South America.
Before that taxonomic revision, some species were included in Paracentris intuitively or for practical reasons. An example of this is the species of the 'hyptidis group ' Vivallo & Melo, 2009, whose species have been cited in the subgenera Ptilocentris Snelling, 1984;Centris. s. str.;Ptilotopus Klug, 1810;Wagenknechtia Moure, 1950; as well as in Paracentris (Moure et al. 2009), with the species of this group recently located in a new subgenus Anisoctenodes Vivallo, 2020. A similar case was also observed for Penthemisia Moure, 1950, synonymized with Paracentris by Snelling (1966) and still kept as a junior synonym by Michener (2007), which was later recognized as a distinct lineage exclusive from southern South America and reinstated as a distinct subgenus of Centris (Zanella 2002).
Another similar case is observed in a species apparently endemic to northeastern Brazil described as C. (Paracentris) xanthomelaena Moure & Castro, 2001 and whose phylogenetic affiliation has remained uncertain until now. Moure et al. (2007) cited this species in the subgenus Paracentris, although the results obtained by Zanella (2002) indicated that it is not closely related to that subgenus, but it would correspond to a relict and undescribed lineage close to Centris s. str.
The phylogenetic relationships of C. xanthomelaena with other species of the genus were newly reconstructed by Martins & Melo (2015) in a study using molecular characters. According to those authors, this species would correspond to a lineage not closely related to Centris s. str., but remotely related to the South American species of Paracentris. Despite this inconsistency, in both cases C. xanthomelaena appears as a relict and distinct lineage, which is part of a larger clade known as the 'Centris group' (Zanella 2002).
Considering the results obtained by Zanella (2002) and Martins & Melo (2015), we formally propose a new monotypic subgenus, Relicthemisia subgen. nov., in this paper, containing C. xanthomelaena as type species and recognizing it as another of the major internal lineages of Centris. Both morphological and molecular evidence cited above support and justify the proposition of this new taxon.

Material and methods
General morphological terminology follows Michener (2007). Specimen labels were transcribed under the section 'Material examined'. The backward slash (\) indicates different labels on the pin of the specimen. Specimens marked with a cross '[ †]' were lost in the fire of the Museu Nacional of Rio de Janeiro on September 2 nd , 2018. The literature cited below the name of the species and above its diagnosis corresponds to an update of the information presented by Moure et al. (2007) in the Catalogue of Bees in the Neotropical Region.
Photographs were taken using a Leica DFC 450 camera attached to a Leica M205C stereo microscope and using extended-focus software Leica Application Suite ver. 4.8.0. All images were prepared using CombineZP ver. 7.0.0.1 software, and then enhanced with Adobe Photoshop® (ver. 7.0) without distorting the morphological characters of the specimens.
The distribution map was created using ArcView software (ver. 3.2 GIS) and prepared from locality records taken from specimen labels and from records available in literature listed in the section 'References'. The biogeographical provinces are according to Morrone (2014) and were implemented with the shape file provided by Löwenberg-Neto (2014). This was also done for the compilation of the floral records (Table 1). Plant names were checked and updated according to the International Plant Names Index (ipni.org). New distribution and/or floral records were marked with an asterisk (*).

Diagnosis
Integument dark brown to black, clypeus and labrum coriaceous with coarse and dense punctation, but the clypeus with an unpunctated area as a median longitudinal band on upper half (Fig. 1A).

Female
Inner orbits of compound eyes converging downward (Fig. 1A). Mandible with four apically acute teeth, the fourth tooth slightly larger than the third (Fig. 1A). Basitibial plate elliptical, with S-like secondary plate ( Fig. 2A). Elaiospathes normally developed.

Etymology
From Latin 'relictus' (a survivor from a previous age) plus 'Hemisia' (a junior synonym of Centris) due to the antiquity and isolation of this lineage.

Remarks
Centris xanthomelaena, the only species of the new subgenus Relicthemisia, was recognized as a distinct lineage with no close relationship to other species, based on morphological (Zanella 2002) and molecular data (Martins & Melo 2015). Depending on the study, the phylogenetic position of this lineage was different, either as sister group of Centris s. str. or Paracentris Cameron, 1903 respectively. Nevertheless, it was always recovered as a distinct and relatively old lineage within the 'Centris group'. According to Martins & Melo (2015), C. xanthomelaena diverged from a South American clade formed by Paracentris around 18 million years ago, at about the same time when the major lineages within the 'Centris group' diverged from each other.
The hypothetical relationship of this species with Centris s. str. was based on the interpretation of two morphological characters: the strong emargination on the apical margin of T7 ( Despite the fact that new phylogenetic analyses using a higher number of terminals of Centris s. str. and Paracentris can provide new information regarding the history and relatedness of the lineage of C. xanthomelaena, its distinctness and old history are well supported (see Martins & Melo 2015). Besides the uniqueness of the intense yellow slightly greenish pilosity covering the head, mesosoma (except the ventral surface) and on the anterior half of T1 that allow to easily recognize C. xanthomelaena from other species of the genus (Fig. 1A-D), this monotypic subgenus presents a unique combination of characters of the male's genitalia that distinguishes it from the other members of the 'Centris group': an emargination on the apical margin of T7 (Fig. 2B); a long dorsoapical projection of gonocoxite, ca 2/3 lengths of gonostylus (Fig. 2E); the dorsomedial projections of the genital capsule (Fig. 2E), as well as the S-like lower margin of the female's secondary basitibial plate ( Fig. 2A). Moure & Castro, 2001 Figs 1-4

Diagnosis
Female Integument dark brown to black, except flagellum dark brown and tegula yellowish brown (Fig. 1A-B). Wings brown with veins dark brown (Fig. 1B). Head, mesosoma (except the ventral surface) and anterior half of T1 with intense yellow slightly greenish pilosity, lighter on labrum and gena (Fig. 1A-B). The rest of the body with blackish hairs, except posterior apex of the femur of forelegs with some yellowish hairs (Fig. 1A-B). Clypeus coriaceous with coarse and dense punctation (Fig. 1A). Clypeal disc with an unpunctated area on upper half, without smooth longitudinal band. Labrum with the same punctation, but denser, without smooth basal margin. Terga and sterna, except T6 and S6, with very narrow smooth distal margin, wider on T4. Mandible with four apically acute teeth (Fig. 1A). Fourth teeth slightly larger than the third (Fig. 1A). Maxillary palpus 4-segmented. Malar area very narrow (Fig. 1A). Labrum semicircular (Fig. 1A). Inner orbits of compound eyes converging downward (Fig. 1A). Elaiospathes normally developed. Basitibial plate elliptical, with S-like secondary plate ( Fig. 2A). S2-S4 projected in the middle. Apex of primary pygidial plate slightly rounded with the apex of the secondary plate open and slightly projected towards the distal edge of the primary plate (Fig. 2D).

Male
Similar to the female, except for the following characters: integument dark brown to black, except basal segments of the flagellum brown and apical segments slightly orange (Fig. 1C-D). Supraclypeal area, discs of clypeus and labrum yellow (Fig. 1C-D). Tegula yellowish brown. Clypeal disc with small unpunctated area on upper half, without smooth longitudinal band. Terga and sterna, except T7 and S6, with relatively broad light brown smooth distal margin, wider on T4. Mandible with three apically acute teeth (Fig. 1C). Distance between clypeus and compound eyes shorter than half of the shortest diameter of F1 (Fig. 1C). Apical margin of the hind tibia without tooth-like projection. Apical half of fore and middle basitarsi without a row of long, erect, slightly spatulate and curved setae similar to an elaiospathe. Pygidial plate absent.

Discussion
The distinctiveness of Centris xanthomelaena as compared with the previously described subgenera of Centris was already characterized by Zanella (2002), especially based on the analysis of male genitalia. In the key for subgenera of Centris of Michener (2007), this species fits in Paracentris, considering the "female's basitibial plate with defined secondary plate that lacks sharp projecting margin" and the "margin of secondary plate extending [...] near posterior margin of basitibial plate" (dilemma 13), while the male's lateral ocellus is separated from the eyes by a distance similar to the ocellar diameter, and the T2-T4 covered with dark pubescence (dilemma 20). Nevertheless, males of C. xanthomelaena are clearly distinguished from males of Paracentris by the strong emargination on the apical margin of T7 (Fig. 2B), by the absence of emargination on the basal border of S7 (Fig. 2B), and by the presence of a long dorsoapical projection of gonocoxite, ca ⅔ lengths of gonostylus ( Fig. 2E-F). This latter feature is unique, being a somewhat intermediate condition between that observed in Centris s. str. and Paracentris. Previously to its description and naming, Centris xanthomelaena was already recognized as a legitimate pollinator of Angelonia campestris Nees & Mart. and A. salicariifolia Bonpl. (Plantaginaceae) in the Caatinga (Vogel & Machado 1991 A similar context was noted by Aguiar et al. (2003) in relation to Centris hyptidis Ducke, 1908, another species endemic from northeastern Brazil and typical from Caatinga vegetation. This species also has a more specialized relation with pollen and oil sources in the Caatinga biome as compared to other species with wider distribution patterns. This can be interpreted as a result of a longer history with plants of this semiarid region. Differing from the interpretation of Giannini et al. (2013), C. hyptidis, along with C. hyptidoides Roig-Alsina, 2000 and C. thelyopsis Vivallo & Melo, 2009, does not belong to the same lineage of the subgenus Wagenknechtia, but to C. (Anisoctenodes), an old lineage distributed in the South American diagonal of open dry vegetation (Werneck 2011;Zanella 2011), probably with association to flowers of Angelonia (Plantaginaceae) (Vivallo & Melo 2009;Martins & Melo 2015).
A similar old history and restricted distribution is found in Centris (Relicthemisia) xanthomelaena, in spite of similar oil-collecting apparatuses found in other species of Centris that also occur in the Caatinga (Vogel & Machado 1991). Those structures are specialized in exploring plant species with epithelial elaiophores (Giannini et al. 2013). It must also be noted that there is no record of this bee visiting the introduced West Indian cherry (Malpighia emarginata D.C.) even though the intense collection effort in this tree at sites where C. (Relicthemisia) xanthomelaena occurs (Coelho et al. 2018;Siqueira et al. 2011).