Two new species of Euglossa from South America, with notes on their taxonomic affinities (Hymenoptera, Apidae)

Abstract Two new species of the genus Euglossa Latreille, subgenus Glossurella Dressler are here presented. Euglossa (Glossurella) embera sp. n., from the Pacific lowlands of Colombia, and Euglossa (Glossurella) adiastola sp. n., from the Atlantic Forest of Brazil. Their taxonomic association and distinction are discussed, as well as the correct understanding of the subgenus Glossurella.


Introduction
The appealing external morphology and interesting behavioral features of orchid bees make them one of the most notorious groups among the Neotropical bee fauna. Males of this group of bees have a characteristic set of secondary sexual morphological features involved in the collection of aromatic substances from floral and non-floral resources, notably from flowers of Orchidaceae (Dressler 1982a). The aromatic compounds are exposed during mating (Eltz et al. 2005). Of the five genera comprising the group, Euglossa Latreille is the most diverse with around 130 species (Nemésio and Rasmussen 2011). Since the discovery of the chemicals involved in the attraction of euglossine males to orchid flowers (Dodson et al. 1969), numerous new species have been described. Revision of historical material, discovery of new suites of morphological features, and access to newly collected sets of specimens in recent years has contributed to the recognition of various new species, particularly in Euglossa (e.g., Engel 2007, 2011a, b;Hinojosa-Díaz et al. 2011;Nemésio 2007Nemésio , 2011bNemésio , 2011cParra et al. 2006;Ramírez 2005Ramírez , 2006Rasmussen and Skov 2006). Here we describe and illustrate two new species of Euglossa in the subgenus Glossurella Dressler, one from the Pacific lowlands of Colombia and another from the Atlantic Forest of Brazil. We discuss the taxonomic affiliation of both species and one possible re-interpretation of the subgenus Glossurella in the light of current phylogenetic hypotheses.

Material and methods
Specimens here examined belong to the following institutions: Division of Entomology, University of Kansas Natural History Museum, Lawrence, Kansas, USA (SEMC), and the Entomological Collection, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil (UFMG). Label information for each specimen is presented enclosed by quotation marks (""), each label separated by double slash symbols (//), and every row on individual labels separated by a semicolon in italics (;), all of this followed by the number and sex of individuals corresponding to that dataset.
Diagnosis. Labiomaxillary complex in repose surpassing tip of metasoma by about one metasomal tergum length in the male (Figs 1-2), slightly shorter than metasoma in the female (Figs 3-4); both sexes with integument coloration light blue-green in the head, metasoma and mesosoma green with strong golden-bronzy coloration on dorsal areas as well as on metasomal sterna (Figs 1-4), male paraocular ivory marks narrow, not noticeably widened on lower sections, in most specimens not reaching epistomal sulcus (Figs 2, 5); male mandible tridentate, middle tooth reduced; female mesoscutellar tuft tear-drop shaped, occupying two thirds of mesoscutellar length (Fig. 3); female metabasitarsus trapezoidal with narrower straight distal margin, anterior and posterior margins convex (Fig. 9); metasomal terga in both sexes with dense punctures, becoming slightly shallower towards posterior margin; male mesotibia as follows: michrotrichia (velvety area) with anterior margin noticeably sparser, posterior margin obliquely truncate distally (Fig. 7), anterior mesotibial tuft ellipsoidal, proximal margin concave, and posterior mesotibial tuft elongated antero-posteriorly (Fig. 8); male metatibial shape scalene obtuse triangular, metatibial organ slit of male metatibia with basal section tear-drop shaped, distal section narrow and noticeably elongated, only separated from tibial ventral margin by less than the organ's distal section maximum width (Fig. 10), Figures 5-13. Euglossa embera sp. n. 5 Facial aspect of male holotype 6 Facial aspect of female paratype 7 Outer surface of male mesotibia (arrow pointing to oblique truncation of velvety area) 8 Mesotibial tufts of male 9 Outer view of female metatibia and metatarsus 10 Outer view of male metatibia and metatarsus (arrow pointing to distal-most extreme of organ slit) 11 Inner view of male metatibia and metatarsus (arrow pointing to circular depression) 12 Section of male second metasomal sternum 13 Dorsal view of pronotal dorso-lateral angle (arrow) of male.
inner surface with notorious circular depression near metabasitarsal joint (Fig. 11); male second metasomal sternum with two notorious omega-like integumental depressions (Fig. 12); male terminalia features as follows: eighth metasomal sternum with posterior section triangular (Fig. 15); dorsal process of gonocoxite thumb-like, about as long as broad (Fig. 18); lateral area of gonostylar process of gonocoxite projected as a short, broad prong; lateral section of gonostylus large, spoon-like, covered with dense, simple, long setae (Fig. 17). See also Table 1.
Coloration. Head light blue-green with golden-bronzy iridescence specially on paraocular areas, antennal depressions and preoccipital area; clypeal medial ridge dark brown; paraocular ivory marks thin but well developed, slightly wider below, in most specimens not reaching epistomal sulcus (separated from it by about their width); lower lateral parts of clypeus, labrum, malar area, and mandibles (except teeth) ivory; labral windows amber-translucent; antennal scape with ivory spot covering all lateral surface and part of anterior surface, scape otherwise dark brown as remainder of antenna (Fig. 5). Pronotum green, blue-purple lights on lower ventral areas, golden-bronzy iridescence all over; mesoscutum, mesoscutellum and tegula green with strong golden-bronzy iridescence, dominant (obscuring green coloration) on mesoscutum and mesoscutellum (Figs 1-2); mesepisternum green with golden-bronzy iridescence specially on lateral areas (not as marked as on mesoscutum), preomaular area with brownbrassy spot on upper lateral area (Fig. 15); metepisternum and propodeum concolor with lateral areas of mesepisternum plus some blue-green coloration on areas close to leg joints; legs mainly bottle green on outer surface (except all tarsomeres beyond basitarsa) with moderate golden-bronzy iridescence, inner surface of all podites and entire tarsomeres beyond basitarsi brown-brassy, blue-purple lights on outer-anterior margins of most podites, specially notorious on mesofemur and mesotibia (Figs 2, 7); wings glossy hyaline with brown veins (Figs 1-2). Metasomal terga green with strong golden-bronzy iridescence in a gradient, strong anteriorly (fully bronzy) to weaker posteriorly (green-golden-bronzy) (Fig. 1); sterna with same colors and pattern as terga.
Sculpturing. Face densely areolate-punctate, areole-puncture size around one third of median ocellar diameter on clypeal disc, one eighth on frons (frontal fringe), and somewhere in between in other areas, paraocular groove between paraocular marks and torulus smooth (Fig. 5), gena with areole-punctures comparable in size to those of clypeal disc, well marked above, shallow on lower areas. Mesoscutum with round punctures about one fifth of median ocellar diameter, dense (separated by less than a puncture diameter) on most areas, becoming slightly sparser along median mesoscutal line (separated by one to two puncture diameters), where smaller punctures (about one fourth of a regular puncture size) are intermixed sparsely; mesoscutellum with punctation as on mesal areas of mesoscutum (sparse punctures intermixed with smaller punctures), punctures becoming denser (contiguous) and bigger (at least double in size) on posterior area along mesoscutal margin (Fig. 1); mesepisternal lateral-facing surface with dense punctures on upper areas as big as punctures on frons, becoming slightly bigger and sparser towards lower areas (separated by one or more puncture diameters on ventral areas); preomaular area with punctation as a continuation of lateral-facing area of mesepisternum, except for impunctate brown-brassy spot; metatibial outer surface with punctures comparable in size to those on posterior margin of mesoscutellum, relatively dense (separated by less than one puncture diameter) on upper half, sparser (separated by two to three puncture diameters) on lower half, smooth (impunctate) on small depression contiguous to organ slit (Fig. 10). Dorsal surface of posterior half of first metasomal tergum and second through fifth terga with dense punctures, around half the size of regular mesoscutal punctures, becoming slightly shallower towards posterior margin, anterior half of first tergum, lateral sections of second through fifth terga, and entire surface of sixth and seventh terga with similar pattern but punctures as big as those on posterior margin of mesoscutellum (Fig. 1); metasomal sterna with relatively dense punctation (punctures of a varied size, but most comparable to those on mesepisternum), leaving large semicircular smooth areas mesally on every sternum.
Vestiture. Frontal fringe with dense setae of two natures, some brown, very minutely branched, straight, as long as two mid-ocellar diameters, the others, ambergolden, with noticeable but short branches, shorter than the brown setae; remainder of the face (except as noted hereafter) with scattered amber-golden setae (as the ones on frontal fringe), shorter on most areas, and noticeably plumose on antennal depressions; posterior section of vertex and mid-ocellar area with long curved brown setae; gena with dense, light, plumose setae, increasing in size towards lower genal section; antenna with scattered amber golden setae (Fig. 5). Mesoscutum and mesoscutellum densely setose, majority of setae amber-golden with few intermixed brown setae (these last notorious on anterolateral corners of mesoscutum) (Figs 1-2, 13); lateral-facing surface of mesepisternum, metepisternum and propodeum with, dense, pale, plumose setae as long as those on lower gena, some brown setae interspaced on pronotal lobe; preomaular area with setae as those on lateral-facing mesepisternal areas, except bare on preomaular spot and contiguous smooth area (Fig. 2); outer surface of all legs with light yellowish setae, moderately dense and short in most areas except as follows: dense, long (as long as those on lower gena) and plumose on posterior surface of foreleg, dense and erect downwards on anterior surface of mesotibia (Fig. 7), dense and appressed on mesobasitarsus, long (as long as those on vertex) and arranged in a fringe on distal half of postero-dorsal margin of metatibia, other leg setal features as follows: inner surface of all basitarsi with dense, hirsute, brown-amber setae, chemical gathering tufts on second through fourth protarsomeres with dense, brown-amber, moderately long, setae, microtrichia on outer mesotibial surface (velvety area) composed of dense, fulvous, simple, minute setae, anterior margin of velvety area noticeably sparser, distal third of posterior margin diagonally truncate (Fig. 7), anterior mesotibial tuft ellipsoidal with proximal margin concave, composed of dense, fulvous, minutely plumose setae, posterior tuft sitting on a deep cavity elongated antero-posteriorly, with a distinctive semicircular setose patch on posterior half, anterior inner margin of the cavity covered with a fringe of setae, all setae fulvous (Fig. 8); metatibial organ slit closed with dark brown setae (Fig. 10); inner metatibial depression devoid of setae (Fig. 11). Anterolateral corners of first tergum, with moderately dense, amber-golden, simple setae as long as those on mesoscutum, lateral areas of all terga and posterior margin of seventh tergum with similar setae but rather pale, dorsum of posterior half of first tergum and second through sixth terga with dense, appressed, grayish, minute setae, intermixed with scattered, sturdy, brown, short setae appressed, similar setae but appearing simple, shorter and appressed, on lateral margins of remainder terga, as well as posterior half of fifth tergum and entire surface of sixth to seventh terga; posterior dorsal half of first tergum through anterior half of fifth tergum with dense, dusky, appressed short setae, intermixed with some scattered, darker, longer setae (Figs 1, 2); metasomal sterna with moderately dense setae on punctate areas; integumental omega-like depressions on second sternum lined with amber, appressed, simple setae (Fig. 12).
Terminalia. Seventh metasomal sternum with posterior disc margin deeply emarginated mesally, bearing a row of scattered setae (Fig. 14). Eighth metasomal sternum with posterior section triangular (lateral margins straight) on dorsal or ventral view, covered with scattered, minute setae (Fig. 15). Dorsal process of gonocoxite thumblike, about as long as broad, basal incision broadly concave (Fig. 18); lateral area of gonostylar process of gonocoxite projected as a short, broad prong; lateral section of gonostylus large, spoon-like, ventral lobe with scattered, short, simple setae on outer surface, inner concave surface covered with dense, simple, long setae (Fig. 17).

Coloration. As described for male
Sculpturing. As described for male except no differentiation on preomaular area (preomaular spot absent); mesoscutellum with slightly denser punctation (Fig. 3).
Vestiture. As described for male (some setal features on protarsi, meso-and metatibia exclusive of male) except as follows: Mesoscutellar tuft tear-drop shaped, occupying about two thirds of mid mesoscutellar length, composed of dense, dark, erect, multibranched (branches minute) setae (Fig. 3). Foreleg with slightly shorter setae on posterior surface as compared to male (Fig. 6); mesotibial posterior margin with some scattered, dark, sturdy short setae; metatibial corbicula surrounded for the most part by setae as in other leg areas, except by some scattered, dark, sturdy, curved setae (Fig. 9).
Sculpturing. In general as described for E. embera, except as follows: punctation along median mesoscutal line not as sparse, although sparser than elsewhere; metatibial outer surface with denser punctation, area along ventral margin with punctures separated by one to two puncture diameters (Fig. 26).
Vestiture. In general as described for E. embera, except as follows: setae on mesoand metasoma, evenly fulvous, mesoscutum and mesoscutellum with a noticeable number of intermixed brown sturdy setae; anterior section of velvety area on mesotibia, sparser than in E. embera, distal third of posterior margin of velvety area rather concave (Fig. 24).
Terminalia. As described for E. embera. ♀: Unknown. Etymology. The specific epithet is based on the Greek word adiastolos, meaning "confused" or "not separated", as a reference to the confusion between this species and E. augaspis.

Discussion
The two new species described here are unequivocally related to E. bursigera Moure, E. augaspis Dressler, and E. prasina Dressler. The males of all of these species have characteristically tridentate mandibles and share a similar habitus, integumental sculpturing, and genitalic features. It is easy to separate E. prasina from those species by its distinctive metatibial shape (trapezoidal), and rather enlarged scape (see also Table 1). Before the addition of the species here described, it was relatively easy to distinguish E. bursigera and E. augaspis based on their distribution because the former is found in Central America (Moure 1970) while the second is found in the Amazon Basin (Dressler 1982b). Both species share a good amount of morphological similarity, and this is also the case for E. embera and E. adiastola. Euglossa embera is closer to E. bursigera, and although not from Central America, the type material is from a biogeographically related region, the Pacific lowlands of Colombia; E. adiastola on the other hand is more akin to E. augaspis.
The four males known for E. embera are remarkably uniform in their morphology which is not surprising given that all of them come from the same locality. This species can be differentiated from E. bursigera by the noticeably longer labiomaxillary complex of the male (clearly exceeding the metasomal tip while in repose), which does not surpass or barely surpasses the metasomal tip in E. bursigera; the slightly longer malar area in the male (length comparable to width of the mid-flagellomeres), which is much narrower than the mid-flagellomeres width in E. bursigera; and the posteriorly elongate distal section of the metatibial organ slit (separated from ventral metatibial margin by less than its maximum width), which in E. bursigera is separated from the ventral metatibial margin by more than the slit's maximum width (see Table 1). Coloration could also be used to differentiate these two species, although Moure (1970) described a subspecies of E. bursigera (E. bursigera cupreicolor), based on the dominant bronzyreddish coloration of specimens found principally (but not exclusively) in the Pacific slope of Costa Rica. Most of the Panamanian specimens of E. bursigera are, however, predominantly green. Collection of specimens in the contact areas of both E. bursigera and E. embera will help clarify the color variation in E. bursigera. Dressler (1982b), when describing E. augaspis, addressed the close morphological similarity of this species with E. bursigera from which he distinguished it by its distinctively smaller size and denser abdominal punctation. Euglossa adiastola, although definitely closer to E. augaspis, is noticeably larger, even slightly larger than E. bursigera. Besides size, E. adiastola can be distinguished from E. augaspis by the much thicker dorso-lateral angle of the prothorax and the well-developed middle tooth in the mandible.
The new species here presented together with E. bursigera, E. augaspis, and E. prasina are assigned to the subgenus Glossurella. When Dressler (1982b) originally erected the subgenus, he included a variety of species that share some biological (nesting) and external morphological features. However, currently available phylogenetic information based both on external morphology (Hinojosa-Díaz 2010) and molecular data (Ramírez et al. 2010) indicate that the group as envisioned by Dressler (1982b) is not supported as monophyletic. Since the type species for Glossurella is E. bursigera we tentatively restrict the use of this subgeneric name herein for those species allied to it. As so conceived, such a restricted Glossurella would encompass E. bursigera, E. augaspis, E. prasina, E. embera, and E. adiastola. Species formerly included in Glossurella but not part of the complex allied to E. bursigera, would then be regarded as incertae sedis in terms of their subgeneric placement within Euglossa and until such time as relationships are further resolved (e.g., Hinojosa-Díaz and Engel 2011b). Naturally, this is one of several classificatory options but is the one which offers the greatest nomenclatural stability for the moment.