Ceratina (Ceratinula) manni Cockerell, 1912

Oliveira, Favizia Freitas de, Silva, Livia Raquel de Sousa, Zanella, Fernando Cesar Vieira, Garcia, Caroline Tito, Pereira, Heber Luiz, Quaglierini, Claudia & Pigozzo, Camila Magalhaes, 2020, 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), ZooKeys 1006, pp. 137-165 : 137

Ceratina (Ceratinula) manni Cockerell, 1912 Figures 4 , 5 , 6 , 7 , 8 , 9 , 10

Ceratina manni Cockerell, 1912: 47 [original description]; Schwarz 1943:30 [citation]; Michener 1954: 152 [citation]; ITS, 2009 [online catalog, geographic distribution]; Discover Life 2020 [online catalog, geographic distribution].

Ceratinula manni : Zanella 2000: 591 [biogeography]; Zanella 2003: 235 [biogeography];

Ceratina (Ceratinula) manni : Silveira et al. 2002: 146 [partim; geographic distribution]; Aguiar and Martins 2003: 213 [biogeography]; Zanella and Martins 2005: 383 [biogeography]; Moure et al. 2012 [online catalog, geographic distribution]; Cruz 2013 [floral visit record].

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 ).

Description.

♀: Structure (mm): total body length 4.7; forewing length 3.2; head width 1.3; eye length 0.89, width 0.43; gena width in profile 0.26; ocellocular distance 0.33; diameter of median ocellus 0.12; upper interorbital distance 0.91, median interorbital distance 0.78, lower interorbital distance 0.67; clypeus length 0.43, width 0.61; labrum length 0.22, width 0.44; scape length 0.31, width 0.09; F1 length 0.09; F2 length 0.05; F3 length 0.05; metatibia length 0.54, width 0.16; T2 width 1.25; T4 width 1.45. Antennal sockets located in shallow depression (Fig. 8C ), frons and supraclypeal area raised above clypeus and median paraocular region, head sutures shallow; a puncture line delimiting the supraclypeal plain raised area above, with lateral branches divergent basally, maximum diameter of puncture on line ca. 1 DS basally; supraclypeal plain raised surface subtriangular (Figs 5A, E, F ; 8C ; 9C, D ). Coloration: integument mostly dark metallic golden-olive-green (Figs 4A-C ; 5A-F ), except following parts: large elliptical longitudinal yellow maculation in median paraocular area, extending upward and downward from level of antennal socket, almost filling the entire space between the eye and antennal socket, and almost reaching the height of upper part of the epistomal suture (maculation width ca. 1.4DS, length 2.4DS, ending at a height ca. 0.5DS - scape maximum width - Figs 5A, E, F ; 8C ; 9C, D ); large yellow subtriangular longitudinal maculation on disc of clypeus (Figs 4A, B ; 5A, D, E, F ; 8C ); oval relatively large yellow maculation on lower paraocular areas near tentorial pit (Figs 4A, B ; 5A, 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.

♂: Structure (mm): total body length 3.9; forewing length 3.06; head width 1.3; eye length 0.76, width 0.46; gena width in profile 0.23; ocellocular distance 0.24; diameter of median ocellus 0.12; upper interorbital distance 0.84, medium interorbital distance 0.61, lower interorbital distance 0.57; clypeus length 0.49, width 0.57; labrum length 0.21, width 0.33; scape length 0.23, width 0.08; F1 length 0.05; F2 length 0.04; F3 length 0.06; metatibia length 0.5, width 0.14; metasomal width 1.19 (measured on T4). Antennal sockets located in shallow depression (Fig. 8D ), frons and supraclypeal area raised above clypeus and median paraocular area, head sutures shallow (Fig. 6A ); comparing with the female: eyes closer medially, scape shorter and wider, gena narrower in profile (Fig. 6D ). Male terminalia: 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 ); S7 quite narrow and less sclerotized, almost transparent in median portion which is wider, apical margin rounded (Fig. 7D ; this structure was broken, with part missing, and not possible to see in its entirety); gonostyle robust, enlarged and recurved, with an angulation in the median and preapical portion almost forming a 90 degrees, lateral-distal surface flattened, apical portion directed to valves ending in narrow bidentate apex (Fig. 7A ); valves slender in apical 1/2, hook-shaped, with dentiform projection dorsomedially, which is connected to base by less-sclerotized, transparent membranous portion (Fig. 7A-C ). Coloration: similar to that of female (Fig. 6A-D ) except clypeus yellow, narrowly black along epistomal suture from tentorial pit upward, honey-brown translucent stripe on apical border and darker irregularly rounded honey-brown translucent maculation in middle of disc (Fig. 6A, C ); labrum yellow, paler than clypeus, with paired oval translucent brown maculation laterally, and apical margin translucent brown (Fig. 6C ); lower paraocular area yellow from slightly below base of clypeus downward, upper margin of maculation rounded (Figs 6A, C , 8D ); mandible yellow, brownish at base and apex (Fig. 6C ); gena without yellow stripe (Fig. 6B, D ); apex of scape lighter brown; legs with small yellow maculation on apices of femurs and base of tibiae; wide yellow stripe on protibia, from base to apex, occupying almost entire dorsal surface (Fig. 6B, D ); tarsus entirely yellow (Fig. 6B ). Pubescence: pilosity whitish as in female, slightly shorter and sparse, especially on mesoscutum, terga and legs. Microsculpture: punctures smaller and sparser, interspaces much larger, especially on mesoscutum, mesepisternum and tergum; clypeus smooth, polished and shiny on most surface; with smooth impunctate areas on T1-T3 slightly larger, as well as those of mesoscutellum; microreticulation of metanotum and basal area of propodeum shallower.

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 honey-yellow 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) in peri-urban and rural areas and in Mamanguape, all in Paraíba, indicate that the species is not restricted to the semiarid region, and occurs in other areas of open vegetation, at least near the limit of the Caatinga (open dry diagonal, or South American diagonal of open formations - Vanzolini 1974). The record from São Paulo state ( Salesópolis, Boracéia Biological Station - Wilms 1995), secondarily cited by Pedro and Camargo (2000), Imperatriz-Fonseca et al. (2011) and in the Discover Life website (2020 -Table 2 ) must be checked (see remarks below).

Brazil: * Piauí State: Caracol. * Ceará state: Crato. Rio Grande do Norte state: Serra Negra do Norte ( Zanella 2000, 2003). Paraíba state: Cacimba de Dentro ( Zanella and Martins 2005), Alhambra, Conde, João Pessoa ( Cruz 2013), Mamanguape ( Aguiar and Martins 2003). * Bahia state: Amélia Rodrigues, Maracás, Milagres.

Material examined

(11♀, 2♂). 1 ♂ // (CE-UNILA HYAP 6072) // Brasil, Rio Grande do Norte, Serra Negra do Norte, Estação Ecológica do Seridó, 17.xii.1994, Zanella FCV and Moura ON leg.; 1 ♀ // (CE-UNILA HYAP 6073) // Brasil, Rio Grande do Norte, Serra Negra do Norte, Estação Ecológica do Seridó, 30.xii.1994, Zanella FCV and Moura ON leg.; 1 ♀ // (CE-UNILA HYAP 3350) // Brasil, Paraíba, Cacimba de Dentro, Fazenda Cachoeira da Capivara, 25.x.2003, F. Zanella leg.; 1 ♀ // (CE-UNILA HYAP 1109) // Brasil, Piauí, Caracol, 518 m, 13.xii.2010, F. Zanella and A. Carvalho leg.; 1 ♀ // (CE-UNILA HYAP 1110) // Brasil, Piauí, Caracol, 518 m, 13.xii.2010, F. Zanella and A. Carvalho leg.; 1 ♂ // (CE-UNILA HYAP 1120) // Brasil, Ceará, Crato, Estrada para Exú, Encosta, 07.ii.2011, F. Zanella leg.; 1 ♀ // (CE-UNILA HYAP 1117) // Brasil, Bahia, Maracás, 13°26'33.8"S, 40°20'42.6"W, 945 m, 13.iii.2012, Zanella FCV. leg.; 1 ♀ // (CE-UNILA HYAP 1118) // Brasil, Bahia, Maracás, 13°26'33.8"S, 40°20'42.6"W, 945 m, 13.iii.2012, Zanella FCV. leg.; 1 ♀ // (CE-UNILA HYAP 1112) // Brasil, Bahia, Milagres, 12°54'19.2"S, 39°50'46.5"W, 758 m, 16.iii.2012, Zanella FCV. leg.; 1 ♀ // (CE-UNILA HYAP 1115) // Brasil, Bahia, Milagres, 12°54'19.2"S, 39°50'46.5"W, 758 m, 16.iii.2012, Zanella FCV. leg.; 1 ♀ // (BIOSIS-UFBA, Favízia 06380) // Brasil, Bahia, Amélia Rodrigues, 12°22'31.70"S, 38°46'05.82"W, 21.i.2017, Hora: 13:10 P. 11, n° 404, on flowers of Stemodia foliosa Benth. Silva, Anjos and Melo leg.; 1 ♀ // (BIOSIS-UFBA, Favízia 06381) // Brasil, Bahia, Amélia Rodrigues, 12°22'31.70"S, 38°46'5.82"W, 21.i.2017, Hora: 13:10 P. 11, n° 405, on flowers of Stemodia foliosa Benth. Silva, Anjos and Melo leg.; 1 ♀ // (BIOSIS-UFBA, Favízia 06382) // Brasil, Bahia, Amélia Rodrigues, 12°22'31.70"S, 38°46'5.82"W, 11.iii.2017, Hora: 10:00 P. 11, on flowers of Stemodia foliosa Benth. Silva, Anjos and Melo leg. (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).

Figures

Figure 4. Female syntype of Ceratina (Ceratinula) manni Cockerell, 1912 deposited at the Entomological Collection of the American Museum of Natural History (AMNH, New York, United States of America) A head in frontal view (Photograph: I _ HHG 3587) B body in dorsal view (Photograph: I _ HHG 3585) C body in lateral view (Photograph: I _ HHG 3586) D labels (Photograph: I _ HHG 3588). Ownership rights to these images and their copyright belong to AMNH and Hadel Go. Photographs by Copyright Hadel Go 2011 - 2016 downloaded from the Discover Life Website.

Figure 5. Female of Ceratina (Ceratinula) manni Cockerell, 1912 A head in frontal view B body in lateral view C head and mesosoma in lateral view D labrum in frontal view E median paraocular area and clypeus in detail F head in frontal view A, E specimen from Amelia Rodrigues, Bahia, deposited at the Reference Collection of the Laboratorio de Bionomia, Biogeografia e Sistematica de Insetos (BIOSIS), Federal University of Bahia (MHNBA-MZUFBA), in Salvador, Bahia, Brazil; Specimens B, C, F from Caracol, Piaui, and D Milagres, Bahia, deposited at the Entomological Collection of the Federal University of Integracao Latino-Americana (CE-UNILA), in Foz do Iguacu, Parana, Brazil.

Figure 6. Male of Ceratina (Ceratinula) manni Cockerell, 1912, specimen from Crato, Ceara, deposited at the Entomological Collection of the Federal University of Integracao Latino-Americana (CE-UNILA), in Foz do Iguacu, Parana, Brazil A head in frontal view B body in lateral view C labrum in frontal view D head and mesosoma in lateral view.

Figure 7. Male genitalia and associated metasomal sternum of Ceratina (Ceratinula) manni Cockerell, 1912, specimen from Serra Negra do Norte, Rio Grande do Norte, Brazil, deposited at the Entomological Collection of the Federal University of Integracao Latino-Americana (CE-UNILA), in Foz do Iguacu, Parana, Brazil A genital capsule in dorsal view (red arrow shows the bidentate apex) B genital capsule in ventral view C genital capsule in lateral view D seventh sternum in dorsal view (E 7) E sixth sternum in dorsal view (E 6) F fifth sternum in dorsal view (E 5).

Figure 8. Head of Ceratina (Ceratinula) Moure, 1941 species in frontal view A (female holotype) B (male paratype) Specimens of Ceratina (Ceratinula) fioreseana sp. nov., deposited at the Entomological Collection of the Natural History Museum of the Federal University of Bahia (MHNBA-MZUFBA), in Salvador, Bahia, Brazil C, D Ceratina (Ceratinula) manni Cockerell, 1912: C female specimen from Amelia Rodrigues, Bahia, deposited at the Reference Collection of the Laboratorio de Bionomia, Biogeografia e Sistematica de Insetos (BIOSIS), Federal University of Bahia (MHNBA-MZUFBA), in Salvador, Bahia, Brazil D male specimen from Crato, Ceara, deposited at the Entomological Collection of the Federal University of Integracao Latino-Americana (CE-UNILA), in Foz do Iguacu, Parana, Brazil. Drawings by Luisa de Lima Ruschioni.

Figure 9. Head of Ceratina (Ceratinula) Moure, 1941 species in frontal view, showing the supraclypeal area and median paraocular area A, B female holotype of Ceratina (Ceratinula) fioreseana sp. nov., specimen deposited at the Entomological Collection of the Natural History Museum of the Federal University of Bahia (MHNBA-MZUFBA), in Salvador, Bahia, Brazil C, D female specimen of Ceratina (Ceratinula) manni Cockerell, 1912 from Amelia Rodrigues, Bahia, deposited at the Reference Collection of the Laboratorio de Bionomia, Biogeografia e Sistematica de Insetos (BIOSIS), Federal University of Bahia (MHNBA-MZUFBA), in Salvador, Bahia, Brazil. Details: pls = puncture line delimiting the supraclypeal plain raised area above; ues = upper part of the epistomal suture.

Figure 10. Geographic distribution map of Ceratina (Ceratinula) fioreseana sp. nov. and Ceratina (Ceratinula) manni Cockerell, 1912 in and Brazil: (1) Goias, Agua Fria de Goias, Fazenda Nossa Senhora Aparecida, Bayer Forward Farming (Ceratina fioreseana Type locality); (2) Bahia, Maracas; (3) Bahia, Milagres; (4) Bahia, Amelia Rodrigues; (5) Piaui, Caracol; (6) Ceara, Crato; (7) Rio Grande do Norte, Serra Negra do Norte, Estacao Ecologica do Serido; (8) Paraiba, Cacimba de Dentro, Fazenda Cachoeira da Capivara; (9) Paraiba, Mamanguape; (10) Paraiba, Joao Pessoa, Periurban Area - Sitio ponta de Gramame; (11) Paraiba, Conde, Granja Pitumirim; (12) Paraiba, Alhandra, Assentamento Tapuiu - Sitio Olho D'agua; (13) Paraiba, Guarabira (Ceratina manni Type locality).