The species of the bee genus Centris of the “hyptidis group” revisited with the description of Centris (Anisoctenodes) new subgenus (Hymenoptera: Apidae: Centridini)

In this paper, the species of Centris of the “hyptidis group” are revisited, proposing to recognize them as members of Anisoctenodes subgen. nov., a new subgenus supported by morphological and molecular data. The species included in this new taxon are C. hyptidis Ducke, 1908 (type-species), C. hyptidoides Roig-Alsina, 2000, C. thelyopsis Vivallo & Melo, 2009 and C. anisitsi (Schrottky, 1908), transferring this latter from Centris (Xanthemisia) Moure, 1945. An updated key, information on the type depository, a distribution map, photographs of both sexes as well as of the diagnostic characters of the new subgenus are also provided.


Introduction
Centris Fabricius, 1804 is the most diverse lineage of oil-collecting bees in the Western Hemisphere. This genus contains more than 300 described species of which approximately 230 are considered valid (Moure et al. 2007). Throughout the taxonomic history of Centris, various subgenera have been proposed with the objective of grouping the numerous species described in more discrete units that reflect their natural history. Some of those groups, such as C. (Centris), C. (Heterocentris) Cockerell, 1899, C. (Hemisiella) Moure, 1945 and C. (Xanthemisia) Moure, 1945 are easily identifiable from morphological characters, while others are more difficult to recognize. In the latter category are those morphologically more heterogeneous subgenera, most of which have their monophyly never been demonstrated. Roig-Alsina, 2000 (Figs 2C, 3C, 5A-D) and C. thelyopsis Vivallo & Melo, 2009 (Figs 2D, 3D, 6A-D) (Vivallo & Melo 2009). The "hyptidis group" is a very uniform and clearly monophyletic group, which is supported by both morphological (Vivallo 2004) and molecular data (Martins & Melo 2016). However, the phylogenetic relationships between it and the other internal lineages of Centris have been subject of some controversy, depending on the type of characters considered.
Morphologically, the species of the "hyptidis group" share some unique morphological characteristics within the genus, highlighting among them the quadrangular shape of the trochanter of fore ( Fig. 2A-D) and middle legs in both sexes, and the particular morphology of the fore oil-collecting apparatus (elaiospathe) of the females (Fig. 3A-D), being both diagnostic characteristics for the group (Vivallo 2004;Vivallo & Melo 2009).
During the development of a taxonomic revision of some centridine bees, the holotype of C. anisitsi (Schrottky, 1908) (Fig. 1C-D) housed at the Museum für Naturkunde Berlin, Germany (ZMB), was examined. This species is only known from its type specimen collected in Asunción, Paraguay and nothing is known about its bionomy or distribution range. In the subgeneric arrangement of the centridine bees, Moure et al. (2007) included it in C. (Xanthemisia) following the information cited by Schrottky (1908) in the original description about its proximity with C. bicolor Lepeletier, 1841 and C. lutea Friese, 1899.
The detailed study of the type specimen, along with the examination of the undescribed female ( Fig. 1A-B) also housed at ZMB, revealed that C. anisitsi is not related to C. (Xanthemisia) but with the species of the "hyptidis group", sharing the same morphology of fore ( Fig. 2A) and middle trochanters as well as the modified fore elaiospathes (Fig. 3A). Thus C. anisitsi becomes the fourth species of this particular lineage of bees. The removal of this species from C. (Xanthemisia) transforms this subgenus in a monophyletic group.
Taking into account the unique synapomorphic morphological characters exhibited by the species of the "hyptidis group" (Vivallo 2004) and despite the difficulty of relating the clade formed by them with other internal lineages of Centris, I propose to formally include them in their own subgenus. As mentioned previously, the clade formed by these species has always been recovered in phylogenetic analyzes using both morphological (see Vivallo 2004: fig. 2.2) and molecular (see Martins & Melo 2016: figs 1-2) data, which supports and justifies its description.

Material and methods
The specimens studied are four couples and the primary type of Centris hyptidis (Coleção Entomológica, MNRJ and MPEG), three females, two males and the primary type of C. hyptidoides (MLP and LPBC), the type series of C. thelyopsis formed by three females and two males (DZUP), along with the holotype male and the single female known of C. anisitsi, both housed at ZMB.
All labels are considered rectangular and yellowish white (by effect of time), and the data is handwritten or printed in black, unless otherwise indicated. The specific features of the labels, such as the coloration or type of writing, are presented in squared brackets ([]). The backward slash (\) indicates different labels on the pin of the same specimen. Specimens marked with a cross ( †) were lost in the fire of the Museu Nacional Rio de Janeiro on September 2 nd , 2018. Specimens from others than the MNRJ marked with a cross were in loan at the museum and also lost in the fire.
In the redescription of the holotype of Centris anisitsi (Fig. 1C-D) and the description of its female ( Fig. 1A-B), the morphological terminology follows Michener (2007). The morphology of the oilcollecting apparatus (elaiospathes) is according to Snelling (1984) and Neff & Simpson (1981). Maxillary palpomeres were numbered from the base to the apex. The position of the vertex in relation to the compound eyes was considered in frontal view. Antennal flagellomeres are indicated as F1, F2, etc., and the metasomal terga as T1, T2, etc.
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 the 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 maps were created based on the records provided by Vivallo & Melo (2009)
The species of this new subgenus can be recognized by the shape of the trochanter of fore and middle legs with a basal laminar projection ( Fig

Etymology
From Greek 'anisos' ('unequal') and 'ctenodes' ('comb-like') based on the particular shape of the fore elaiospathe of the females. The morphology of the oil-collecting apparatuses of the species of this group is unique in Centris which contrasts with the pattern found in the rest of the species of the genus. The shape considered ancestral includes an anterior primary comb formed by a single row of enlarged, flattened and apically curved overlapping setae, and a secondary comb formed by four giant spatulate setae located in opposition to the primary comb (Neff & Simpson 1981).

Remarks
Most species of Anisoctenodes subgen. nov. exhibit interesting associations with oil-offering flowers, mainly with Angelonia (Plantaginaceae). The species of this genus have trichomatic elaiophores, which require specialized structures for their exploitation (Vogel 1974;Neff & Simpson 1981). The females have long and branched hairs of spatulate apex (Vogel &Machado 1991: fig. 9C, G andMartins et al. 2013: fig. 9C-E). These bristles are used for oil collection not through scraping by the elaiophores as in other species of Centris, but by absorption, using capillarity forces (Vogel & Machado 1991). A detailed description of the oil-collecting apparatus and the collecting behavior of C. hyptidis can be found in Machado et al. (2002) and in Martins et al. (2013) for C. hyptidoides.

Distribution
The species of Anisoctenodes subgen. nov. occur in the South American diagonal of open dry areas formed by the Caatinga, Cerrado, Chacoan and Pampean Provinces. These provinces belong to the Chacoan subregion of the Neotropics (Morrone 2014). Centris hyptidis is distributed mainly in the Caatinga, with peripheral records in the north of the Paraná Forest Province and in the Cerrado. In this latter province also occurs C. thelyopsis in the dry forests of the upper Tocantins River (Vivallo & Melo 2009). Centris anisitsi and C. hyptidoides are distributed in the Chacoan Province, with the latter species also being registered -for the moment by a single record -in the Paraná Forest Province (Fig. 7).
The description of the morphology of Centris hyptidis, C. hyptidoides and C. thelyopsis, along with their distribution ranges and floral hosts, can be found in Vivallo & Melo (2009). The redescription of C. anisitsi and the description of the female are provided below.

Type data
This species was described by the German entomologist Curt Schrottky (1874Schrottky ( -1937 based on a single male specimen collected by János Dániel Anisits  in Asunción, Paraguay. Anisits was a Hungarian pharmacist, biologist, botanist and researcher who migrated to Paraguay after he graduated as a pharmacist in Budapest. In Paraguay he was head of the Department of Zoology and Botany at the National University. Working actively, he conducted two decades of exploration, collecting biological material and discovering several new species of plants, mainly palm and cactus (Magyarország és Latin-Amerika 2019). The labels of the holotype and the additional material are quoted verbatim.

Redescription of the male
Coloration. Integument dark brown, slightly lighter to reddish brown on labrum. Tegula yellowish, darker towards anterior margin. Wings light brown (Fig. 1C-D).
integument and sCulptured surfaCe. Clypeus finely areolate towards upper margin, with very coarse and dense punctation, giving it a rough appearance (Fig. 1C). Labrum with similar punctation, with denser and finer punctures towards upper margin (Fig. 1C). T2 and T3 with fine, very dense and uniform punctation. T4 and T5 with coarser and disperse puncture. T3-T6 with smooth and translucent distal margins, more evident towards apex of metasoma.
integument and sCulptured surfaCe. Clypeus with very coarse and dense punctation (giving it a rough appearance), slightly scattered towards lower margin (Fig. 1A); central surface with median, coarse and conspicuous carina between upper and lower margins. Labrum with coarse punctation, more scattered than on clypeus, with finer and denser puncture towards lower margin (Fig. 1A). T2 and T3 with fine, very dense and relatively uniform punctation. Terga and sterna with smooth translucent distal margins, more evident towards apex of metasoma.

Distribution
This species has only been recorded in Paraguay (Capital District: Asunción; Cordillera Department: San Bernardino) (Fig. 7).

Type data
Centris hyptidis was described by the Italian botanist and entomologist Adolf (Adolpho) Ducke  based on an undetermined number of female specimens collected in Baturité, Ceará state, northeastern Brazil. The lectotype female was designated by Nascimento (1979), the labels are quoted verbatim.
Cockerell described Centris (Ptilotopus) libertatis based on a single female collected at "Independencia", Paraíba state, northeastern Brazil by Harold Heath (1868-1951) and William Mann (1886-1960, both members of the Stanford Expedition (Oliveira 2014). The type specimen is currently housed at AMNH, the label is quoted verbatim.

Discussion
The formal recognition of Centris (Anisoctenodes) as a new subgenus allows a better organization of and clarity on the phylogenetic relationships between certain groups of species within Centris. The removal of the species of the "hyptidis group" sensu Moure et al. (2007) from C. (Paracentris) allows recognizing that it is not related to the species of that subgenus, as well as contributing to our better understanding of the latter taxon. Centris (Paracentris), along with C. (Melanocentris) Friese, 1901, are the two subgenera with the highest specific richness and they include the species most difficult to identify. It is expected that both groups will undergo further modifications with respect to the number of species they have, once the taxonomy and the morphology of their species is studied. Fig. 7. Distribution map of the species of Centris (Anisoctenodes) subgen. nov.
The removal of C. anisitsi from C. (Xanthemisia), its recognition as a member of the "hyptidis group" and its subsequent inclusion in C. (Anisoctenodes) subgen. nov. allows recognizing the former subgenus as a monophyletic group. Now including only species that share the very particular morphology of the mandible and the pygidial plate of the females that characterizes this group.
The species of C. (Anisoctenodes) subgen. nov. occur in the South American diagonal of dry open areas. This distribution pattern is very interesting from the biogeographic point of view, so new research focused on this fact could contribute significantly to the knowledge of the relationships between the biogeographic provinces that compose the Chacoan dominion. According to Martins & Melo (2016), this group of bees arose approximately 35 million of years ago during the Eocene, being a relatively old lineage within the genus.
Among the species of this new subgenus only C. hyptidis and C. hyptidoides have been studied relatively in detail, mainly as pollinators. Unfortunately, the knowledge of the bionomy of C. anisitsi and in a certain way of C. thelyopsis is almost completely unknown.