Engel, Engel & Herhold & Davis & Wang & Thomas, 2021

Engel, Michael S., Herhold, Hollister W., Davis, Steven R., Wang, Bo & Thomas, Jennifer C., 2021, Stingless bees in Miocene amber of southeastern China (Hymenoptera: Apidae), Journal of Melittology 2021 (105), pp. 1-83 : 14-20

Tribe Meliponini Lepeletier de Saint Fargeau

The stingless bees, tribe Meliponini , are one of two lineages of exclusively highly eusocial bees in the apine clade Corbiculata ( Michener, 2007; Engel & Rasmussen, 2021; Engel et al., 2021; Melo, 2021). Like honey bees ( Apini ), meliponines live in typically large, perennial colonies, and are actively managed (meliponiculture) in certain regions of the tropics for the production of honey, pollination services, as well as other materials (e.g., propolis, resin). The 520 modern species are distributed pantropically and are most diverse in those regions where honey bees are not native (i.e., South and Central America), perhaps reflecting a historical competitive pressure between these two eusocial rivals ( Engel , 2001a). Unlike honey bees, not all stingless bees collect pollen. Species of the Asian genera Lisotrigona Moure and Pariotrigona Moure are lachryphages (tear-drinking bees), collecting tears from a variety of vertebrates and using this as a source of nutrients ( Bänziger et al., 2009, 2011; Bänziger & Bänziger, 2010; Bänziger, 2018). Although the minute species of Trigonisca (Leurotrigona) Moure are known as “lambe olhos” (eye lickers), they are apparently not lachryphagous as in the aforementioned genera. Species of Lestrimelita Friese (Neotropical) and Liotrigona (Cleptotrigona) Moure (Afrotropical) are robber bees (cleptobiotic) and make mass raids on other meliponine colonies, during which they steal resources to bring back to their home nest ( Portugal-Araújo, 1958; Wille, 1983; Sakagami et al., 1993; Grüter et al., 2016). Species of Trichotrigona Camargo & Moure are also robber bees, but these make solitary raids on their hosts ( Engel & Rasmussen, 2021). Lastly, there is a small clade of vulture bees (necrophages) in the genus Trigona Jurine (Necrotrigona Engel , n. subgen.: Appendix), species of which harvest tissues from vertebrate carcasses and store these in pots within the nest ( Camargo & Roubik, 1991; Noll et al., 1996; Noll, 1997; Mateus & Noll, 2004).

The tribe is most closely related to the extinct tribe Melikertini ( Engel , 2001a, 2001b; Schult et al., 2001; Cardinal & Packer, 2007), known only from Eocene amber deposits of Europe and Asia. Characteristics of melikertines have recently been summarized in detail ( Engel & Davis, 2021), and that material is not repeated here. The closest relative of the Melikertini + Meliponini clade remains somewhat controversial. Many analyses based on diverse data support the highly eusocial Apini as sister, along with the concomitant reconstruction of a single origin of highly eusocial behavior among corbiculate bees (e.g., Roig-Alsina & Michener, 1993; Schult et al., 1999, 2001; Engel , 2001b; Noll, 2002; Cardinal & Packer, 2007; Canevazzi & Noll, 2015; Porto et al., 2016, 2017, 2021; Porto & Almeida, 2021; Noll et al., in press). Nonetheless, some analyses suggest that meliponines are more closely related to the primitively eusocial bumble bees, with Apis Linnaeus clustering with the orchid bees or as sister to Meliponini + Bombini (e.g., Kawakita et al., 2008; Ramírez et al., 2010; Martins et al., 2014; Romiguier et al., 2016; Kwong et al., 2017; Bossert et al., 2019).

Meliponines are distinguished by a large number of traits relative to other corbiculate bees, and particularly from their relatives in the Melikertini and Apini . As their cognomen implies, the sting apparatus of stingless bees is vestigial, although the sting stylet itself is still distinct with an acutely sharp apex and therefore sting-like in Melipona Illiger , Liotrigona (Cleptotrigona) , Meliplebeia Moure , Axestotrigona Moure , Meliponula Cockerell , and somewhat in Plebeiella Moure. Beyond the structure of the sting, stingless bees lack extensive outer mandibular grooves (as in Melikertini , Apini , and those weakened grooves in Electrapini ), have the anterior mandibular condyle contiguous with the clypeal border (as in Apini and Melikertini , covered by the clypeal border in Euglossini and Bombini ), have the mentum and submentum separated (as in Apini and Bombini , rather than fused in Euglossini ), and the compound eyes usually bare (hirsute in Apini ). The mesoscutum lacks the supraälar carina that is otherwise present in all other living and fossil corbiculate bees. The wings of stingless bees are noteworthy for the reduction of the distal wing venation, rather than the complete venation of all other corbiculate bees. The distal portion of the wing lacks alar papillae (as is the case in Apini and Melikertini , while papillae are generally present in Euglossini , Bombini , Electrobombini , and Electrapini ), and the jugal lobe of the hind is present proximally (as is the case in all corbiculate bees with the exception of Euglossini and Bombini ). The protibial strigilis lacks an anterior velum, as in Melikertini , that is otherwise present in all other living and fossil corbiculate bees. The meliponine metatibia has a distinct penicillum at the distal inferior angle [except absent in the cleptobiotic Lestrimelita and Liotrigona (Cleptotrigona) , and rudimentary in Trichotrigona ], a unique trait not otherwise known in any other living and fossil corbiculate bees, although there is a patch of setae in Melikertini that is situated in the position of the penicillum and that could be a homologous precursor ( Engel & Davis, 2021). Metatibial spurs are completely absent in Meliponini , as well as in Apini , while a single spur, sometimes reduced, is present in Melikertini and Electrapini , and the normal complement and development of spurs are present in Euglossini , Bombini , and Electrobombini . The auricle that is present in all corbiculate bees (except parasitic forms), is characteristically absent in stingless bees. The pretarsal claws are simple (toothed to some degree in all other corbiculate bees), and the arolium is present (as in all living and fossil corbiculate bees with the exception of Euglossini and Bombini ). In males, the hidden metasomal sterna VII and VIII are reduced (as in Apini , well-developed in Euglossini and Bombini ), and the gonobase is absent or vestigial (as in Apini , present in Euglossini and Bombini ). Although a single melikertine male is known ( Engel et al., 2014), it has yet to be scanned to see if the terminalia could be visualized and compared with that of Meliponini and other corbiculate bees.

The Old World fauna of stingless bees, while diverse, is minor by comparison to the plethora of species found in the New World tropics ( Michener, 2007; Rasmussen, 2008; Rasmussen et al., 2017). Nonetheless, there is considerable variety in the lineages and biology of the Eastern Hemisphere Meliponini . This fauna was largely assigned to the otherwise New World genus Trigona until Moure (1961) provided a far-reaching, and in some ways prescient, rearrangement of the fauna (in the same fashion as he had for the New World fauna earlier: Moure, 1951), ascribing the numerous species to a series of unique genera and subgenera. While some chose to retain most of Moure’s groups within Trigona (e.g., Michener, 1990, 2007), gradually an augmented version of his system has become adopted (e.g., Michener, 2013; Rasmussen et al., 2017; Engel et al., 2018; Engel , 2019; Grüter, 2020; Melo, 2021; herein) and is followed herein. The classification of the tribe can be outlined as follows ( Table 2) (Appendix):

Subtribe Hypotrigonina Engel, new subtribe (type genus: Hypotrigona Cockerell ): This clade comprises all extant Eastern Hemisphere stingless bees. The group is quite heterogenous and there are repeated convergences with genera of the Meliponina , such as the presence of the basal sericeous area on the proximal retrolateral surface of the metabastarsus. Nonetheless, the group includes those species with flatened worker gonostyli bearing gonotrichia (except also present in Trigoniscitae , but in those bees the marginal cell base is greatly broadened such that the basal angle is slightly acute to orthogonal), or species with a distinctive pollen pocket proximally on the prolateral surface of the metabasitarsus (those species with the pollen pocket have the worker gonostyli cylindrical and lack gonotrichia). Wille (1979) and Michener (2007) discussed some of these convergences in greater detail. The occurrence of gonotrichia on the worker gonostyli is largely split between the two internal clades of this subtribe, with none present among Heterotrigonitae and gonotrichia largely present in Hypotrigonitae aside from two exceptions (vide infra). The two major clades of the subtribe are:

Infratribe Heterotrigonitae Engel, new infratribe (type genus: Heterotrigona Schwarz ): The genera of this clade all possess a distinctive apical glabrate (apicoglabrate) zone on the retrolateral surface of the metatibia and have a robust, broad, ovoid metasoma that tapers in width apically from the third segment. The worker gonostyli, where known, are cylindrical and lack gonotrichia. On the prolateral surface of the metabasitarsus there is a proximal superior concavity, inferiorly bordered by a ridge (sometimes the ridge is strong but can vary to exceptionally weak and largely grading onto the otherwise normal planar prolateral surface) that bears a distinctive fimbria of fine, simple, superiorly directed setae (the fimbriate line) that border the otherwise largely glabrous concave surface. Wille (1979) considered this to be a “pollen press” of sorts, but not to be confused with the more typical pollen press formed by the auricle which is present in other corbiculate bee lineages. The function of this structure is unknown but to avoid confusion with the actual pollen press of other bees, we here refer to it as a pollen pocket. A pollen pocket is found in all Heterotrigonitae , albeit more weakly so in some of the minute species of Tetragonula s.str. In fact, the pollen pocket is generally weaker in Tetragonula s.l. than in other Heterotrigonitae . A pollen pocket is also present in Oxytrigona Cockerell ( Meliponina : Meliponitae ). The clade includes seven genera: Tetragonula Moure ( Tetragonula s.str. and Tetragonilla Moure ), Homotrigona Moure ( Homotrigona s.str., Lophotrigona Moure , Odontotrigona Moure , and Tetrigona Moure ), Geniotrigona Moure , Heterotrigona Schwarz ( Heterotrigona s.str., Sundatrigona Inoue & Sakagami , Borneotrigona Engel, Platytrigona Moure , Sahulotrigona Engel & Rasmussen), Papuatrigona Michener & Sakagami , Lepidotrigona Schwarz , and Wallacetrigona Engel & Rasmussen.

Tribe MELIPONINI Lepeletier de Saint Fargeau

Subtribe Meliponina Lepeletier [New World] Subtribe Hypotrigonina Engel, n. subtrib. [Old World]

Infratribe Trigoniscitae Engel, n. infratrib. Infratribe Heterotrigonitae Engel, n. infratrib.

Trigonisca Genus Group Clan Heterotrigona Genus Trigonisca Moure Heterotrigona Genus Group Subgenus Leurotrigona Moure Genus Geniotrigona Moure Subgenus Exochotrigona Engel Genus Heterotrigona Schwarz Subgenus Celetrigona Moure Subgenus Borneotrigona Engel Subgenus Trigonisca Moure , s.str. Subgenus Sundatrigona Inoue & Sakagami Genus † Exebotrigona Engel & Michener Subgenus Heterotrigona Schwarz , s.str.

Infratribe Meliponitae Lepeletier Subgenus Platytrigona Moure

Clan Trigona Subgenus Sahulotrigona Engel & Rasmussen

Paratrigona Genus Group Genus Papuatrigona Michener & Sakagami Genus Paratrigona Schwarz Genus Lepidotrigona Schwarz Subgenus Aparatrigona Moure Genus Wallacetrigona Engel & Rasmussen Subgenus Paratrigona Schwarz , s.str. Homotrigona Genus Group Genus Paratrigonoides Camargo & Roubik Genus Homotrigona Moure Genus Nogueirapis Moure Subgenus Lophotrigona Moure Genus Partamona Schwarz Subgenus Homotrigona Moure , s.str. Subgenus Partamona Schwarz , s.str. Subgenus Odontotrigona Moure Subgenus Parapartamona Schwarz Subgenus Tetrigona Moure

Trigona Genus Group Clan Tetragonula Genus Oxytrigona Cockerell Genus Tetragonula Moure Genus Scaptotrigona Moure Subgenus Tetragonilla Moure Genus Geotrigona Moure Subgenus Tetragonula Moure , s.str. Genus Ptilotrigona Moure Infratribe Hypotrigonitae Engel, n. infratrib. Genus Tetragona Lepeletier & Audinet-Serville Hypotrigona Genus Group Subgenus Camargoia Moure Genus Hypotrigona Cockerell Subgenus Tetragona s.str. Genus Liotrigona Moure Genus Trigona Jurine Subgenus Cleptotrigona Moure Subgenus Aphaneuropsis Engel , n. subgen. Subgenus Liotrigona Moure , s.str. Subgenus Koilotrigona Engel , n. subgen. Genus Pariotrigona Moure Subgenus Necrotrigona Engel , n. subgen. Genus Lisotrigona Moure Subgenus Nostotrigona Engel , n. subgen. Genus Austroplebeia Moure Subgenus Ktinotrofia Engel , n. subgen. Subgenus † Anteplebeina Engel , n. subgen. Subgenus Aphaneura Gray Subgenus Austroplebeia Moure , s.str. Subgenus Trigona Jurine , s.str. Genus † Kelneriapis Sakagami Subgenus Dichrotrigona Engel , n. subgen. Genus † Liotrigonopsis Engel Genus Cephalotrigona Schwarz Meliponula Genus Group Genus Meliwillea Roubik, Segura, & Camargo Genus Meliplebeia Moure

Plebeia Genus Group Subgenus Apotrigona Moure Genus Tetragonisca Moure Subgenus Meliplebeia Moure , s.str. Genus Frieseomelita Ihering Genus Axestotrigona Moure Genus Trichotrigona Camargo & Moure Subgenus Atrichotrigona Engel , n. subgen. Genus Duckeola Moure Subgenus Axestotrigona Moure , s.str. Genus Plectoplebeia Melo Genus Plebeiella Moure Genus Plebeia Schwarz Genus Dactylurina Cockerell Subgenus Nanoplebeia Engel , n. subgen. Genus Meliponula Cockerell Subgenus Plebeia Schwarz , s.str. Genus Plebeina Moure Genus Lestrimelita Friese Genus Friesella Moure Genus Asperplebeia Engel, n. gen. Subtribe Incertae sedis Genus Nannotrigona Cockerell Genus † Cretotrigona Engel [ Meliponina ?] Subgenus Lispotrigona Gonzalez & Engel , n. subgen. Genus † Meliponorytes Tosi [Heterotrigonina?] Subgenus Nannotrigona Cockerell , s.str. Genus Schwarziana Moure Subgenus Mourella Schwarz Subgenus Chapadapis Engel , n. subgen. Subgenus Schwarziana Moure , s.str. Genus Scaura Schwarz Subgenus Scaura Schwarz , s.str. Subgenus Schwarzula Moure Genus † Proplebeia Michener

Clan Melipona Genus Melipona Illiger Subgenus Melipona Illiger , s.str. Subgenus Meliponotes Engel Subgenus Melikerria Moure Subgenus Eomelipona Moure Subgenus Mouremelia Engel Subgenus Michmelia Moure

Infratribe Hypotrigonitae Engel, new infratribe (type genus: autobasic with Hypotrigonina Engel, vide supra): The genera of this clade all lack a broad apical glabrate zone on the retrolateral surface of the metatibia, with the exception of Dactylurina Cockerell , which, while having such a glabrate zone, combines it with an elongate, subclavate, finger-like metasoma, not found in the Heterotrigonitae . The worker gonostyli, where known, are flatened and have gonotrichia, with the exception of the minute species of Hypotrigona Cockerell and Pariotrigona , which have the gonostyli greatly reduced and almost tuberculiform. The pollen pocket of the Heterotrigonitae is lacking, with the proximal superior surface where it would otherwise be found largely coplanar with the remainder of the metabasitarsal prolateral surface (sometimes there is a faint slope leading to the retrodorsal margin) and the setae are largely uniform across the surface (i.e., not defining a line bordering a polished superior surface), although often subappressed and superiorly directed. This clade includes 11 extant genera: Lisotrigona , Pariotrigona , and Austroplebeia Moure in the Indomalayan and Papuan and Australian regions, respectively; and the African Hypotrigona , Liotrigona Moure ( Liotrigona s.str. and Cleptotrigona ), Plebeina Moure , Meliponula , Dactylurina , Plebeiella , Axestotrigona [Atrichotrigona Engel , new subgenus (Appendix), and Axestotrigona s.str.], and Meliplebeia ( Meliplebeia s.str. and Apotrigona Moure ) [Note: contra Michener (2007), one of us (M.S.E.) considers Meliponula , Axestotrigona , and Plebeiella to be distinct genera (Appendix), and that Meliplebeia here constitutes those species with yellow markings, a sloping basal area distinct from the vertical posterior surface, and the propodeal basal area covered with fine erect setae. The subgenera are then distinguished by the mesoscutum tessellate in Meliplebeia s.str. versus punctate in Apotrigona , the mandible with small teeth in Meliplebeia s.str. versus pronounced and strong in Apotrigona , the scape as long as the torulocellar distance in Meliplebeia s.str. versus shorter in Apotrigona , the basal vein (1M) slightly distad 1cu-a in Meliplebeia s.str. versus slightly basad in Apotrigona ; the superior parapenicillum is well developed in Meliplebeia s.str. and poorly developed, scarcely definable as a parapenicillum, in Apotrigona ; Apotrigona also has a faint opalescence observable under certain lightings that is seemingly not present in Meliplebeia s.str. The superior parapenicillum is only present in Meliplebeia , Axestotrigona , Plebeiella , and Meliponula .]. Although Dactylurina has been placed as sister to Meliponula ( Rasmussen & Cameron, 2010) , most morphological characters suggest it should be in a more basal position along with or just basal to Plebeina (e.g., absence of superior parapenicillum), with Meliponula more closely related to Plebeiella , Axestotrigona , and Meliplebeia . A possible set of relationships that should be more fully explored would be: Dactylurina ( Plebeina ( Meliponula ( Plebeiella ( Axestotrigona + Meliplebeia )))). Under such an arrangement, the superior parapenicillum and the more developed sting would unite everything from Meliponula onward (and those groups could potentially all be classified as subgenera of Meliponula once again, analogous to but not equivalent to the system of Wille, 1979, and Michener, 2007). The fossil genera Kelneriapis Sakagami and Liotrigonopsis Engel, both in Eocene Baltic amber, belong to this clade.

Subtribe Meliponina Lepeletier de Saint Fargeau (type genus: Melipona Illiger ): The subtribe is characterized by the absence of features otherwise distinctive for the Hypotrigonina . The worker gonostyli of the subtribe lack gonotrichia in all genera except those of the basal Trigoniscitae (likely a plesiomorphic feature for that subtribe, shared symplesiomorphically with the Hypotrigonitae , and then independently lost in Meliponitae , Heterotrigonitae , Hypotrigona , and Pariotrigona ; such loss is clearly not linked to minute body sizes as the minute species of Trigoniscitae , Liotrigona s.l., Lisotrigona , and Austroplebeia all retain such gonotrichia). The subtribe is exclusively distributed in the Western Hemisphere, from Mexico to northern Argentina, although Plebeia (Plebeia) frontalis (Friese) has been introduced into coastal central California (M. Hauser, pers. comm.; M.S.E., per. obs.).

Infratribe Trigoniscitae Engel, new infratribe (type genus: Trigonisca Moure ): This group was characterized recently (as the “ Trigonisca Genus Group”) by Engel et al. (2019). The included species are united by the distinctively broadened base to the marginal cell in which the basal angle is slightly acute to orthogonal (68°–90°), and with the marginal cell, at the apex of the pterostigma, broader than the area encompassed by the submarginal cells. The forewing is less, usually much less, than 4 mm in length. The work- er gonostyli have a field of gonotrichia (otherwise known only in most African and two Indomalayan-Australasian genera). Additionally, the retromarginal edge of the metatibia is typically nodulose to tuberculate, sometimes weakly so, with the exception of the fossil genus Exebotrigona Engel & Michener. The clade includes the extant genus Trigonisca Moure ( Trigonisca s.str., Leurotrigona Moure , Exochotrigona Engel, and Celetrigona Moure ). The fossil genus Exebotrigona , in Baltic amber, belongs to this clade as evidenced by the form of the marginal cell and small body size. Modern species of the infratribe occur from southern Mexico to southern Peru, Bolivia, and the southern reaches of the Central-West and Southeast Regions of Brazil.

Infratribe Meliponitae Lepeletier de Saint Fargeau (= Trigonini Moure, Lestrimelitini Moure): This group differs from Trigoniscitae by the distinctly acute base to the marginal cell, with it’s breadth at the apex of the pterostigma litle if any broader than the area encompassed by the submarginal cells. The forewing is usually over 4 mm in length. The worker gonostyli lack gonotrichia. The retromarginal edge of the metatibia is not nodulose or tuberculate. The clade includes all remaining extant genera of Meliponini [ Table 2: subgeneric system of Melipona from Engel (in pressb)]. The Miocene genus Proplebeia Michener , in Dominican and Mexican amber, belongs to the Plebeia -group of this infratribe.

The fossil genera Meliponorytes Tosi and Cretotrigona Engel are currently considered incertae sedis, pending further study. Meliponorytes is a poorly understood genus of putatively two species in Sicilian amber, but has not been studied since the Bolognese archeologist Alessandro Tosi (1865–1949) described and figured the group in 1896. The material was in the Collezione di Mineralogia (Museo di Mineralogia), Universitá di Bologna but the current state of preservation relative to oxidation (Sicilian amber can turn quite black), crazing, and deterioration is unknown. The species are minute and have various features typical of minute Meliponini (e.g., Michener, 2002), but other peculiar traits illustrated by Tosi (1896) require confirmation, although Meliponorytes appears to be similar to some African forms and is likely of the Hypotrigonina : Hypotrigonitae . The genus Cretotrigona , a stingless bee from the latest Cretaceous of eastern North America, is currently the oldest occurrence of eusocial bees and the earliest definitive crown-group bee ( Michener & Grimaldi, 1988; Engel , 2000). Its placement among Meliponini is uncertain and so the genus is considered as unplaced among the subtribes. Other fossil meliponines have been recovered from Eocene amber of the Baltic region, and the Miocene of China, Ethiopia (M.S.E., unpubl. data), Mexico, and the Dominican Republic ( Table 1).

As alluded to in the Introduction, stingless bees are not uncommon in the fossil record, and although the number of fossil species is not great, the abundance of individuals can be prodigious for certain taxa ( Camargo et al., 2000; Engel & Michener, 2013a). The same is true for meliponines in the Miocene deposits of Zhangpu. The stingless bees in Zhangpu amber represent both the Heterotrigonitae ( Tetragonula ) and Hypotrigonitae ( Austroplebeia ).