Contents

ABSTRACT 2

INTRODUCTION 2

MATERIAL AND METHODS 3

SYSTEMATICS 4

Wallacetrigona incisa (Sakagami and Inoue), new combination 8

Genus Geniotrigona Moure 8

Key to Species of Geniotrigona 9

Geniotrigona thoracica (Smith) 9

Geniotrigona lacteifasciata (Cameron) 9

Key to Indomalayan and Australasian Genera and Subgenera of Meliponini (based on worker caste) 12

DISCUSSION 13

ACKNOWLEDGMENTS 14

REFERENCES 14

APPENDIX 16

AMERICAN MUSEUM NOVITATES

Number 3888: 33 pp. December 14, 2017

Copyright © American Museum of Natural History 2017

ISSN 0003-0082

A New Genus of Eastern Hemisphere Stingless Bees (Hymenoptera: Apidae), with a Key to the Supraspecific Groups of Indomalayan and Australasian Meliponini

CLAUS RASMUSSEN,1 JENNIFER C. THOMAS,2 AND MICHAEL S. ENGEL3

ABSTRACT

A new genus of stingless bees (Apinae: Meliponini) is described and figured from Indonesia (Sulawesi), known from a single species previously placed in Geniotrigona Moure. Based on recent phylogenetic studies, Trigona (Geniotrigona) incisa Sakagami and Inoue renders Geniotrigona polyphyletic and is more closely related to Lepidotrigona Moure. The species is transferred to Wallacetrigona Engel and Rasmussen, new genus, and differentiated from Geniotrigona proper as well as all other meliponines occurring in Sundaland, Wallacea, and Sahul (Australinea). The new genus occurs east of the Wallace Line and separate from the distribution of Geniotrigona, which is otherwise restricted to Sundaland, but Wallacetrigona is presently not known beyond the Weber Line. A hierarchical classification of Indomalayan and Australasian stingless bees is tabulated and a revised key to the genera and subgenera provided, as well as an appendix tabulating the species and synonyms. The following new combinations are established: Wallacetrigona incisa (Sakagami and Inoue), Homotrigona (Lophotrigona) canifrons (Smith), Homotrigona (Odontotrigona) haematoptera (Cockerell), Homotrigona (Tetrigona) apicalis (Smith), H. (T.) binghami (Schwarz), H. (T.) melanoleuca (Cockerell), H. (T.) peninsularis (Cockerell), and H. (T.) vidua (Lepeletier de Saint Fargeau).

INTRODUCTION

Bees are attractive insects that mostly visit flowers and secure pollination of plants (Michener, 2007). While most species live a solitary life, with a single female establishing and providing for the nest, some species of bees live in large perennial colonies where they store food as honey, known to humans since prehistory. While honey bees (species of Apis Linnaeus) are well-known for their honey products, the much larger, and more diverse, group of tropical and subtropical bees, the stingless bees (Apinae: Corbiculata: Meliponini) have regionally also played important roles as honey producers (e.g., Nogueiro-Neto, 1953; Cortopassi-Laurino et al., 2006; Heard, 2016), particularly in the Americas where no native honey bees cooccurred with humans (Apis occurred in the New World only prior to the Pliocene: Engel et al., 2009). There are about 500 species of stingless bees known, and the classification of this highly diverse group of pantropical bees comprises one of the greatest challenges among the diversifications of corbiculate apines.

The Indomalayan/Australasian clade of stingless bees (as defined by Rasmussen and Cameron, 2010), was traditionally treated as belonging to a single genus, Trigona Jurine (e.g., Schwarz, 1937). Schwarz (1939) was the first to propose two subgenera from the region, Heterotrigona Schwarz and Lepidotrigona Schwarz. The remaining stingless bee taxa were at the time placed in either the New World or Afrotropical (then) subgenera of Trigona: Tetragona Lepeletier and Audinet-Serville or Hypotrigona Cockerell. Finally, in 1961 Moure proposed a series of 11 genera that took into consideration the distinctiveness and diversity of the known Indomalayan/Australasian fauna (Moure, 1961). Two additional higher-level groups were proposed as Trigonella Sakagami and Moure (in Sakagami, 1975), replaced later as Sundatrigona Inoue and Sakagami (1993), and Papuatrigona Michener and Sakagami (1990). While the names were available, they were only reluctantly accepted and major works dealing with the classification, such as Michener (1990, 2007), refrained from removing the majority of the taxa from the New World genus of Trigona. Instead, they were merged into a restricted subset of subgenera within the otherwise New World genus Trigona. Recently, however, a phylogenetic study focused on the Old World fauna (Rasmussen and Cameron, 2007), and a comprehensive taxonomic catalog of the region (Rasmussen, 2008), emphasized the need to diverge from tradition and adopt a revised classification, closer in line to that advocated by Moure (1961), that more adequately reflected the inferred evolutionary relationships among these distinctive clades. In the study by Rasmussen and Cameron (2007), a distinct species originally described as Trigona (Geniotrigona) incisa Sakagami and Inoue from Sulawesi (Sakagami and Inoue, 1989) (fig. 1A) rendered the genus Geniotrigona Moure polyphyletic. Geniotrigona incisa was recovered with significant support as sister to Lepidotrigona. As the genus Lepidotrigona is morphologically and behaviorally distinct based on the unique plumose or scalelike setae along the mesoscutal margins (Schwarz, 1939) and oviposition rituals (Sakagami and Yamane, 1987), it was undesirable to accommodate G. incisa within that genus. Morphologically, G. incisa appeared only superficially related to other members of Geniotrigona and based on priority it was thus suggested that a new supraspecific name for G. incisa was needed (Rasmussen and Cameron, 2007, 2010).

Here we provide the description of the new stingless bee genus from Indonesia (Sulawesi) along with revised keys to the genera and subgenera of Indomalayan and Australasian Meliponini. An appendix is provided with a synonymic list of the Indomalayan stingless bees arranged according to the hierarchical organization of the genera and subgenera as used herein (table 1).

MATERIAL AND METHODS

Specimens of pertinent species were examined in the collections of the Division of Invertebrate Zoology, American Museum of Natural History, New York (AMNH); the Claus Rasmussen Collection, Aarhus University, Denmark (CRCD); California State Collection of Arthropods, California Department of Food and Agriculture, Sacramento, California (CSCA); and the Division of Entomology, University of Kansas Natural History Museum, Lawrence (SEMC), and included representatives of all currently recognized supraspecific groups of Indomalayan and Australasian stingless bees. Standard, translingual typographic symbols for sex and caste are employed in reporting specimens examined: ♀, for reproductive female (= queen caste); ♂, for reproductive male (= drone caste of highly eusocial species); ⚲, for sterile or nonreproductive female (= worker caste). Morphological terminology is adapted from Engel (2001) and Michener (2007), while the general format used for the descriptions is augmented from those provided by Moure (1961) and Sakagami (1975). Terms for the various stages of vein development and reduction follow those of Mason (1986). Greek letters are used herein to denote proximal or distal subsections of the individual vein abscissae of 1Cu. The forewing 1Cu extends from the divergence of M from Cu to the placement of 1m-cu, distal of which Cu then angles toward the posterior wing margin as 2Cu. Depending on the position of 1cu-a, 1Cu may at times be divided into two subsections (i.e., when 1cu-a is antefurcal the vein is simply 1Cu, but if 1cu-a is postfurcal and meets 1Cu, then 1Cu may be segregated into a proximal and apical portion). Sharkey and Wharton (1997) advocated using “1Cua” and “1Cub” to distinguish between these two units when 1Cu is subdivided by 1cu-a, thereby preserving the homology of the entire abscissae of 1Cu and 2Cu more broadly. We agree with this scheme although have preferred the use of Greek letters: 1Cuα for the proximal section and 1Cuβ for the distal section. Such usage avoids any potential confusion with the lowercase Roman letters for crossveins (e.g., 1cu-a) or the broader entomological system for distinguishing between anterior and posterior sectors of longitudinal veins (e.g., CuA). Contrary to some other usage, however, we have not restricted the numbering of abscissae to proximal, middle, and distal, and used additional numbering, particularly in relation to the abscissae of Rs and M. Microphotography was done by J.C.T. with the aid of an Infinity K-2 long-distance lens attached to a Canon EOS 7 digital camera, and the images then edited, cropped, arranged, and labeled in Adobe Photoshop by M.S.E. The descriptions are provided to enhance our understanding of general patterns among Indomalayan and Australasian bees, patterns that form the foundation for broader evolutionary interpretations (Grimaldi and Engel, 2007), as well as modernize the circumscription of taxa within the region (Gonzalez et al., 2013).

SYSTEMATICS

Tribe Meliponini Lepeletier de Saint Fargeau

Wallacetrigona Engel and Rasmussen, new genus

Type species: Trigona (Geniotrigona) incisa Sakagami and Inoue, 1989.

Diagnosis: The genus Wallacetrigona is most similar to Geniotrigona (see below), in which its type species was initially placed. The genus can be distinguished from Geniotrigona by the narrowly concave emargination (= interdental incision) separating the two preapical teeth (broadly concave interdental incision in Geniotrigona); the absence of a strongly elevated ridge posteriorly on the vertex (present in Geniotrigona); the presence of a deep, U- or V-shaped concave incision medially on the posterior border of the vertex (absent in all other Indomalayan and Australasian taxa); the absence of a dense covering of short, plumose setae on the mesoscutum (present in Geniotrigona); the apical metasomal terga with short, scattered plumose setae amid longer, erect, black setae (plumose setae of Geniotrigona longer); keirotrichiate zone of metatibial inner surface about as broad as or slightly broader than posterior glabrate zone, and subequal to the length of the apical glabrate zone.

Description: Workers of moderate size, forewing length approximately 7.0–8.0 mm; integument fairly shiny (fig. 1A), smooth, with scattered microscopic punctures (some of which are setigerous) giving appearance of fine imbrication or tessellation on face (fig. 2A), gena, and apical margins of metasomal terga, but otherwise without distinctive sculpturing; integumental maculation absent; with fine, minute, plumose pubescence on face and clypeus and fine, plumose pubescence on mesosoma particularly numerous on metanotum, metepisternum, and propodeal lateral surfaces but not greatly obscuring integument; apical metasomal terga without dense, elongate, apically plumose setae (such setae present in Geniotrigona).

Head as broad as mesosoma, with face broader than compound eye length (fig. 2A); vertex with faint depression immediately posterior to ocelli and with faint transverse ridge before occipital border but never elevated above level of ocelli (figs. 3A, 3B) (vertex with depression immediately posterior to ocelli and with posterior border greatly elevated as ridge above ocelli in frontal view in Geniotrigona: figs. 2C, 6A, 6B), with deep, concave, medial notch along border with rounded preoccipital ridge (immediately posterior to median ocellus), notch approximately 0.3× ocellar diameter (notch shallow, narrow, and scarcely evident in Geniotrigona); ocelloccipital distance slightly greater than one ocellar diameter; interocellar distance approximately 2.5× ocellar diameter; ocellocular distance 2.5× ocellar diameter; scape longer than torulocellar distance; second flagellomere longer than first, second and third flagellomeres subequal in length; second through 10th flagellomeres each longer than wide; intertorular distance a little less than one-half torulorbital distance; upper torular (“alveolar” in the terminology of Moure, 1961, and Sakagami, 1975) tangent at about facial midlength; frontal carina present but faint; inner orbit of compound eye weakly concave in upper third; gena slightly broader than compound eye in profile, posterior border rounded; malar area elongate, nearly twice as long as flagellar diameter (figs. 2A, 3A, 3B); labrum flat, large, wider than long, apical margin medially concave; mandible bidentate, teeth well defined and incised (i.e., interdental spaces distinct) (fig. 3C) (but not broadly concavely incised, i.e., with interdental spaces deep, as in Homotrigona Moure), interdental incision between first and second preapical teeth (teeth of the pollex sensu Michener and Fraser, 1978) angulate (fig. 3C) (broadly orthogonal or concave in Geniotrigona: fig. 6D); galea with longitudinal rows of long, erect, apically hooked, brightly colored setae; first and second labial palpomeres with numerous, elongate, strongly apically wavy but simple setae (see also Michener and Roubik, 1993) (similar to those setae present in Geniotrigona: figs. 2D, 6C).

Mesoscutum with median sulcus weakly impressed; notauli short and scarcely evident; parapsidal lines short, length less than ocellar diameter, and weakly impressed. Mesoscutellum short, ending at profile of metanotum and not overhanging propodeum, rounded, swollen in profile, with shining transverse depression along mesoscuto-mesoscutellar sulcus. Propodeum declivitous, with shallow change in slope between basal area and posterior surface; basal area smooth, glabrous, and shining; propodeal spiracle elongate, 8× as long as wide.

Forewing extending beyond apex of metasoma (fig. 1A), with 2Rs, 1rs-m, 1m-cu, apical half 3M, 4M, apical half 1Cuβ, 2Cu, 3Cu, and 2cu-a indicated by brownish nebulous traces and fenestrae demarcated by white spectral lines on otherwise infuscate wing membrane (fig. 3D); membrane with dark brown microtrichia; prestigma short, scarcely longer than anterior width of 1Rs; pterostigma slender; marginal cell slightly less than 4× as long as maximum breadth, separated from wing apex by slightly more than its maximum width, with apex narrowly open, opening less than one-fifth maximum marginal cell width, with nebulous, angled, appendiculate apex to 4Rs; 1M basad 1cu-a (1M either basad or confluent with 1cu-a in Geniotrigona), thus short 1Cuα present, 1Cuα shorter than 1cu-a; submarginal angle (i.e., anterior angle between 1Rs and Rs+M), nearly orthogonal; M obtusely angled at 1m-cu (i.e., angle between 2M and 3M); 3M tubular in basal half, then nebulous; 2Rs angulate; 1rs-m straight; r-rs about as long as 3Rs. Hind wing with 8–9 distal hamuli; radial and cubital cells closed by nebulous veins.

Metatibia slightly less than 3× as long as greatest width, elongate clavate (figs. 4A, 4B); posterior margin gently recurved with subangulate distal angle (fig. 4B) (recurved with rounded distal angle in Geniotrigona: figs. 4C, 4D), setae along posterior margin and upper outer surface mostly plumose; outer surface weakly concave apically, with corbicula occupying apical third (fig. 4A); apical margin transverse; inner surface with narrow, elevated keirotrichiate zone and broad subglabrous zone (figs. 4B, 5A), with abrupt clivulus4; keirotrichiate zone about as broad as or slightly broader than posterior glabrate zone (figs. 4B, 5A) (narrower than posterior glabrate zone in Geniotrigona: figs. 4D, 5B), width of keirotrichiate zone subequal to length of apical glabrate zone (figs. 4B, 5A) (greater than length of apical glabrate zone in Geniotrigona: figs. 4D, 5B); penicillus and rastellar comb present, each composed of stiff setae. Metabasitarsus lightly concave and trapezoidal, with posterior margin arched, distal angle not projecting (figs. 4A, 4B, 5A); outer surface with small basal posterior fimbriate field; inner surface with short basal sericeous area (figs. 4B, 5A).

Metasoma narrow, with first metasomal tergum smooth and shining, second through fourth terga largely smooth and shining except narrow apical marginal zones microscopically punctate; apical half of fifth and entire postgradular surface of sixth terga with short, plumose setae intermixed amid stiff, erect, black setae, plumose setae distinctly shorter than thicker erect, black setae and not densely covering integument (such setae as long as or longer than black setae, apically plumose, and dense in Geniotrigona).

Etymology: The generic name honors Alfred Russel Wallace (1823–1913), an intrepid and early explorer of the Indomalayan insect fauna and coauthor with Charles R. Darwin (1809–1882) of the theory of evolution. The gender of the name is feminine.

Included species: Presently the genus is understood to only include the type species, Wallacetrigona incisa (Sakagami and Inoue), new combination, from Indonesia (Sulawesi), east of the important faunal boundary known as the Wallace Line (and part of the biogeographic area known as Wallacea).

FIGURE 1. Lateral habitus of workers. A. Wallacetrigona incisa (Sakagami and Inoue). B. Geniotrigona thoracica (Smith). C. G. lacteifasciata (Cameron).

FIGURE 2. Facial views and mouthparts of workers. A. Facial view of Wallacetrigona incisa (Sakagami and Inoue). B. Facial view of G. lacteifasciata (Cameron). C. Facial view Geniotrigona thoracica (Smith). D. Lateral view of extended mouthparts of G. lacteifasciata, note erect, hooked setae of galea and wavy setae of basal labial palpomeres.

FIGURE 3. Morphological details of Wallacetrigona incisa (Sakagami and Inoue), worker caste. A. Head in profile. B. Head and anterior mesosoma in profile. C. Mandible outer surface, with preapical teeth (P1 and P2) labeled. D. Forewing with prominent veins and crossveins labeled.

FIGURE 4. Metatibiae and metatarsi of workers. A. Outer surface of Wallacetrigona incisa (Sakagami and Inoue). B. Inner surface of W. incisa. C. Outer surface of Geniotrigona thoracica (Smith). D. Inner surface of G. thoracica.

FIGURE 5. Inner surfaces of worker metatibiae and metarsi, with prominent zones and areas colored and labeled (green = keirotrichiate zone; yellow = posterior glabrate zone; red = lower glabrate zone blending into anterior surface; pink = basal sericeous area). A. Wallacetrigona incisa (Sakagami and Inoue). B. Geniotrigona thoracica (Smith).

FIGURE 6. Morphological details of Geniotrigona thoracica (Smith), worker caste. A. Head in profile. B. Head and anterior mesosoma in profile. C. Oblique view of lower face, with mouthparts extended to show hooked galeal setae and wavy setae ventrally on basal labial palpomeres. D. Mandible outer surface, with preapical teeth (P1 and P2) labeled.

Wallacetrigona incisa (Sakagami and Inoue), new combination

Figures 1A, 2A, 3, 4A, 4B, 5A, 11E

Trigona (Geniotrigona) incisa Sakagami and Inoue, 1989: 605.

Geniotrigona incisa (Sakagami and Inoue); Rasmussen, 2008: 11.

Material examined (n = 22⚲⚲): INDONESIA: Sulawesi: 8⚲⚲, Indonesia: Central Sulawesi, 8 km N Sedoa, Kec. [Kecamatan] Lore Utara [North Lore District], Kab. Poso [Kabupaten Poso, a.k.a. Poso Regency], 1500 m, XI-10-1995 [10 November 1995], G.W. Otis, ex: at honey bait [120.29°, -1.22°] (SEMC); 12⚲⚲, Indonesia: Central Sulawesi, 8 km N Sedoa, Kec. [Kecamatan] Lore Utara [North Lore District], Kab. Poso [Kabupaten Poso, a.k.a. Poso Regency], 1500 m, XI-10-1995, G.W. Otis, ex: at honey bait [120.29°, -1.22°] (CRCD); 2⚲⚲, Indonesia: C. Sulawesi, Kamarora, Survey Site 12, Waterfall, 24 ix 1996 [24 September 1996], 800m, G.W. Otis [55 km SE of Palu, 120.14°, -1.22°] (CRCD).

Additional localities: Although we have not examined specimens from the following localities in Sulawesi, the following were reported by Sakagami and Inoue (1989): N. Celebes [North Sulawesi], Minahasa [Peninsula], Modoinding [124.45°, 0.80°]; C. Celebes, Todyamboe [Tojambu, actually South Sulawesi], 900 m [120.10°, -2.93°]; Sulawesi, Sulteng, Kab. Poso [Kabupaten Poso, a.k.a. Poso Regency, Central Sulawesi], Wuasa [120.29°, -1.42°]; Central Sulawesi, Lore Lindu National Park [120.19°, -1.47°]; Gn. [Gunung] Tokosa [Central Sulawesi], 2100–2200 m [120.04°, -1.35°]; Lake Tambing [in Poso Regency, Central Sulawesi], Mal. Trap 5 [Malaise trap 5], swamp [120.31°, -1.33°]. According to J.S. Ascher (pers. comm.), an additional specimen is present in the Essig Museum of Entomology, University of California, Berkeley: [South] Sulawesi, Latimojong, along aqueduct, 1350 m, 9 Aug 2016, Pete Obovski [120.10°, -3.40°].

Genus Geniotrigona Moure

Geniotrigona Moure, 1961: 212. Type species: Trigona thoracica Smith, 1857, by original designation.

Diagnosis: The genus Geniotrigona is distinctive among Indomalayan Meliponini owing to the combination of its large size; elongate malar space (more than twice diameter of the third flagellomere) (figs. 1B, 1C, 2B, 2C, 6A, 6B); short mesoscutellum; short, declivitous propodeum; distinctively raised ridge posteriorly on the vertex (figs. 1B, 6A, 6B); and comparatively short, dense, plumose setae that largely obscure the integument on the mesosoma. It is most similar to the new genus described above, but can be distinguished by those features outlined there (above).

Included species: Presently, the genus includes two species: Geniotrigona thoracica (Smith) and G. lacteifasciata (Cameron).

Key to Species of Geniotrigona

1. Anterior corners of mesoscutum covered in golden, brushlike setae; wings markedly bicolored (Malaysia: Sabah, Sarawak; Indonesia: West Kalimantan) .....G. lacteifasciata (Cameron)

– Anterior corners of mesoscutum covered in dark brown, brushlike setae; wings weakly bicolored (Thailand, Laos, Vietnam, Singapore, Malaysia, Indonesia: Sumatra).....G. thoracica (Smith)

Geniotrigona thoracica (Smith)

Figures 1B, 2C, 4C, 4D, 5B, 6

Trigona thoracica Smith, 1857: 50.

Melipona thoracica (Smith); Dalla Torre, 1896: 584.

Trigona ambusta Cockerell, 1918: 387. Synonymy vide Schwarz (1939).

Trigona thoracica variety ambusta (Cockerell); Schwarz, 1937: 327.

Trigona (Tetragona) thoracica Smith; Schwarz, 1939: 104.

Geniotrigona thoracica (Smith); Moure, 1961: 212.

Trigona (Geniotrigona) thoracica Smith; Sakagami, 1975: 56.

Trigona (Heterotrigona) thoracica Smith; Michener, 1990: 126.

Material examined (n = 98⚲⚲, 10♂♂): MALAYSIA: Kedah: 1⚲, Malay Penin. [Malay Peninsula], Kedah, Alor Setar, Gunong Keriang, April 1, 1928 (AMNH); Pahang: 1⚲, Frasers Hill, F.M.S. [Federated Malay States], 30.ix.29 [30 September 1929], N.C.E. Miller (AMNH); 1⚲, Malay Penin. [Malay Peninsula], Pahang, F.M.S. [Federated Malay States], Jerantut, Datu Dalan [?], March 19, 1927 (AMNH); Perak: 1⚲, Malaya, Maxwell Gardens, Taiping Hills, 3300 ft., 12.xi.1931 [12 November 1931], H.T. Pagden (AMNH); Selangor: 2⚲⚲, Malaysia: Selangor, Kepong, 9-VIII-2004, H.R. Hepburn, ex: caught on flowers (SEMC); 3⚲⚲, Malaysia: Selangor, Phoon Chun Guan, March 1980, R9, Azhar P.C. Guan (SEMC); 7⚲⚲, Malaysia: Selangor, Kepong, Sept. 1976, S. Appanah (SEMC); 2⚲⚲, Malaysia, W. Selangor, Serdaag, 1983, on Brazil nut (SEMC); 1⚲, Malaya, Bukit Kutu [peak near Kuala Kubu], 30.i.1930 [30 January 1930], H.T. Pagden, 3485 ft. (AMNH); Kuala Lumpur: 18⚲⚲, Malaysia: Kepong Forest Res. Inst., 18 October 1975, Rudolf Jander (SEMC); 1⚲, Malay Penin. [Malay Peninsula], ex: Coll. Agr. Dept. Kuala Lumpur, April 23, 1909 (AMNH); Johor: 1⚲, Malaysia: Johor, 15.3 km W. Sedili Besar, 16 Oct 1986, John W. Wenzel (SEMC); Malacca: 1⚲, Malacca, Kuala Kubu [it is unclear which locality Buttel-Reepen is referring to as “Kuala Kubu” is in Selangor, we have merely listed it as it appears on his label], 3.1912 [March 1912], Butt.-Reep. [Buttel-Reepen] (AMNH); SINGAPORE: 14⚲⚲, Singapore, Bukit Timah, 12 Oct 1986, J.W. Wenzel (SEMC); THAILAND: Sisaket: 1⚲, Thailand, Sisaket, Huai Thap Than Distr., 25.iii.2004, S. Thummajitsakul (SEMC); Prachuap Khiri Khan: 2⚲⚲, Thailand, Prachuap Khiri Khan, Thap Sakae Distr., 12.ii.2006, S. Thummajitsakul (SEMC); 7⚲⚲, Thailand: Prachuap Khiri Khan Prov., Huai Yang waterfall, 25 km SW Prachuap Khiri Khan, 27 January 1993, S. Boongird, C. Michener (SEMC); 6⚲⚲, Thailand: Prachuabkirikan Prov., Huay Yang Waterfall, 30.iii.2004, S. Boongird (SEMC); 1⚲, Thailand, Thap-Sakae, 2.9.76 [2 September 1976], Pauly rec, composit, radiee, blanche (CRC); Ranong: 1⚲, S. Thailand, hills above hot springs, 29.4.08 [29 April 2008], Ranong, Ranong Prov., Hans Bänziger leg. (SEMC); 8⚲⚲, Thailand: Ranong Prov., Muang Distr., 9–13 Nov 2002, Samnuk [sic: Somnuk] Boongird (SEMC); 3♂♂, Thailand, Ngao, A. Muang, Ranong, 16.12.03 [16 December 2003], [S. Boongird] (SEMC); Surat Thani: 2⚲⚲, Thailand, Surat Thani, Chaiya Distr., 20.x.2003, S. Thummajitsakul (SEMC); Phang Nga: 2⚲⚲, Thailand, Phang Nga Prov., Khao Sok National Park, between Takua Pa and Khao Mok, March 2000, D.R. Smith (SEMC); Krabi: 5⚲⚲, Thailand: Krabi Prov., Owluk Distr., 8–15 Nov 2002, Samnuk [sic: Somnuk] Boongird (SEMC); 7♂♂, Thailand: Krabi Prov., Khoa Phanom Distr., 13.v.2004, S. Boongird (SEMC); Songkhla: 4⚲⚲, Ban Prakamp, Song Kalo Prov. [Songkhla Province], vii.18.28 [18 July 1928], Siam [Thailand] (AMNH); INDONESIA: North Sumatra (Sumatera Utara): 4⚲⚲, O. Sumatra [Ost Sumatra], [illegible], 7.1932 [July 1932] (AMNH); South Sumatra (Sumatera Selatan): 1⚲, S. Sumatra [South Sumatra], Kedaton, 150 m, 28 Maart 1937 [28 March 1937], J.v.d. Vecht (AMNH); 1⚲, Z. Sumatra [Zuid Sumatra], Ranau [Lake Ranau], 24.viii.33 [24 August 1933], H.R.A. Miller (AMNH).

Geniotrigona lacteifasciata (Cameron)

Figures 1C, 2B, 2D, 11D

Trigona lacteifasciata Cameron, 1902: 131.

Trigona borneënsis Friese, 1933a: 46. Synonymy vide Schwarz (1939).

Trigona thoracica variety lacteifasciata Cameron; Schwarz, 1937: 317.

Trigona thoracica variety borneënsis Friese; Schwarz, 1937: 328.

Geniotrigona lacteifasciata (Cameron); Moure, 1961: 213.

Material examined (n = 21⚲⚲): MALAYSIA: Sabah (Borneo): 1⚲, Malaysian Borneo: Sabah, Kampung Bam Bam (20 km SW of Tenom), 06-VIII-2009 [6 August 2009], R.S. Hepburn (SEMC); 2⚲⚲, Malaysia: Sabah (Borneo), Penampang Distr., Crocker Range, Kipandi Butterfly Park, 720 m, 5°52’20’’N, 116°14’53’’E, 15.x.2011 [15 October 2011], M. Hauser and S. Gaimari (SEMC, CSCA); 10⚲⚲, Malaysia, Sabah, near Sek. Keb. Labang, at the Sapulut River, 20–27.vii.2005 [20–27 July 2005], 300 m, Claus Rasmussen leg. (CRCD); 1⚲, Sabah, Babagon, 7.vii.1968 [7 July 1968], P.J.L. Roche (SEMC); 1⚲, Sabah, Sandakan, 3.viii.1985 [3 August 1985], C.G. Roche (SEMC); 1⚲, Sabah, Sepilok F.R., 14.vii.1968 [14 July 1968], C.G. Roche (SEMC); Sarawak (Borneo): 1⚲, Lundu, Sarawak, April 1913 (AMNH); INDONESIA: West Kalimantan: 4⚲⚲, Borneo, Sanggau [Sanggau Regency], 24.7.32 [24 July 1932] (AMNH).

FIGURE 7. Anatomical details of the minute genera of Indomalayan Meliponini. A. Forewing of Lisotrigona carpenteri Engel, with pertinent veins and crossveins labeled. B. Facial view of L. carpenteri. C. Facial view of Pariotrigona pendleburyi (Schwarz).

FIGURE 8. Anatomical details of Austroplebeia cincta (Mocsáry). A. Facial view. B. Dorsal view. C. Inner surface of metatibia and metatarsus. D. Inner surface of metatibia colored using the same scheme as presented in figure 5.

FIGURE 9. Anatomical details of various genera of Indomalayan and Australasian genera of Meliponini.
A. Dorsal view of head and mesosoma of Lepidotrigona terminata (Smith). B. Dorsal view of head and mesosoma of Papuatrigona genalis (Friese). C. Propodeum of L. terminata. D. Mandible of Homotrigona (Homotrigona) fimbriata (Smith). E. Outer surface of metatibia, metabasitarsus, and two further metatarsomeres of L. doipaensis (Schwarz).

FIGURE 10. Forewing venation of Tetragonula (Tetragonilla) atripes (Smith). A. Unadulterated wing with pertinent veins labeled. B. Wing with particular sectors of veins and crossveins colored to highlight homologous portions and positions of nebulous and spectral traces.

FIGURE 11. Anatomical details of various genera of Indomalayan and Australasian genera of Meliponini.
A. Profile of upper mesosoma of Heterotrigona (Heterotrigona) itama (Cockerell). B. Profile of upper mesosoma of Tetragonula (Tetragonilla) collina (Smith). C. Propodeum of Homotrigona (Lophotrigona) canifrons (Smith). D. Metasomal apex of Geniotrigona lacteifasciata (Cameron). E. Ocellar triangle and medial vertex of Wallacetrigona incisa (Sakagami and Inoue), with arrow indicating posterior, medial, U-shaped incision.

Key to Indomalayan and Australasian Genera and Subgenera of Meliponini (based on worker caste)

Given the introduction of a new genus along with the significant alteration of the generic classification (e.g., Rasmussen, 2008) since Michener’s (2007) recent key to the fauna, we provide here a new dichotomous identification key to the genera and subgenera as conceived herein.

1. Forewing length less than 3 mm, wing venation greatly reduced (fig. 7) and posterior margin of metatibia without plumose setae; hind wing without closed cells, veins closing radial and cubital cells, if visible at all, clear and unpigmented (spectral); forewing with 2Rs and 1rs-m almost always completely absent, thus without indication of submarginal cells (fig. 7); at least distal part of second cubital cell of forewing undefined or defined completely by unpigmented spectral vein traces (i.e., at least 2Cu and 3Cu absent or spectral); vein M of forewing terminating without bend at about position of anterior end of 1m-cu which, however, is absent (i.e., 3M lacking) .....2

– Forewing length typically over 4 mm, wing venation typically not greatly reduced for Meliponini, but if minute and with some wing reduction, then posterior margin of metatibia with plumose setae intermixed with simple setae; hind wing typically with radial and cubital cells closed by at least weakly brownish nebulous veins; forewing with one or two submarginal cells usually weakly indicated by nebulous traces of 2Rs and 1rs-m (fig. 3D), first submarginal cell usually recognizable; second cubital cell of forewing completely indicated by at least faint nebulous veins (i.e., 2Cu present); vein M of forewing usually extending at least slightly beyond position of 1m-cu and angular at apex of tubular portion of vein (i.e., 3M present) (fig. 3D), the stub of which is usually at least faintly visible .....3

2. Malar space shorter than flagellar diameter (fig. 7B); inner margins of compound eyes converging below (fig. 7B); worker gonostylus with many minute setae, in addition to setae along outer and distal margins (India; Vietnam; Laos; Cambodia; Thailand; Malaysia: Sarawak, Sabah; Indonesia: Sumatra) .....Lisotrigona Moure

– Malar space almost one-fifth as long as compound eye, much longer than flagellar diameter (fig. 7C); inner margins of compound eyes nearly parallel (fig. 7C); worker gonostylus with setae but without minute setae (Thailand; Malaysia: West Malaysia, Sarawak, Sabah; Brunei; Indonesia: Sumatra) .....Pariotrigona Moure

3. Head and mesosoma without distinct maculation; inner surface of metatibia with strong longitudinal keirotrichiate ridge above which is a broad, depressed shining marginal area .....4

– Mesoscutellum and usually face and mesoscutum with well-developed yellow maculation (figs. 8A, 8B); inner surface of metatibia with keirotrichiate area broad, nearly reaching posterior margin of metatibia (figs. 8C, 8D) (Australia; Papua New Guinea; Indonesia: Irian Jaya [West Papua]) .....Austroplebeia Moure

4. Setae along posterior margin of worker metatibia and males entirely simple, or some plumose only on apical one-fifth or one-sixth of margin; keirotrichiate median zone of inner surface of metatibia separated from shining posterior marginal zone by gentle slope .....5

– Setae along posterior margin of worker metatibia and some males partly plumose; elevated keirotrichiate median zone of inner surface of metatibia separated from shining posterior marginal zone by abrupt slope .....6

5. Mesoscutum margined with whitish, densely plumose (scalelike) setae (fig. 9A); head and mesosoma dull, with minute close punctures (fig. 9A); propodeal dorsum finely reticulate (fig. 9C); posterior margin of worker metatibia without plumose setae (fig. 9E); (Indomalaya [Sundaland]) .....Lepidotrigona Moure

– Mesoscutum without conspicuous plumose setae (fig. 9B); head and mesosoma shining, although with minute, rather close punctures (fig. 9B); propodeal dorsum smooth, shining; posterior margin of worker metatibia with plumose setae among bristles on apical one-fifth or one-sixth of margin (Indonesia: Irian Jaya [West Papua]; Papua New Guinea) .....Papuatrigona Michener and Sakagami

6. Mesoscutellum short, only slightly projecting over metanotum (best seen in profile, fig. 11A); malar area variable, typically as long as diameter of diameter of third flagellomere or greater but sometimes approximately 0.5–0.75× diameter of third flagellomere; vein M of forewing bent at trace of 1m-cu, sometimes present only as minute stub beyond bend (e.g., fig. 3D) .....7

– Mesoscutellum well projected posteriorly, extending over propodeum as far as posterior propodeal angle (change in slope between basal area and posterior surface) (best seen in profile, fig. 11B); malar area linear or at least narrower than 0.5× diameter of third flagellomere; vein M of forewing straight and ending at or shortly after 1m-cu (fig. 10) (Tetragonula Moure, s.l.) .....10

7. Malar space less than 2× diameter of third flagellomere .....8

– Malar space 2× or greater diameter of third flagellomere (figs. 2, 3A, 3B, 6A, 6B) .....9

8. Mandible unidentate or bidentate, teeth small (Heterotrigona Schwarz, s.l.) .....11

– Mandible bidentate, teeth large, deeply incised, i.e., interdental spaces deep (fig. 9D) (Homotrigona Moure, s.l.) .....14

9. Vertex with deep depression and elevated ridge rising above level of ocelli (figs. 6A, 6B), posteriorly without deep, concave, medial notch; mesoscutum with dense covering of short, plumose setae amid scattered erect, black setae; apical metasomal terga with dense, long, apically plumose setae amid erect, black setae, with plumose setae at least as long as black setae (fig. 11D); keirotrichiate zone of metatibial inner surface narrower than posterior glabrate zone, and greater than length of apical glabrate zone (figs. 4C, 4D, 5B) (Myanmar; Cambodia; Thailand; Singapore; Malaysia: West Malaysia, Sarawak, Sabah; Indonesia: Kalimantan, Sumatra) .....Geniotrigona Moure

– Vertex without strongly elevated ridge, with faint transverse depression and ridge posterior to ocelli (fig. 3A), posteriorly with deep, concave medial incision (fig. 11E); mesoscutum without dense covering of short, plumose setae amid scattered erect, black setae; apical metasomal terga with short, scattered plumose setae amid longer, erect, black setae; keirotrichiate zone of metatibial inner surface about as broad as or slightly broader than posterior glabrate zone, and subequal to length of apical glabrate zone (figs. 4A, 4B, 5A) (Indonesia: Sulawesi) .....Wallacetrigona, n. gen.

10. Scape shorter than torulocellar distance; about five distal hamuli; posterior contour of metatibia slightly convex, with distal angle subangulate; penicillus usually composed of soft setae (India to Australia and Solomon Islands) .....Tetragonula Moure, s.str.

– Scape at least as long as torulocellar distance; six distal hamuli; posterior contour of metatibia distinctly convex and distal angle rounded almost without angulation; penicillus composed of stiff setae (Cambodia; Vietnam; Laos; Myanmar; Thailand; Malaysia: West Malaysia, Sarawak, Sabah; Brunei; Indonesia: Sumatra, Kalimantan).....Tetragonilla Moure

11. Basal area of propodeum largely or entirely glabrous, at most with wispy apicolateral patches of setae .....12

– Basal area of propodeum entirely pubescent (fig. 11C), or with a small medial glabrous patch (in H. hobbyi (Schwarz)) (Indonesia: Irian Jaya [West Papua, Papua], Moluccas; Papua New Guinea) .....Platytrigona Moure

12. Basal vein (1M) of forewing basad 1cu-a .....13

– Basal vein (1M) of forewing distad 1cu-a (Indonesia [Papua]; Papua New Guinea) .....Sahulotrigona Engel and Rasmussen

13. Posterior glabrate zone of metatibial inner surface apically broader than keirotrichiate zone; forewing length more than 5.5 mm (Thailand; Singapore; Malaysia: West Malaysia, Sarawak, Sabah; Brunei; Indonesia: Java, Sumatra, Kalimantan) .....Heterotrigona Schwarz, s.str.

– Posterior glabrate zone of metatibial inner surface apically narrower than or at most as broad as keirotrichiate zone; forewing length less than 6.0 mm (Singapore; Malaysia: West Malaysia, Sarawak; Indonesia: Sumatra) .....Sundatrigona Inoue and Sakagami

14. Basal sericeous area of metabasitarsus present; clypeus approximately 2× broader than long .....15

– Basal sericeous area of metabasitarsus absent; clypeus short, at least 2.5× broader than long (Thailand; Laos; Singapore; Vietnam; Cambodia; Indonesia: Sumatra, Kalimantan; Brunei; Malaysia: West Malaysia, Sarawak; Myanmar) .....Homotrigona Moure, s.str.

15. Basal area of propodeum smooth and glabrous; vertex not elevated posterior to ocelli .....16

– Basal area of propodeum pubescent; vertex elevated posterior to ocelli (Thailand; Malaysia: West Malaysia, Sarawak, Sabah; Singapore; Indonesia: Sumatra, Kalimantan; Myanmar; Sri Lanka; Australia) .....Lophotrigona Moure

16. Malar space as long as flagellar diameter; clypeus with a transverse row of erect setae along apical margin; metabasitarsus 2× as long as wide (Cambodia; Malaysia: Sarawak, Sabah, West Malaysia; Brunei; Myanmar; Indonesia: Sumatra, West Timor, Kalimantan; East Timor; Thailand; Laos; Vietnam) .....Tetrigona Moure

– Malar space about as long as 1.5× flagellar diameter; clypeus with erect black setae scattered over entire surface; metabasitarsus less than 1.5× as long as wide (Malaysia: Sarawak, Sabah; Brunei) .....Odontotrigona Moure

DISCUSSION

The classification of stingless bees has made tremendous strides during the last 20 years (table 2), although there remains significant challenges. Recognizing their diversity is merely the first step toward properly assessing their classification, and we have here emphasized both the hidden diversity in the Eastern Hemisphere as well as the importance of the Wallace Line for the stingless bees of the region (e.g., Vane-Wright, 1991). At present, Wallacetrigona incisa is known only from Sulawesi, where it has been captured at localities ranging from 800–2200 m (fig. 12). While the Australasian fauna of stingless bees is rather species poor compared to the Indomalayan fauna (Dollin et al., 1997, 2015; Rasmussen, 2008), Wallacetrigona is the third endemic genus/subgenus of stingless bees to be reported from the easternmost range of meliponines, the others being Austroplebeia Moure and Heterotrigona (Papuatrigona). Species of Tetragonula and Lepidotrigona are also found east of the Wallace Line, but not near the diversity known from the island of Borneo or continental Southeast Asia. Extensive sampling of stingless bees throughout the Sunda Islands, Wallacea, and the western limits of the Sahul is needed to clarify the biogeographic limits and history of these lineages. In addition, considerable effort is needed to resolve species circumscriptions for groups such as Tetragonula where numerous, presumably cryptic species exist, sometimes distinguishable more by morphometrics and biology than clear demarcations among workers. It is hoped that by providing an easier means for identifying monophyletic genera and subgenera among the fauna there shall be a growing number of melittologists investigating the bees of the Indomalayan and Australasian regions. A tremendous interest in local stingless bees is already seen from the increase in beekeepers and producers of the highly appraised and valued “kelulut” honey produced by meliponines, likely including W. incisa.

FIGURE 12. Collection localities of individuals of Wallacetrigona incisa (Sakagami and Inoue) in Indonesia (Sulawesi). Specimens are those either examined here or reported in the literature (refer to text). The species is apparently restricted to mountainous areas of Sulawesi as all localities are at elevations above 800 m.

ACKNOWLEDGMENTS

We are grateful to Gard W. Otis and Alain Pauly for providing some of the specimens used as part of this study, to John S. Ascher for providing an additional specimen record, and to Sydney A. Cameron for discussing the implications of the initial molecular work that suggested the distinctiveness of the taxon. The manuscript received helpful input from Jerome G. Rozen, Jr., and an anonymous reviewer. This is a contribution of the Division of Entomology, University of Kansas Natural History Museum.

REFERENCES

Bingham, C.T. 1897. The fauna of British India, including Ceylon and Burma. Hymenoptera. Vol. 1, wasps and bees. London: Taylor and Francis, xxix + 579 pp., +4 pls.

Bingham, C.T. 1903. Diagnoses of aceuleate Hymenoptera. In N. Annandale, and H.C. Robinson (editors), Fasciculi malayenses: anthropological and zoological results of an expedition to Perak and the Siamese Malay States, 1901–1902. Zoology, part 2: iii–vii. London: University Press of Liverpool, 201–304 + vii pp., + pls. xi–xiv.

Cameron, P. 1897. Hymenoptera orientalia, or contributions to a knowledge of the Hymenoptera of the Oriental zoological realm. Part 5. Memoirs and Proceedings of the Manchester Literary and Philosophical Society 41 (4): 1–144, +2 pls.

Cameron, P. 1901. On the Hymenoptera collected during the “Skeat Expedition” to the Malay Peninsula, 1899–1900. Proceedings of the Zoological Society of London 2 (1): 16–44.

Cameron, P. 1902. On the Hymenoptera collected by Mr. Robert Shelford at Sarawak, and on the Hymenoptera of the Sarawak Museum. Journal of the Straits Branch of the Royal Asiatic Society 37: 29–131.

Cameron, P. 1908. On some Bornean species of Trigona (Apidae). Entomologist 41 (543): 192–195.

Cockerell, T.D.A. 1905. Descriptions and records of bees – I. Annals and Magazine of Natural History (7) 16 (92): 216–225.

Cockerell, T.D.A. 1910. New and little known bees. Transactions of the American Entomological Society 36 (3–4): 199–249.

Cockerell, T.D.A. 1911. The bees of the Solomon Islands. Proceedings of the Linnean Society of New South Wales 36 (1): 160–178.

Cockerell, T.D.A. 1912. Descriptions and records of bees – XLII. Annals and Magazine of Natural History (8) 9 (50): 220–229.

Cockerell, T.D.A. 1915. Descriptions and records of bees – LXVIII. Annals and Magazine of Natural History (8) 16 (91): 1–9.

Cockerell, T.D.A. 1918. Descriptions and records of bees – LXXX. Annals and Magazine of Natural History (9) 2 (10): 384–390.

Cockerell, T.D.A. 1919a. Descriptions and records of bees – LXXXV. Annals and Magazine of Natural History (9) 3 (15): 240–250.

Cockerell, T.D.A. 1919b. The social bees of the Philippine Islands. Philippine Journal of Science 14 (1): 77–81.

Cockerell, T.D.A. 1920. Descriptions and records of bees – LXXXVIII. Annals and Magazine of Natural History (9) 5 (25): 113–119.

Cockerell, T.D.A. 1925. Descriptions and records of bees – CIV. Annals and Magazine of Natural History (9) 15 (88): 489–496.

Cockerell, T.D.A. 1926. Descriptions and records of bees – CXII. Annals and Magazine of Natural History (9) 18 (104): 216–227.

Cockerell, T.D.A. 1927. Bees from the Malay Peninsula. Annals and Magazine of Natural History (9) 20 (119): 530–541.

Cockerell, T.D.A. 1929a. Bees in the Australian Museum collection. Records of the Australian Museum 17 (5): 199–243.

Cockerell, T.D.A. 1929b. Descriptions and records of bees – CXVII. Annals and Magazine of Natural History (10) 4 (19): 131–141.

Cockerell, T.D.A. 1929c. Descriptions and records of bees – CXX. Annals and Magazine of Natural History (10) 4 (24): 584–594.

Cockerell, T.D.A. 1929d. Bees in the Queensland Museum. Memoirs of the Queensland Museum 9 (111): 298–323.

Cockerell, T.D.A. 1929e. Bees from the Australian region. American Museum Novitates 346: 1–18.

Cockerell, T.D.A. 1934. Some African meliponine bees. Revue de Zoologie et de Botanique Africaines 26 (1): 46–62.

Cortopassi-Laurino, M., et al. 2006. Global meliponiculture: challenges and opportunities. Apidologie 37 (2): 275–292.

Dalla Torre, C.G., de [K.W., von]. 1896. Catalogus hymenopterorum hucusque descriptorum systematicus et synonymicus. Vol. 10, Apidae (Anthophila). Lipsiae [Leipzig]: Engelmann, viii + 643 pp. 

Dollin, A.E., L.J. Dollin, and S.F. Sakagami. 1997. Australian stingless bees of the genus Trigona (Hymenoptera: Apidae). Invertebrate Taxonomy 11 (6): 861–896.

Dollin, A.E., L.J. Dollin, and C. Rasmussen. 2015. Australian and New Guinean stingless bees of the genus Austroplebeia Moure (Hymenoptera: Apidae)—a revision. Zootaxa 4047: 1–73.

Dover, C. 1929. Wasps and bees in the Raffles Museum, Singapore. Bulletin of the Raffles Museum 2: 43–70.

Eardley, C.D. 2004. Taxonomic revision of the African stingless bees (Apoidea: Apidae: Apinae: Meliponini). African Plant Protection 10 (2): 63–96.

Eardley, C.D., and R. Urban. 2010. Catalogue of Afrotropical bees (Hymenoptera: Apoidea: Apiformes). Zootaxa 2455: 1–548.

Engel, M.S. 2000. A review of the Indo-Malayan meliponine genus Lisotrigona, with two new species (Hymenoptera: Apidae). Oriental Insects 34: 229–237.

Engel, M.S. 2001. A monograph of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bulletin of the American Museum of Natural History 259: 1–192.

Engel, M.S., and C.D. Michener. 2013. A minute stingless bee in Eocene Fushun [sic] amber from northeastern China (Hymenoptera: Apidae). Journal of Melittology 14: 1–10.

Engel, M.S., and C. Rasmussen. 2017. A new subgenus of Heterotrigona from New Guinea (Hymenoptera: Apidae). Journal of Melittology 73: 1–16.

Engel, M.S., I.A. Hinojosa-Díaz, and A.P. Rasnitsyn. 2009. A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae: Apini). Proceedings of the California Academy of Sciences (Series 4) 60 (3): 23–38.

Engel, M.S., C.D. Michener, and Y. Boontop. 2017. Notes on Southeast Asian stingless bees of the genus Tetragonula (Hymenoptera: Apidae), with the description of a new species from Thailand. American Museum Novitates 3886: 1–17.

Franck, P., E. Cameron, G. Good, J.-Y. Rasplus, and B.P. Oldroyd. 2004. Nest architecture and genetic differentiation in a species complex of Australian stingless bees. Molecular Ecology 13 (8): 2317–2331.

Friese, H. 1898. Die Trigona-Arten Australiens. Természetrajzi Füzetek 21 (3–4): 427–431.

Friese, H. 1900. Neue Arten der Bienengattungen Melipona Ill., und Trigona Jur. Természetrajzi Füzetek 23: 381–394.

Friese, H. 1901. Neue Arten der Bienengattung Trigona Jur. (Hym.). Zeitschrift für systematische Hymenopterologie und Dipterologie 1 (5): 265–271.

Friese, H. 1908 [1909]. Hymenoptera II. Apidae. In A. Wichmann (editor), Nova Guinea. Résultats de l’expédition scientifique néerlandaise à la Nouvelle-Guinée en 1903. Vol. 5, Zoologie [Lieferung 3]: 353–359, + pl. xv. Leiden: Brill, v + 651 pp., +28 pls.

Friese, H. 1909. Die Bienenfauna von Neu-Guinea. Annales Historico-Naturales Musei Nationalis Hungarici 7: 179–288.

Friese, H. 1918. Wissenschaftliche Ergebnisse einer Forschungsreise nach Ostindien, ausgeführt im Auftrage der Kgl. Preuß Akademie der Wissenschaften zu Berlin von H. v. Buttel-Reepen. VII. Bienen aus Sumatra, Java, Malakka und Ceylon. Gesammelt von Herrn Prof. Dr. v. Buttel-Reepen in den Jahren 1911–1912. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Tiere 41 (5): 489–520.

Friese, H. 1925. Neue neotropischen Bienenarten, zugleich II. Nachtrag zur Bienenfauna von Costa Rica (Hym.). Stettiner Entomologische Zeitung 86 (2): 1–41.

Friese, H. 1933a. Neue Trigona-Arten von Borneo (Hym.). Natuurhistorisch Maandblad 22 (4): 45–46.

Friese, H. 1933b. Eine neue Trigona von Sumatra (Hymenoptera, Apidae). Natuurhistorisch Maandblad 22 (12): 147.

Gonzalez, V.H., T. Griswold, and M.S. Engel. 2013. Obtaining a better taxonomic understanding of native bees: where do we start? Systematic Entomology 38 (4): 645–653.

Gribodo, G. 1891. Contribuzioni imenotterologiche sopra alcune specie nuove o poco conosciute di imenotteri antofili (generi Ctenoplectra, Xylocopa, Centris, Psithyrus, Trigona, e Bombus). Bollettino della Società Entomologica Italiana 23: 102–119.

Gribodo, G. 1893. Note imenotterologische. Nota II. Nuovi generi e nuove specie di imenotteri antofili ed osservazioni sopra alcune specie già conosciute. Bollettino della Società Entomologica Italiana 25: 248–287.

Grimaldi, D., and M.S. Engel. 2007. Why descriptive science still matters. BioScience 57 (8): 646–647.

Heard, T. 2016. The Australian native bee book: keeping stingless bee hives for pets, pollination and sugarbag honey. West End: Sugarbag Bees, x + 246 pp.

Horne, C., and F. Smith. 1870. Notes on the habits of some hymenopterous insects from the north-west provinces of India, with an appendix containing descriptions of some new species of Apidae and Vespidae collected by Mr. Horne. Transactions of the Zoological Society of London 7 (3): 161–196, + pls. xix–xxii.

Illiger, K. 1806. William Kirby’s Familien der Bienenartigen Insekten mit Zusätzen, Nachweisungen und Bemerkungen. Magazin für Insektenkunde 5: 28–175.

Inoue, T., and S.F. Sakagami. 1993. A new name of Trigona (Hymenoptera, Apidae). Japanese Journal of Entomology 61 (4): 769.

Jobiraj, T., and T.C. Narendran. 2004. A revised key to the world species of Lisotrigona Moure (Hymenoptera: Apoidea: Apidae) with description of a new species from India. Entomon 29 (1): 39–43.

Lepeletier de Saint Fargeau, A.L.M. 1836. Histoire naturelle des insectes – hyménoptères [vol. 1]. Paris: Roret, 547 pp.

Mason, W.R.M. 1986. Standard drawing conventions and definitions for venational and other features of wings of Hymenoptera. Proceedings of the Entomological Society of Washington 88 (1): 1–7.

Michener, C.D. 1990. Classification of the Apidae (Hymenoptera). University of Kansas Science Bulletin 54 (4): 75–163.

Michener, C.D. 2000. The bees of the world. Baltimore: Johns Hopkins University Press, xiv + [i] + 913 pp., +16 pls.

Michener, C.D. 2007. The bees of the world [2nd ed.]. Baltimore: Johns Hopkins University Press, xvi + [i] + 953 pp., +20 pls.

Michener, C.D., and S. Boongird. 2004. A new species of Trigona from peninsular Thailand (Hymenoptera: Apidae: Meliponini). Journal of the Kansas Entomological Society 77 (2): 143–146.

Michener, C.D., and A. Fraser. 1978. A comparative anatomical study of mandibular structure in bees (Hymenoptera: Apoidea). University of Kansas Science Bulletin 51 (14): 463–482.

Michener, C.D., and D.W. Roubik. 1993. Observations on the labium of meliponine bees (Hymenoptera: Apidae). In T. Inoue and S. Yamane (editors), Evolution of insect societies: comparative sociology of bees, wasps and ants: 251–266. Tokyo: Hakuhin-sha Publishing, vii + 532 pp.

Michener, C.[D.], and S.F. Sakagami. 1990. Appendix: Trigona genalis Friese, a hitherto unplaced New Guinea species. University of Kansas Science Bulletin 54 (4): 153–157.

Moure, J.S. 1961. A preliminary supra-specific classification of the Old World meliponine bees (Hymenoptera, Apoidea). Studia Entomologica 4 (1–4): 181–242.

Moure, J.S., and J.M.F. Camargo. 1978. A fossil stingless bee from copal (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 51 (4): 560–566.

Nogueiro-Neto, P. 1953. A criação de abelhas indígenas sem ferrão (Meliponinae). São Paulo: Chácaras e Quintais, 280 pp.

Nurse, C.G. 1907. A new species of Indian wax-producing bee. Journal of the Bombay Natural History Society 17 (3): 619.

Pugh, B.M. 1947. Varieties of bees found in Assam (extract from the report of the Assistant Agriculture Officer, North East Frontier Agency, Assam, on “Agriculture in the Mynner (Jirang) State, Khasi Hills, Assam”). Indian Bee Journal 9 (5–6): 62.

Rasmussen, C. 2008. Catalog of the Indo-Malayan/Australasian stingless bees (Hymenoptera: Apidae: Meliponini). Zootaxa 1935: 1–80.

Rasmussen, C., and S.A. Cameron. 2007. A molecular phylogeny of the Old World stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Systematic Entomology 32 (1): 26–39.

Rasmussen, C., and S.A. Cameron. 2010. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biological Journal of the Linnean Society 99 (1): 206–232.

Rayment, T. 1930. New and remarkable bees. Proceedings of the Royal Society of Victoria 43 (1): 42–61.

Rayment, T. 1932. The stingless bees of Australia. 6. The finding of a new species. Victorian Naturalist 49 (584): 104–107.

Sakagami, S.F. 1959. Stingless bees collected by Prof. S. Matsumura from Singapore (Hymenoptera, Apidae). Insecta Matsumurana 22 (3–4): 119–121.

Sakagami, S.F. 1975. Stingless bees (excl. Tetragonula) from the Continental Southeast Asia in the collection of Berince [sic] P. Bishop Museum, Honolulu (Hymenoptera, Apidae). Journal of the Faculty of Science, Hokkaido University (Series 6) Zoology 20 (1): 49–76.

Sakagami, S.F. 1978. Tetragonula stingless bees of the continental Asia and Sri Lanka (Hymenoptera, Apidae). Journal of the Faculty of Science, Hokkaido University (Series 6) Zoology 21 (2): 165–247.

Sakagami, S.F., and T. Inoue. 1985. Taxonomic notes on three bicolorous Tetragonula stingless bees in Southeast Asia. Kontyû 53 (1): 174–189.

Sakagami, S.F., and T. Inoue. 1987. Stingless bees of the genus Trigona (subgenus Trigonella) with notes on the reduction of spatha in male genitalia of the subgenus Tetragonula (Hymenoptera, Apidae). Kontyû 55 (4): 610–627.

Sakagami, S.F., and T. Inoue. 1989. Stingless bees of the genus Trigona (subgen. Geniotrigona) (Hymenoptera, Apidae), with description of T. (G.) incisa sp. nov. from Sulawesi. Japanese Journal of Entomology 57 (3): 605–620.

Sakagami, S.F., and S. Yamane. 1987. Oviposition behavior and related notes of the Taiwanese stingless bee Trigona (Lepidotrigona) ventralis hoozana. Journal of Ethology 5 (1): 17–27.

Schwarz, H.F. 1937. Results of the Oxford University Sarawak (Borneo) expedition: Bornean stingless bees of the genus Trigona. Bulletin of the American Museum of Natural History 73 (3): 281–328, + pls. ii–vii.

Schwarz, H.F. 1939. The Indo-Malayan species of Trigona. Bulletin of the American Museum of Natural History 76 (3): 83–141.

Sharkey, M.J. and R.A. Wharton. 1997. Morphology and terminology. In R.A. Wharton, P.M. Marsh, and M.J. Sharkey (editors), Manual of the New World genera of the family Braconidae (Hymenoptera): 19–37. Washington, D.C.: International Society of Hymenopterists, [ii] + 439 pp.

Smith, F. 1854. Catalogue of Hymenopterous Insects in the Collection of the British Museum. Part II. Apidae. London: British Museum, 199–465 pp., + pls. vii–xii.

Smith, F. 1857. Catalogue of the hymenopterous insects collected at Sarawak, Borneo; Mount Ophir, Malacca; and at Singapore, by A.R. Wallace. Journal of the Proceedings of the Linnean Society, Zoology 2 (6): 42–88, +2 pls.

Smith, F. 1865. Descriptions of new species of hymenopterous insects from the islands of Sumatra, Sula, Gilolo, Salwatty, and New Guinea, collected by Mr. A.R. Wallace. Journal of the Proceedings of the Linnean Society, Zoology 8 (30): 61–94, + pl. iv.

Smith, F. 1878. List of Hymenoptera obtained by Mr. Ossian Limborg east of Maulmain, Tenasserim Provinces, during the months December 1876, January, March and April 1877, with descriptions of new species. Journal of the Asiatic Society of Bengal, Part 2 (Physical Science) 47 (3): 167–169.

Strand, E. 1913. [H. Sauter’s Formosa-Ausbeute] Apidae I (Hym.). Supplementa Entomologica 2: 23–67.

Tadauchi, O., M. Ito, J.-I. Kojima, and M.J. Toda. 1998. Species and subspecies described by the late professor Dr. Sh.F. Sakagami (Insecta: Hymenoptera). Natural History Bulletin of Ibaraki University 2: 229–246.

Tosi, A. 1896. Di un nuovo genere di Apiaria fossile nell’ambra di Sicilia (Meliponorytes succini – M. sicula). Rivista Italiana di Paleontologia 2 (6): 352–356, +1 pl.

Vane-Wright, D. 1991. Transcending the Wallace line: do the western edges of the Australina region and the Australian plate coincide? Australian Systematic Botany 4 (1): 183–197.

Viraktamath, S., and K. Sajan Jose. 2017. Two new species of Lisotrigona Moure (Hymenoptera: Apidae: Meliponini) from India with notes on nest structure. Bioscan 12 (1): 21–28.

Walker, F. 1860. Characters of some apparently undescribed Ceylon insects. Annals and Magazine of Natural History (3) 5 (28): 304–311.

APPENDIX

Synonymic Checklist of Indomalayan-Australasian Meliponini

The following list summarizes the currently recognized species within the genera and subgenera of stingless bees occurring in the Indomalayan and Australasian regions. The species are arranged according to the organization of the genera given in the present work (table 1). Currently valid names are indicated in boldface, with known synonyms listed, and asterisks identify the type species for the genus-group taxa.

Genus Austroplebeia Moure, 1961

Austroplebeia australis (Friese, 1898)

= Trigona cincta percincta Cockerell, 1929a

= Trigona cockerelli Rayment, 1930

= Trigona cockerelli ornata Rayment, 1932

= Trigona websteri Rayment, 1932

Austroplebeia cassiae (Cockerell, 1910)*

= Trigona symei Rayment, 1932

Austroplebeia cincta (Mocsáry in Friese, 1898)

Austroplebeia essingtoni (Cockerell, 1905)

Austroplebeia magna Dollin, Dollin, and Rasmussen, 2015

Genus Geniotrigona Moure, 1961

Geniotrigona lacteifasciata (Cameron, 1902)

= Trigona borneënsis Friese, 1933a

Geniotrigona thoracica (Smith, 1857)*

= Trigona ambusta Cockerell, 1918

Genus Heterotrigona Schwarz, 1939

Subgenus Heterotrigona Schwarz, 1939

Heterotrigona (Heterotrigona) bakeri (Cockerell, 1919b)

Heterotrigona (Heterotrigona) erythrogastra (Cameron, 1902)

= Trigona luteiventris Friese, 1908 [1909]

= Trigona sandacana Cockerell, 1919a

Heterotrigona (Heterotrigona) itama (Cockerell, 1918)*

= Trigona breviceps Cockerell, 1919a

Subgenus Platytrigona Moure, 1961

Heterotrigona (Platytrigona) flaviventris (Friese, 1908 [1909])

Heterotrigona (Platytrigona) hobbyi (Schwarz, 1937)

Heterotrigona (Platytrigona) keyensis (Friese, 1901)

Heterotrigona (Platytrigona) lamingtonia (Cockerell, 1929a)

Heterotrigona (Platytrigona) planifrons (Smith, 1865)*

Subgenus Sahulotrigona Engel and Rasmussen, 2017

Heterotrigona (Sahulotrigona) atricornis (Smith, 1865)

Heterotrigona (Sahulotrigona) paradisaea Engel and Rasmussen, 2017*

= Trigona (Pacificotrigona) okazawai Tadauchi et al., 1998, nomen nudum

= Trigona (Pacificotrigona) okazawai irianensis Tadauchi et al., 1998, nomen nudum

Subgenus Sundatrigona Inoue and Sakagami, 1993

Heterotrigona (Sundatrigona) lieftincki (Sakagami and Inoue, 1987)

Heterotrigona (Sundatrigona) moorei (Schwarz, 1937)*

= Trigona (Tetragona) matsumurai Sakagami, 1959

Genus Homotrigona Moure, 1961

Subgenus Homotrigona Moure, 1961

Homotrigona (Homotrigona) aliceae (Cockerell, 1929b)

= Trigona kusutkana Dover, 1929

Homotrigona (Homotrigona) anamitica (Friese, 1909)

= Trigona melanotricha Cockerell, 1918

Homotrigona (Homotrigona) fimbriata (Smith, 1857)*

= Melipona castanea Bingham, 1903

= Trigona flavistigma Cameron, 1902

= Trigona versicolor Friese, 1908 [1909]

Homotrigona (Homotrigona) lutea (Bingham, 1897)

= Trigona ferrea Cockerell, 1929b

Subgenus Lophotrigona Moure, 1961

Homotrigona (Lophotrigona) canifrons (Smith, 1857)*, new combination

= Trigona busara Cockerell, 1918

Subgenus Odontotrigona Moure, 1961

Homotrigona (Odontotrigona) haematoptera (Cockerell, 1919a)*, new combination

= Trigona haematoptera variety dulitae Schwarz, 1937

Subgenus Tetrigona Moure, 1961

Homotrigona (Tetrigona) apicalis (Smith, 1857)*, new combination

= Trigona hemileuca Cockerell, 1929b

= Trigona sericea Friese, 1933b

Homotrigona (Tetrigona) binghami (Schwarz, 1937), new combination

Homotrigona (Tetrigona) melanoleuca (Cockerell, 1929b), new combination

Homotrigona (Tetrigona) peninsularis (Cockerell, 1927), new combination

Homotrigona (Tetrigona) vidua (Lepeletier de Saint Fargeau, 1836), new combination

Genus Lepidotrigona Schwarz, 1939

Lepidotrigona arcifera (Cockerell, 1929c)

= Melipona tunneli Pugh, 1947, nomen dubium et inquirendum

Lepidotrigona doipaensis (Schwarz, 1939)

Lepidotrigona flavibasis (Cockerell, 1929c)

Lepidotrigona hoozana (Strand, 1913)

Lepidotrigona javanica (Gribodo, 1891)

Lepidotrigona latebalteata (Cameron, 1902)

Lepidotrigona latipes (Friese, 1900)

Lepidotrigona nitidiventris (Smith, 1857)*

= Trigona fulvopilosella Cameron, 1908

Lepidotrigona palavanica (Cockerell, 1915)

Lepidotrigona terminata (Smith, 1878)

= Trigona fulvomarginata Cockerell, 1919b

Lepidotrigona trochanterica (Cockerell, 1920)

Lepidotrigona ventralis (Smith, 1857)

= Trigona (Lepidotrigona) ventralis form nigribasis Sakagami, 1975, nomen invalidum

Genus Lisotrigona Moure, 1961

Lisotrigona cacciae (Nurse, 1907)*

= Trigona scintillans Cockerell, 1920

= Lisotrigona mohandasi Jobiraj and Narendran, 2004, new synonym

= Lisotrigona chandrai Viraktamath and Sajan Jose, 2017, new synonym

= Lisotrigona revanai Viraktamath and Sajan Jose, 2017, new synonym

Lisotrigona carpenteri Engel, 2000

Lisotrigona furva Engel, 2000

Genus Papuatrigona Michener and Sakagami, 1990

Papuatrigona genalis (Friese, 1908 [1909])*

Genus Pariotrigona Moure, 1961

Pariotrigona pendleburyi (Schwarz, 1939)*

= Trigona (Hypotrigona) pendleburyi variety klossi Schwarz, 1939

Genus Tetragonula Moure, 1961

Subgenus Tetragonilla Moure, 1961

Tetragonula (Tetragonilla) atripes (Smith, 1857)*

Tetragonula (Tetragonilla) collina (Smith, 1857)

= Trigona cambodiensis Cockerell, 1926

Tetragonula (Tetragonilla) fuscibasis (Cockerell, 1920)

Tetragonula (Tetragonilla) rufibasalis (Cockerell, 1918)

Subgenus Tetragonula Moure, 1961

Tetragonula (Tetragonula) bengalensis (Cameron, 1897)

Tetragonula (Tetragonula) biroi (Friese, 1898)

Tetragonula (Tetragonula) carbonaria (Smith, 1854)

= Trigona angophorae Cockerell, 1912

Tetragonula (Tetragonula) clypearis (Friese, 1909)

= Trigona wybenica Cockerell, 1929d

Tetragonula (Tetragonula) dapitanensis (Cockerell, 1925)

Tetragonula (Tetragonula) davenporti (Franck in Franck et al., 2004)

Tetragonula (Tetragonula) drescheri (Schwarz, 1939)

Tetragonula (Tetragonula) fuscobalteata (Cameron, 1908)

= Trigona erythrostoma Cameron, 1908

= Trigona pallidistigma Cameron, 1908

= Trigona atomella Cockerell, 1919a

= Trigona brevis Friese, 1925, nomen nudum

= Trigona pfeifferi Friese, 1925

= Trigona pygmaea Friese, 1933b

Tetragonula (Tetragonula) geissleri (Cockerell, 1918)

= Trigona confusella Cockerell, 1919a

Tetragonula (Tetragonula) gressitti (Sakagami, 1978)

Tetragonula (Tetragonula) hirashimai (Sakagami, 1978)

Tetragonula (Tetragonula) hockingsi (Cockerell, 1929e)

Tetragonula (Tetragonula) iridipennis (Smith, 1854)*

Tetragonula (Tetragonula) laeviceps (Smith, 1857)

Tetragonula (Tetragonula) malaipanae Engel, Michener, and Boontop, 2017

Tetragonula (Tetragonula) melanocephala (Gribodo, 1893)

= Trigona testaceinerva Cameron, 1908

Tetragonula (Tetragonula) melina (Gribodo, 1893)

Tetragonula (Tetragonula) mellipes (Friese, 1898)

Tetragonula (Tetragonula) minangkabau (Sakagami and Inoue, 1985)

= Trigona minangkabu form darek Sakagami and Inoue, 1985, nomen invalidum et nudum

Tetragonula (Tetragonula) minor (Sakagami, 1978)

Tetragonula (Tetragonula) pagdeni (Schwarz, 1939)

Tetragonula (Tetragonula) pagdeniformis (Sakagami, 1978)

Tetragonula (Tetragonula) penangensis (Cockerell, 1919b)

Tetragonula (Tetragonula) praeterita (Walker, 1860)

Tetragonula (Tetragonula) reepeni (Friese, 1918)

= Trigona latigenalis Sakagami, 1978

Tetragonula (Tetragonula) ruficornis (Smith in Horne and Smith, 1870)

= Melipona smithii Bingham, 1897, nomen vanum

Tetragonula (Tetragonula) sapiens (Cockerell, 1911)

Tetragonula (Tetragonula) sarawakensis (Schwarz, 1937)

Tetragonula (Tetragonula) sirindhornae (Michener and Boongird, 2004)

Tetragonula (Tetragonula) testaceitarsis (Cameron, 1901)

= Trigona testaceicornis Cameron, 1901, lapsis calami

= Trigona valdezi Cockerell, 1918

Tetragonula (Tetragonula) zucchii (Sakagami, 1978)

Genus Wallacetrigona Engel and Rasmussen, herein

Wallacetrigona incisa (Sakagami and Inoue, 1989)*, new combination

Nomina dubia and unassociated nomina nuda

Melipona basimaculata Bingham, 1903, nomen dubium et inquirendum

Melipona khasiana Pugh, 1947, nomen nudum

Melipona pulla Illiger, 1806, nomen nudum

Melipona terrestris Pugh, 1947, nomen nudum

Trigona bismarkiana Tadauchi et al., 1998, nomen nudum

Trigona pallidicincta Cockerell, 1918, nomen dubium et inquirendum

Trigona wallacei Tadauchi et al., 1998, nomen nudum (a species of Tetragonula s.str.)

1 Department of Bioscience, Aarhus University, Aarhus, Denmark.

2 Division of Entomology, Natural History Museum, University of Kansas, Lawrence.

3 Division of Invertebrate Zoology, American Museum of Natural History; Division of Entomology, Natural History Museum, and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence.

4 The term clivulus is introduced here (from Latin, diminutive form of clivus, meaning “sloping incline”) to refer to the slope between the elevated keirotrichiate plateau and the posterior glabrate zone. The condition of the clivulus varies between a gentle slope between these two surfaces in Lepidotrigona and Papuatrigona to an abrupt precipice in most Eastern Hemisphere genera.