A new species of Ceratina (Ceratinula) Moure, 1941, with notes on the taxonomy and distribution of Ceratina (Ceratinula) manni Cockerell, 1912, and an identification key for species of this subgenus known from Brazil (Hymenoptera, Apidae, Ceratinini)

Abstract A new species of the small carpenter bee, genus Ceratina (Ceratinula) Moure, from the Cerrado Biome in midwestern Brazil is described and illustrated. Ceratina (Ceratinula) fioreseana Oliveira, sp. nov. is easily distinguished from its congeners by the size of the facial maculations and the honey-yellow color of the legs and antennal scape, which distinguish it especially from Ceratina (Ceratinula) manni Cockerell, 1912, the most similar species in terms of facial maculation patterns. The geographic records of C. manni, here interpreted as endemic to the semiarid Caatinga region in northeastern Brazil, are presented, with new records for the Brazilian states of Piauí, Ceará and Bahia. A morphological description of both species is provided, including a comparison with the type specimen of C. manni from the state of Paraíba (Guarabira, formerly named Independencia). An identification key is provided for the described species of Ceratina (Ceratinula) recorded for Brazil according to Moure’s Catalogue of Neotropical Bees.


Subgenera Species number
Some investigators have considered the genus Ceratina as a key taxon for understanding the transition from subsocial to social behavior, as they have a broad range of social behaviors, ranging from solitary, subsocial, and semisocial to eusocial colony organization (Rehan 2020). Rehan et al. (2015) provided evidence of nest reuse consistent with the hypothesis of kin associations for three Neotropical species of Ceratina (Ceratinula) from Panama, confirming that sociality occurs in low frequency in Ceratina bee populations, generally in a third or less of a population. According to Rehan et al. (2015), the solitary nature of the majority of colonies indicates that solitary nesting is adaptive in the species studied by these authors.
Griswold 2020). Ceratina (Ceratinula) occur throughout the Neotropical region and extend to the United States of America (Silveira et al. 2002;Michener 2007;Moure 2012). Despite the fact that 14 of its 37 valid species occur in Brazil (Moure 2012;Table 2), no taxonomic review that includes the Brazilian species has yet been published. Moure (1941: 78-83), when describing Ceratinula as a new genus, redescribed or added taxonomic information for eight Neotropical species (six from the Brazilian fauna, not including C. manni) and described five new species, including four from Brazil. These are solitary bees, whose role in the pollination of plants is still not well studied, although their importance in pollination of the melon cactus Melocactus curvispinus Pfeiff. and the carnivorous corkscrew plant Genlisea violacea A.St.-Hil. has been reported (Nassar and Ramírez 2004;Aranguren et al. 2018).
Information on the geographic distribution of the described species of C. (Ceratinula) is still limited. Moure (2012) did not mention any record for midwestern Brazil and recorded only four species for the northeastern region (C. augochloroides, C. lucidula, C. manni, and C. muelleri - Table 2). However, several local inventories record unidentified species in these regions (Sigrist et al. 2017 andLima andSilvestre 2017 for midwestern Brazil;and Aguiar and Zanella 2005;Viana and Kleinert 2005;Albuquerque et al. 2007 andMilet-Pinheiro andSchlindwein 2007 for northeastern Brazil).
The present contribution describes and illustrates a distinctive new species of Ceratina (Ceratinula) Moure from midwestern Brazil (in the Cerrado Biome). Ceratina (C.) manni is redescribed, based on female and male individuals, and its geographical records updated. An identification key for the species of Ceratina (Ceratinula) so far recorded in Brazil is also provided, based on the list of Moure (2012).

Materials and methods
The specimens of the new species described here were collected in November 2018, during a rapid assessment for monitoring bee diversity, performed in the area surrounding a soybean field on the Nossa Senhora Aparecida farm, in Água Fria de Goiás, Goiás State, midwestern Brazil. The farm belongs to the Fiorese family (Oli Antonio Fiorese, Edileusa Fiorese, Henrique Gustavo Fiorese, Kaio Felipe Fiorese), who have adapted their production methods to meet the standards for environmental certification, and this is now considered a model farm.
Repository institutions of the specimens are:  Cockerell, 1912 is deposited in the Entomological Collection of the American Museum of Natural History (AMNH), New York, United States of America.
The description of C. (Ceratinula) fioreseana sp. nov. is based on the female holotype and male paratypes. The redescription of the female of C. (Ceratinula) manni Cockerell, 1912 is based on all specimens studied, checking the diagnostic characters presented in the original description (Cockerell 1912) with images of the female syntype deposited in AMNH, which were downloaded from the Discover Life website in 2016 ( Fig. 4 -the images are no longer available on the website).
Due to the COVID-19 pandemic, the identification key presented for Brazilian species of Ceratina (Ceratinula) was constructed based mainly on the original descriptions (as a first key attempt to aid identification, since the subgenus has not yet been revised), but was tested using a few specimens of seven different species that were accessible to us.
Specimens were studied and photographed using a Leica M165C stereomicroscope coupled to a Leica DFC295 digital camera, containing the program LEICA AP-PLICATION SUITE V4.1 Interactive Measurements, Montage. Measurements are given in millimeters and taken at the greatest width or length of structures. When we had access to more than one specimen, all were measured, and we report the average. The ocellocular distance is measured from the lateral ocellus, and the length of the anterior wing is measured from the costal sclerite. Abbreviations are:
The classification follows Michener (2007), whereby all bees correspond to the group Anthophila, and Ceratina is a genus within the family Apidae, subfamily Xylocopinae, tribe Ceratinini. Morphological characters in the identification key for recognition of Brazilian species follow their original descriptions and Moure's (1941) redescriptions.
Diagnosis. Minute bees (3-6 mm long); usually metallic (rarely with the metasoma red); body elongated, with a slightly petiolate metasoma, the first segment as elongate-triangular; integument with extensive impunctate smooth areas, especially on head (paraocular area above antenna and on gena, sometimes on the whole head) and on mesonotum; second submarginal cell narrowed, sometimes converging to a point anteriorly, becoming almost triangular (Moure 1941;Michener 2007).
Among the species of Ceratina (Ceratinula) occurring in South America, C. (C.) fioreseana Oliveira, sp. nov. is similar to C. (C.) manni, especially in the pattern of facial maculation (Fig. 8). However, it is easily distinguished by the smaller and slimmer body, the color of the legs, antennal scape, pedicel and first three flagellomeres (honey-yellow in fioreseana sp. nov. and dark brown in manni); the integumental microsculpture on the paraocular region and on the upper part of the clypeus (smooth in fioreseana sp. nov. and microreticulate in manni); the yellow genal stripe (following the orbit in the lower region in fioreseana sp. nov. and on the upper portion of the head diverging upward from the orbit in manni).
Observed variations. Some male specimens, such as the male paratype ( Fig. 2A), have a discolored translucent area in the middle of the apical 1/2 of the clypeus. Other specimens have a uniformly yellow clypeus (Fig. 2F). Etymology. The specific epithet is a patronym honoring Oli Antonio Fiorese, Edileusa Fiorese, Henrique Gustavo Fiorese and Kaio Felipe Fiorese, owners of the Nossa Senhora Aparecida farm (located in Água Fria de Goiás, Goiás State, midwestern Brazil), where the type specimens of the new species were collected. We honor their recognition of bees as key pollinators important to sustainable production, adapting their production to meet the standards for environmental certification, and also adopting various pollinator-friendly measures through the Bayer Forward Farming Project. Because of these procedures, their property has been certified as a model farm by environmental agency Round  Type locality. Brazil, Paraíba, Guarabira (previously known as Independencia). Diagnosis. Both sexes: integument color tending more to greenish with golden metallic sheen. Female: five yellow maculations on face and one stripe on gena; median paraocular yellow maculation almost filling the entire space between the eye and antennal socket, and almost reaching the height of upper part of the epistomal suture ( Fig. 9, C, D); oval maculation on lower paraocular areas large, near tentorial pit (Figs 4A, B; 5A, D-F; 8C); lower paraocular area microreticulate (Figs 5E; 8C); supraclypeal plain raised surface subtriangular (Fig. 9, A, B); stripe of gena on superior half, extending above dorsal margin of eye, broader and divergent superiorly and closer to eye in lower portion (Figs 4C; 5B, C); antennal scape, pedicel and following three antennomeres brown (Figs 4A-C; 5A-F); coxae, trochanters and femurs of all legs brown, protibia and tarsus lighter honey-brown, meso-and metatibiae and basitarsi lighter brown, following tarsomeres lighter honey-brown (Figs 4C; 5B, C). Male: clypeus almost totally yellow, except for a narrow strip that borders the upper edge above the tentorial pits; two large paraocular yellow spots close to clypeus; labrum and mandible almost entirely yellow; apical margin of S5 slightly tri-concave, median concavity deepest (Fig. 7F); apical margin of S6 strongly bilobed, with deep median concavity intruding almost to midlength of sternum (Fig. 7E).   D, E, F; 8C); wide brownish honey-yellow band on apical 1/3 of clypeus (Fig. 4A, B); yellow stripe occupying superior half of gena, extending above dorsal margin of eye, broader and divergent superiorly and closer to eye in lower portion (Figs 4C; 5B, C); mandible honey-brown, more reddish on base and more blackened on apex; labrum honey-brown, slightly lighter basally (Fig. 5D); antennal scape, pedicel and first three flagellomeres brown, scape with tiny dark honey-brown area on basis and apex (Figs 4A-C; 5A, C, F); yellow maculation on pronotal lobe demarcated by translucent reddish brown band (Figs 4C; 5B, C); coxae, trochanters and femurs of all legs brown with slight dark-olive-green metallic sheen; profemur with lighter-brown apical area; protibia and tarsus lighter honey-brown, tibia with longitudinal yellow stripe dorsally in basal 1/2; meso-and metatibiae and basitarsi lighter brown, following tarsomeres honey-brown; meso-and metatibiae with tiny pale-yellow spot on base of dorsal surface (Figs 4C; 5B, C). Pubescence: whitish, simple and sparse, shorter and sparser on head, denser on venter, longer on labrum (very coarse), sides of mesosoma, metasoma (T3-T6) and legs, especially on metafemur and tibia; longest setae on face between ocelli (1.5DO, much finer), very short on clypeus, lower paraocular, supraclypeal, and vertexal areas (0.5DO); gena nearly glabrous; sides of mesepisternum with relatively dense, long, uniformly distributed pilosity (1.5DO); posterior 2/3 of mesoscutum nearly glabrous; plumose setae easily visible only on pronotal lobe and its surroundings (very short, whitish silver), surrounding propodeal spiracle and on metatibia (ca. 3DO); pilosity on metasoma simple, gradually longer and denser toward apex; denser on base and apical border of tergum; T1-T3 with glabrous area on disc; T4-T6 evenly setaceous; setae on sterna ca. 2.25DO. Microsculpture: Integument impunctate, polished and shiny on most of surface; punctation piliferous, deep and sparse. Punctures denser and deeper on supraclypeal area, anterior 1/3 of mesoscutum, mesepisternum and T4-T6, punctures larger on face and smaller on mesoscutellum; metanotum and propodeum very coarsely microreticulate between sparse punctures; finely microreticulate area on lower paraocular area, between antennal alveolus and tentorial pit, also near epistomal suture on upper half of clypeus (Fig. 5E); gena nearly impunctate, smooth and polished with some very superficial large punctures in middle longitudinally on yellow stripe and some denser and deeper punctures in upper portion (Fig. 5C); mesoscutum with punctation large, dense and deep on anterior 1/3, posterior 2/3 nearly smooth and polished, except for contours with dense small punctures; mesoscutellum with punctation very fine and dense, and smooth polished area on each side of disc; T1-T3 with punctation very fine and sparse, and broad glabrous smooth polished area on each side of disc; T4-T6 with punctation evenly dense, coarse and marked.

Observed variations.
In females, the large elliptical yellow longitudinal maculation on the disc of the clypeus is sometimes enlarged apically, as observed in some specimens from Piauí State; these also have a small translucent brown oval maculation in the middle of the disc (Fig. 5F), invading the area of the wide brownish honeyyellow band on the apical third of the clypeus.
Distribution (new geographical records indicated by*). Ceratina manni is endemic to northeastern Brazil and occurs mainly within the limits of the Caatinga region (Fig. 10), being recorded from near sea level to 945 m a.s.l. The records from João Pessoa and vicinity by Cruz (2013) (Fig. 10).
Remarks. Wilms (1995:52) reported C. manni from the Boracéia Biological Station (2 females), located in Salesópolis, São Paulo, southeastern Brazil. These specimens would have been deposited in the Zoological Museum of São Paulo University (MZSP) and examined by Pedro and Camargo (2000). Unfortunately, the material collected by Wilms (1995) and cited by Pedro and Camargo (2000), Silveira et al. (2002), Imperatriz-Fonseca et al. (2011), and in the Discover Life website (2020 - Table 2) could not be located, so this record must be verified. Additionally, this record from Boraceia is from the Atlantic Forest in southeastern Brazil, far from the Caatinga, at an altitude of approximately 800 m a.s.l. and in a tropical rain forest with more than 3000 mm mean annual rainfall (Wilms 1995).
Identification key for females of Ceratina (Ceratinula) Moure, 1941 Species so far recorded for Brazil, according to the "Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region" (Moure 2012).
The identification key presented above is probably not exhaustive, as there are likely to be many species that have not yet been described or recorded in Brazil, but are known from neighboring countries. Therefore, we recommend that the characters be verified in the original descriptions and with a reference collection or type material, in order to more confidently assign species names.  (Fig. 8C); scape, pedicel and first three flagellomeres dark blackish brown (Fig. 5A); upper corners of clypeus and adjacent paraocular region with microreticulation clearly visible (Figs 5E; 8C); protibia and tarsus yellow-honey; trochanters, femurs and tibiae of meso-and metalegs blackened (Fig. 5B); genal yellow stripe located in upper region of gena, diverging from orbit in upper portion (Fig. 5C); antennal sockets located in shallow depression, frons and supraclypeal area raised above clypeus and median paraocular region (Fig. 5A, E), head sutures shallow; supraclypeal plain raised surface subtriangular (Fig. 9A, B)  8A; 9A, B); yellow maculations on lower paraocular area smaller, rounded, below tentorial pit (Fig. 8A); scape, pedicel and first three flagellomeres yellow-honey; upper corners of clypeus and adjacent paraocular area with smooth polished surfaces (Figs 1A; 8A); pro, meso and metalegs completely honey-yellow (Fig. 1B); * Ceratina combinata Friese, 1910 was not included in the key because it was described based only on a male specimen, which according to the author himself may be the male of C. muelleri Friese, 1910 genal stripe located in lower genal region, adjacent to orbit (Fig. 1C)

Conclusions
As stressed by Moure (1941:78-83), the pattern of yellow maculation is extremely important for distinguishing many species of Ceratina (Ceratinula), and most species were previously described were based on differences in the locations of the yellow maculation, especially on the head and legs. Integumental macrosculpture is also considered an important character in a species diagnosis, but primarily for species without yellow maculation. The yellow maculation is more useful for distinguishing females, as the patterns of yellow maculation of males are very similar among species. With the exception of C. (C.) combinata and C. (C.) minima, which were described from and known only from male specimens, the Brazilian fauna of Ceratina (Ceratinula) has been described based on females, with shape and presence or absence of these yellow maculations explained in the original descriptions.
The identification key presented above is probably not exhaustive, as there are likely to be many species that have not yet been described or recorded in Brazil, but are known from neighboring countries. Therefore, we recommend that the characters be verified in the original descriptions and with a reference collection or type material, in order to more confidently assign species names. Cockerell (1912) described C. (Ceratinula) manni based on six female specimens collected in Guarabira, Paraíba, Brazil. Until the present contribution, in addition to the type locality, the species had been reported in only two states in northeastern Brazil and from a limited number of specimens: Paraíba, near the coast and in the Atlantic Forest Domain, in Mamanguape (2 females and 2 males) (Aguiar and Martins 2003); three localities in and near João Pessoa (in the unpublished Master's dissertation of Cruz 2013); and in Cacimba de Dentro, a city in the Caatinga Domain, but near the type locality (1 female) (Zanella and Martins 2005); and the state of Rio Grande do Norte, in Serra Negra do Norte, in the middle of Seridó, one of the driest regions in the Caatinga Domain (2 females and 1 male) (Zanella 2000(Zanella , 2003. The new geographical records (Bahia: Amélia Rodrigues, Milagres, Maracás; Ceará: Crato; and Piauí: Caracol) expand its distribution considerably to the west and south, but still in the Caatinga Domain or in an ecotone with the Atlantic Forest (open dry diagonal), e.g., Amélia Rodrigues in Bahia (Fig. 10). The new records clearly establish the distribution of C. (Ceratinula) manni in the entire semiarid region of northeastern Brazil (Fig. 10), extending to nearby open-vegetation areas.
Several unidentified specimens of Ceratina (Ceratinula) have been reported in local inventories of bee faunas (some of them cited in the Introduction). Although we have not yet had access to the specimens collected in these surveys, this suggests that the species richness is higher than presently recorded, and that much more collection effort and taxonomic work is necessary to gain a comprehensive knowledge of the diversity and distribution patterns within the subgenus.
Apifaunistic surveys are particularly important sources of floral records for bees on their host plants (Sabino et al. 2011), leveraging data from direct field observations. Surveys also extend taxonomic and biogeographic knowledge, especially regarding species distributions, and are important for assessing pollinator abundance, local richness, and geographic and temporal variations therein, as well as for proposing conservation actions. The only flower records for C.