Print
A primitive honey bee from the Middle Miocene deposits of southeastern Yunnan, China (Hymenoptera, Apidae)
expand article infoMichael S. Engel§, Bo Wang|, Abdulaziz S. Alqarni#, Lin-Bo Jia¤, Tao Su«, Zhe-kun Zhou«¤, Torsten Wappler»
‡ University of Kansas, Lawrence, United States of America
§ American Museum of Natural History, New York, United States of America
| Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
¶ Institute of Zoology, Chinese Academy of Science, Beijing, China
# King Saud University, Riyadh, Saudi Arabia
¤ Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China
« Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China
» Hessisches Landesmuseum Darmstadt, Darmstadt, Germany
Open Access

Abstract

While fossils of honey bees (Apini: Apis Linnaeus) are comparatively abundant in European Oligocene and Miocene deposits, the available material from Asia is scant and represented by only a handful of localities. It is therefore significant to report a new deposit with a fossil honey bee from southern China. Apis (Synapis) dalica Engel & Wappler, sp. n., is described and figured from Middle Miocene sediments of Maguan County, southeastern Yunnan Province, China. This is the first fossil bee from the Cenozoic of southern China, and is distinguished from its close congeners present at the slightly older locality of Shanwang, Shandong in northeastern China. The species can be distinguished on the basis of wing venation differences from other Miocene Apis.

Keywords

Aculeata, Apinae, Apis, Apoidea, Miocene, taxonomy

Introduction

Honey bees (genus Apis Linnaeus) are iconic insects. The domesticated Western honey bee, Apis mellifera Linnaeus, is one of the most intensely studied animals (Winston 1991). Although most work focuses on A. mellifera for obvious apicultural and agricultural purposes, A. cerana Fabricius is also intensively managed and the remaining species are similarly exploited for their wax and honey. Honey bees comprise seven extant species of the corbiculate apine tribe Apini (Engel 1999a; Radloff et al. 2011), all of which are highly eusocial, with fixed queen and worker castes. This eusocial organization is shared with the related tribe Meliponini (stingless bees), while bumble bees (Bombini) occupy the primitively eusocial behavioral grade (Michener 1974, 2007). The putatively basalmost tribe of corbiculate bees, the Euglossini (orchid bees), are solitary or communal, with a few examples of primitive eusocial behavior in some species (Boff et al. 2015; Andrade et al. 2016). Relationships among these tribes have been controversial, although most evidence converges on a Darwinian null-hypothesis supporting a single origin of eusociality in the common ancestor of Bombini + Meliponini + Apini, and a single origin of the highly eusocial grade in the common ancestor of Meliponini + Apini (Michener 1990; Schultz et al. 1999, 2001; Engel 2001a; Noll 2002; Cardinal and Packer 2007; Canevazzi and Noll 2015; Porto et al. 2016, in press). Alternatively, some molecular evidence has placed meliponines as sister to bombines (e.g., Cameron and Mardulyn 2001; Kawakita et al. 2008; Rodriguez-Serrano et al. 2012), although in the most recent such analysis data from Euglossini were excluded (Kwong et al. 2017), and the potential impact of excluding one of the four surviving corbiculate tribes for driving spurious results has not been explored.

As is the case for most bees, the fossil record of corbiculate Apinae is comparatively sparse and largely confined to the Cenozoic, with a heavy bias toward material of Eocene through Miocene ages (Zeuner and Manning 1976; Engel 2001b, 2005; Ohl and Engel 2007; Michez et al. 2012). Euglossini have a meagre record, confined to the Early Miocene (Burdigalian) and younger deposits (Engel 1999b, 2014; Hinojosa-Díaz and Engel 2007), although an enigmatic and difficult to interpret compression from the latest Eocene of North America could represent a stem-group euglossine (Dehon et al. 2014). Bombini have a slightly stronger record (Rasnitsyn and Michener 1991; Michez et al. 2012; Wappler et al. 2012; Prokop et al. 2017), which is in need of revision but demonstrates the persistence of the crown group since at least the Eocene. Perhaps owing to the fact that all species are highly eusocial, often with large numbers of individuals within perennial colonies, fossils of Meliponini and Apini are the most abundant. In fact, in sheer numbers meliponine fossils outpace those of all other bees combined, although this is entirely due to a preponderance of material of workers from one species, Proplebeia dominicana (Wille & Chandler), from the Early Miocene of the Dominican Republic (Camargo et al. 2000). All other fossil stingless bee species are rare, but span from the end of the Cretaceous (Maastrichtian) to Pleistocene copals (Michener 1982; Michener and Grimaldi 1988; Engel 2001b; Greco et al. 2011; Engel and Michener 2013a, 2013b). Honey bees, again largely based on fossils of the worker caste, are known from a sparse number of deposits (Zeuner and Manning 1976; Nel et al. 1999), but at some they can be found in large numbers (e.g., Armbruster 1938; Kotthoff et al. 2011). These fossils span a range of ages from the earliest Oligocene through to the Pleistocene (Engel 1998a, 1999a, 2006; Engel et al. 2009; Kotthoff et al. 2011), although the taxonomic status of several putative species remains to be evaluated. Aside from these tribes, three other corbiculate tribes were once present – Electrobombini, Electrapini, and Melikertini (Engel 1998b, 2001b; Wappler and Engel 2003; Patiny et al. 2007; Engel et al. 2013, 2014). These extinct tribes were all eusocial, with the latter two belonging to the highly eusocial clade (Engel 2000b, 2001a, 2001b), and for at least one there is relatively detailed information on pollen collection for populations from the Lutetian of Germany (Wappler et al. 2015; Grímsson et al. 2017). More extensive work is needed regarding the refinement of relationships, but it is possible that one group of electrapines, genus Thaumastobombus Engel, was more closely related to honey bees owing to the presence of a barbed sting (Engel 2001).

Among the fossil Apini, there is apparently a gradation of taxa leading from the earliest Oligocene to the Miocene appearance of the first species of the clade comprising the surviving subgenera Micrapis Ashmead, Megapis Ashmead, and Apis s. str. (Engel 1998a, 1999, 2006). The extant clades form a monophyletic group relative to earlier species, the subgenera Priorapis Engel, Synapis Cockerell, and Cascapis Engel composing a basal grade (Engel 1998a, 1999, 2006). While most of the fossil species are found across Eurasia, well within the bounds of the modern, native distribution of Apis in Europe, Africa, and Asia, at least one species occurred within western North America during the Middle Miocene (Engel et al. 2009; Kotthoff et al. 2013). Within Asia there are few localities with sufficiently preserved material of honey bees (e.g., Stauffer 1979; Hong 1983; Zhang 1989, 1990; Engel 2006), most specimens deriving from the Upper Miocene deposits of Shanwang in northeastern China (Hong 1983; Zhang 1989, 1990). Herein we report the finding of a new fossil honey bee species from the Middle Miocene deposits of southern China. The species belongs to Synapis, expanding not only the paleogeographic distribution of this group but extending their temporal presence slightly later into the Miocene, approximately 1–2 million years younger than those records from the Northeast.

Materials and methods

Insect fossils were collected from the northwestern Maguan Basin, southeastern Yunnan, southwestern China (23°01'N, 104°23'E, 1320 m a.s.l.) (Figure 1). The Cenozoic sediments in Maguan are composed of the Paleogene Yanshan Group, Neogene Huazhige Formation, and Quaternary deposits (Zhang 1976; Bureau of Geology and Mineral Resources 1990; Zhang et al. 2015b). The basal Paleogene Yanshan Group is characterized by coarse breccias and lacks fossils (Zhang 1976; Zheng et al. 1999). Sitting unconformably on the Paleogene deposits, the Huazhige Formation is a fluvio-lacustrine deposit, composed of light-gray or light-yellow pelitic laminated siltstone and mudstone, and bears abundant animal and plant fossils (Figure 2) (Zhang 1976; Zhang et al. 2015b). The Quaternary deposits overly unconformably on the Huazhige Formation (Zhang 1976; Zhang et al. 2015b).

Figures 1–3. 

Fossil locality in Maguan County, southeastern Yunnan Province, China. 1 Outcrop overview, green arrow showing layers bearing the present fossil 2 Example of preservation, Acer cf. coriaceifolia H. Lév. (Sapindaceae) preserved together with a nematoceran fly (position indicated by white arrow) 3 Schematic cross section of the studied area.

The sediments bearing the present insect fossils are characterized by cyclic deposits of light-yellow or light-grey pelitic laminated mudstone and siltstone (Figure 3). They belong to the Huazhige Formation according to stratigraphic correlations (Zhang 1976; Zhang et al. 2015b). The Huazhige Formation is also well developed in the Wenshan Basin approximately 50 km to the north of the Maguan Basin, and the two basins are inferred to be the same age (Bureau of Geology and Mineral Resources 1990; Lebreton-Anberrée et al. 2016). The age of the Huazhige Formation in the Wenshan Basin was assigned to 16.5–15.2 Ma based on a recent palaeomagnetic study (Lebreton-Anberrée et al. 2016). Therefore, the age of the Huazhige Formation in the Maguan Basin should also be the Middle Miocene.

Besides insect fossils, the sediments bear abundant fossils of fishes, birds, as well as plants in excellent preservation (Figure 2). A preliminary study of plant fossils from the outcrop shows that the plant flora was dominated by Fagaceae and Fabaceae, accompanied by other elements such as Calocedrus Kurz (Zhang et al. 2015a), Sequioa Endl. (Cupressaceae) (Zhang et al. 2015b), Bauhinia L. (Fabaceae), Burretiodendron Rehder (Malvaceae) (Lebreton-Anberrée et al. 2015), Cedrelospermum Saporta (Ulmaceae) (Jia et al. 2015), and Ailanthus Desf. (Simaroubaceae), indicating a subtropical evergreen forest with warm and wet environment.

For the description, morphological terminology is adapted from Engel (2001b) and Michener (2007), with formats following previous studies on fossil honey bees (e.g., Engel 2006; Engel et al. 2009) and presented in the context of furthering refinements of species-level diagnoses for bees (e.g., Engel 2011; Gonzalez et al. 2013). The fossil is carbonized and so the integumental coloration or even patterning of lighter versus darker areas is not preserved. Photographs were taken using a Zeiss Stereo Discovery V16 microscope system at the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences.

Systematic paleontology

Tribe Apini Latreille, 1802

Genus Apis Linnaeus, 1758

Subgenus Synapis Cockerell, 1907

Apis (Synapis) dalica Engel & Wappler, sp. n.

Figs 4–7, 8–9

Holotype

Worker (Figure 4), NIGP154200; Middle Miocene, approximately 16.5–15.2 Ma (around the Tortonian-Serravallian boundary); northeastern suburb of Maguan, Maguan County, Wenshan Zhuang & Miao Autonomous Prefecture, Yunnan Province, China. The holotype is deposited in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China.

Figures 4–7. 

Holotype worker of Apis (Synapis) dalica Engel and Wappler, sp. n., from Maguan County, southeastern Yunnan Province, China. 4 Entire holotype (NIGP154200) as preserved 5 Reconstruction of wing venation; forewing above, hind wing below 6 Detail of foreleg. 7 Detail of apical sterna. Abbreviations: ppl = propleuron, mcx = mesocoxa, tr = trochanter, fm = femur, tb = tibia.

Diagnosis

The new species is most similar to those Miocene honey bees described from Shandong Province, China. Apis dalica differs from them in the gently arched basal vein (comparatively straight in the specimens from Shandong), which is also closer to 1cu-a (separated by about a vein width versus several vein widths and even up to 0.5–0.75 times crossvein length in material from Shandong: refer to figures presented by Zhang 1989, and Zhang et al. 1994). In addition, in A. longitibia Zhang and A. miocenica Hong 2rs-m is comparatively straight (Zhang 1989; Zhang et al. 1994), rather than the distinctly arcuate form of A. dalica. In A. shandongica Zhang and A. miocenica 1m-cu is not so prominently arched and only so at its anterior end rather than strongly so and at midlength in A. dalica. Lastly, in all of the material from Shandong (Zhang 1989; Zhang et al. 1994), 1Rs originates in a strongly proximal position relative to the base of the pterostigma, rather than near the base of the pterostigma in A. dalica. The pterostigma of A. dalica is more distinctly developed than in modern species and most other fossil species of Apis.

Description

Worker. Total length (as preserved) 17.06 mm; preserved in ventral orientation, with head thrust forward, wings extended obliquely away from body, and legs largely tucked underneath the body with most podites not preserved or indiscernible; coloration not preserved (appearing uniformly charcoal black). Head apparently slightly longer than wide as interpreted in ventral position; malar space elongate, longer than basal mandibular width; head narrower than mesosoma. Leg podites incompletely preserved. Metasoma typical for worker honey bee, length (as preserved) 9.03 mm, maximum width 4.36 mm; apical margins of sterna somewhat concave, those more basal sterna relatively straight, apical most sterna more strongly concave; sting not extended but slightly evident extending along midline of apical sterna (Figure 7).

Forewing with venation typical of Apis and subgenus Synapis (Figs 4, 5, 8, 9), length 8.54 mm, maximum width 2.18 mm; basal vein (1M) slightly distad 1cu-a, separated from 1cu-a by distance scarcely greater than vein width, gently arched before meeting 1Rs; 1Rs about as long as 1Rs+M and not in line with 1M; first submarginal cell smallest, with 2Rs sinuate (rather than relatively straight); r-rs about as long as anterior margin of second submarginal cell; second submarginal cell trapezoidal, with 1rs-m relatively straight and strongly slanted apically such that posterior border of cell is slightly more than three times length of anterior border; 1m-cu meeting posterior border of second submarginal cell at basal third of cell length, with distinct abscissal stub present at about angle of midlength, stub projecting into proximal border of second medial cell; third submarginal cell relatively broad anteriorly, with 2rs-m arcuate, anterior border of third submarginal cell distinctly longer than anterior border of second submarginal cell; aRs2 absent (sensu Tan et al. 2008); 2m-cu meeting posterior border of third submarginal cell near apical quarter of cell length, crossvein relatively straight. Hind wing with typical Apis venation, length 6.37 mm, maximum width 1.39 mm; linear series of distal hamuli present along anterior wing margin (precise number not discernible); distal abscissa M (‘indica’ vein) present, about as long as rs-m (Figure 5).

Figures 8–9. 

Wings of Apis (Synapis) dalica Engel and Wappler, sp. n., from Maguan County, southeastern Yunnan Province, China. 8 Details of right forewing 9 Details of left forewing.

Etymology

The specific epithet refers to the Medieval Dali Kingdom which occupied the area of Yunnan from its founding in 937 AD at the close of the Nanzhao Kingdom and until its termination by Kublai Khan (1215–1294) and the Mongol invasion in 1253 AD.

Discussion

Fossil honey bees are comparatively uncommon in Asia relative to the wealth of material available from a variety of European deposits of Oligocene and Miocene ages (e.g., Nel et al. 1999; Kotthoff et al. 2011, 2013). In fact, most fossil honey bees in Asia have been found at a single locality in Shandong Province (Zhang 1989; Zhang et al. 1994). Unfortunately, the descriptions and available photographs of the material from Shandong are incomplete and there is reason to believe that some of the species from these deposits are synonyms of each other (Engel 1998, 1999), particularly in light of the fact that species of Apis can be notoriously variable in many features (e.g., Ruttner 1988; Radloff et al. 2010; Kotthoff et al. 2011, 2013). Thus, the present dearth of abundant specimens from which to work hampers a more comprehensive understanding of apine diversity in Asia during the Neogene, a period of time in which considerable diversification was apparently underway among honey bees such that by the present day the greatest number of species of Apis may be found across the Indomalayan region (e.g., Engel 1999, 2012; Michener 2007; Radloff et al. 2011).

The discovery of A. dalica expands the known localities with fossil honey bees southward in China and the presence of highly eusocial bees and critical pollinators within the Miocene of fauna of Yunnan. It is hoped that further exploration will recover larger numbers of workers from which the general morphometrics of the species can be determined and more precisely circumscribe the taxon among other Apini, as well as refine phylogenetic relationships among early honey bees. Phylogenetic studies on the modern species have demonstrated that open-nesting is ancestral for the genus (Engel and Schultz 1997). Given that most of the known fossil Apis fall basal to the clade of modern subgenera (e.g., Engel 2006; Kotthoff et al. 2013), and that A. dalica’s wing venation places it among species of the extinct subgenus Synapis, it is presumed that A. dalica would have constructed their nests in exposed localities, perhaps attached to the branches of trees or sturdy bushes. Such perennial colonies would have been more impacted by temperature changes over the course of the year, implying that the local paleoclimate was comparatively steady.

Acknowledgements

This research was supported by the National Natural Science Foundation of China (41572010, 41622201, 41688103, U1502231) and the Chinese Academy of Sciences (XDPB05). The project was also supported by the International Scientific Partnership Program (ISPP) at King Saud University through ISPP #0083 (M.S.E. and A.S.A.). T.W. was supported by the German Research Foundation (WA 1496/6-1, Heisenberg grant WA 1496/8-1).

References

  • Andrade AC, Miranda EA, Del Lama MA, Nascimento FS (2016) Reproductive concessions between related and unrelated members promote eusociality in bees. Scientific Reports 6: 26635. https://doi.org/10.1038/srep26635
  • Armbruster L (1938) Versteinerte Honigbienen aus dem obermiocänen Randecker Maar. Archiv für Bienenkunde 19(1): 1–48.
  • Boff S, Forfert N, Paxton RJ, Montejo E, Quezada-Euan JJG (2015) A behavioral guard caste in a primitively eusocial orchid bee, Euglossa viridissima, helps defend the nest against resin theft by conspecifics. Insectes Sociaux 62(2): 247–249. https://doi.org/10.1007/s00040-015-0397-3
  • Bureau of Geology and Mineral Resources (1990) Regional Geology of Yunnan Province. Geology Press, Beijing, 728 pp. [In Chinese].
  • Camargo JMF, Grimaldi DA, Pedro SRM (2000) The extinct fauna of stingless bees (Hymenoptera: Apidae: Meliponini) in Dominican amber: Two new species and redescription of the male of Proplebeia dominicana (Wille and Chandler). American Museum Novitates 3293: 1–24. https://doi.org/10.1206/0003-0082(2000)293<0001:TEFOSB>2.0.CO;2
  • Cameron SA, Mardulyn P (2001) Multiple molecular data sets suggest independent origins of highly eusocial behaviour in bees (Hymenoptera: Apinae). Systematic Biology 50(2): 194–214. https://doi.org/10.1080/10635150120230
  • Canevazzi NCS, Noll FB (2015) Cladistic analysis of self-grooming indicates a single origin of eusociality in corbiculate bees (Hymenoptera: Apidae). Cladistics 31(2): 126–141. https://doi.org/10.1111/cla.12077
  • Cockerell TDA (1907) A fossil honey-bee. Entomologist 40(533): 227–229.
  • Dehon M, Michez D, Nel A, Engel MS, De Meulemeester T (2014) Wing shape of four new bee fossils (Hymenoptera: Anthophila) provides insights to bee evolution. PLoS ONE 9(10): e108865. https://doi.org/10.1371/journal.pone.0108865
  • Engel MS (1998b) A new species of the Baltic amber bee genus Electrapis (Hymenoptera: Apidae). Journal of Hymenoptera Research 7(1): 94–101.
  • Engel MS (1999a) The taxonomy of Recent and fossil honey bees (Hymenoptera: Apidae; Apis). Journal of Hymenoptera Research 8(2): 165–196.
  • Engel MS (1999b) The first fossil Euglossa and phylogeny of the orchid bees (Hymenoptera: Apidae; Euglossini). American Museum Novitates 3272: 1–14.
  • Engel MS (2000b) Fossils and phylogeny: A paleontological perspective on social bee evolution. In: Bitondi MMG, Hartfelder K (Eds) Anais do IV Encontro sobre Abelhas. Universidade de São Paulo, Ribeirão Preto, 217–224.
  • Engel MS (2001a) Monophyly and extensive extinction of advanced eusocial bees: insights from an unexpected Eocene diversity. Proceedings of the National Academy of Sciences, USA 98(4): 1661–1664. https://doi.org/10.1073/pnas.98.4.1661
  • Engel MS (2005) Geological history of the bees (Hymenoptera: Apoidea). Revista de Tecnologia e Ambiente 10(2): 9–33.
  • Engel MS (2006) A giant honey bee from the middle Miocene of Japan (Hymenoptera: Apidae). American Museum Novitates 3504: 1–12.
  • Engel MS (2012) The honey bees of Indonesia (Hymenoptera: Apidae). Treubia 39: 41–49.
  • Engel MS, Hinojosa-Díaz IA, Rasnitsyn AP (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 MS, Michener CD (2013a) A minute stingless bee in Eocene Fushan [sic] amber from northeastern China (Hymenoptera: Apidae). Journal of Melittology 14: 1–10. https://doi.org/10.17161/jom.v0i14.4560
  • Engel MS, Michener CD (2013b) Geological history of the stingless bees (Apidae: Meliponini). In: Vit P, Roubik DW (Eds) Stingless Bees Process Honey and Pollen in Cerumen Pots. Universidad de Los Andes, Mérida, 1–7. http://www.saber.ula.ve/handle/123456789/37108
  • Engel MS, Schultz TR (1997) Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Annals of the Entomological Society of America 90(1): 43–53. https://doi.org/10.1093/aesa/90.1.43
  • Gonzalez VH, Griswold T, Engel MS (2013) Obtaining a better taxonomic understanding of native bees: where do we start? Systematic Entomology 38(4): 645–653. https://doi.org/10.1111/syen.12029
  • Greco MK, Welz PM, Siegrist M, Ferguson SJ, Gallmann P, Roubik DW, Engel MS (2011) Description of an ancient social bee trapped in amber using diagnostic radioentomology. Insectes Sociaux 58(4): 487–494. https://doi.org/10.1007/s00040-011-0168-8
  • Hong YC (1983) Fossil insects in the diatoms of Shanwang. Bulletin of the Tianjin Institute of Geology and Mineral Resources 8: 1–15. [In Chinese]
  • Jia LB, Manchester SR, Su T, Xing YW, Chen WY, Huang YJ, Zhou ZK (2015) First occurrence of Cedrelospermum (Ulmaceae) in Asia and its biogeographic implications. Journal of Plant Research 128(5): 747–761. https://doi.org/10.1007/s10265-015-0739-2
  • Kawakita A, Ascher JS, Sota T, Kato M, Roubik DW (2008) Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein-coding genes (Hymenoptera: Apoidea: Apidae). Apidologie 39(1): 163–175. https://doi.org/10.1051/apido:2007046
  • Kotthoff U, Wappler T, Engel MS (2013) Greater past disparity and diversity hints at ancient migrations of European honey bee lineages into Africa and Asia. Journal of Biogeography 40(10): 1832–1838. https://doi.org/10.1111/jbi.12151
  • Kwong WK, Medina LA, Koch H, Sing K-W, Soh EJY, Ascher JS, Jaffé R, Moran NA (2017) Dynamic microbiome evolution in social bees. Science Advances 3(3): e1600513. https://doi.org/10.1126/sciadv.1600513
  • Latreille PA (1802) Histoire naturelle des fourmis, et recueil de memoires et d’observations sur les abeilles, les araignées, les faucheurs, et autres insectes. Crapelet, Paris, xvi + 445 pp.
  • Lebreton-Anberrée J, Li SH, Li SF, Spicer RA, Zhang ST, Su T, Deng CL, Zhou ZK (2016) Lake geochemistry reveals marked environmental change in Southwest China during the Mid Miocene Climatic Optimum. Science Bulletin 61(11): 897–910. https://doi.org/10.1007/s11434-016-1095-x
  • Lebreton-Anberrée J, Manchester SR, Huang J, Li SF, Wang YQ, Zhou ZK (2015) First fossil fruits and leaves of Burretiodendron s.l. (Malvaceae s.l.) in Southeast Asia: Implications for taxonomy, biogeography, and paleoclimate. International Journal of Plant Sciences 176(7): 682–696. https://doi.org/10.1086/682166
  • Linnaeus C (1758) Systema Naturae per regna tria natura, secundum classes, ordines, genera, species, cum characteribus, differentiis synonymis, locis [10th Edition, revised]. Laurentii Salvii, Holmiae, 824 pp.
  • Michener CD (1974) The Social Behavior of the Bees: A Comparative Study. Harvard University Press, Cambridge, xii + 404 pp.
  • Michener CD (1982) A new interpretation of fossil social bees from the Dominican Republic. Sociobiology 7(1): 37–45.
  • Michener CD (1990) Classification of the Apidae (Hymenoptera). University of Kansas Science Bulletin 54(4): 75–163.
  • Michener CD (2007) The Bees of the World [2nd Edition]. Johns Hopkins University Press, Baltimore, xvi + [i] + 953 pp., 20 pls.
  • Michener CD, Grimaldi DA (1988) A Trigona from Late Cretaceous amber of New Jersey (Hymenoptera: Apidae: Meliponinae). American Museum Novitates 2917: 1–10.
  • Michez D, Vanderplanck M, Engel MS (2012) Fossil bees and their plant associates. In: Patiny S (Ed.) Evolution of Plant-Pollinator Relationships. Cambridge University Press, Cambridge, 103–164.
  • Nel A, Martínez-Delclòs X, Arillo A, Peñalver E (1999) A review of the Eurasian fossil species of the bee Apis. Palaeontology 42(2): 243–285.
  • Noll FB (2002) Behavioral phylogeny of corbiculate Apidae (Hymenoptera; Apinae), with special reference to social behavior. Cladistics 18(2): 137–153. https://doi.org/10.1006/clad.2001.0191
  • Ohl M, Engel MS (2007) Die Fossilgeschichte der Bienen und ihrer nächsten Verwandten (Hymenoptera: Apoidea). Denisia 20: 687–700.
  • Patiny S, Engel MS, Vanmarsenille P, Michez D (2007) A new record of Thaumastobombus andreniformis Engel 2001 in Eocene amber (Hymenoptera: Apidae). Annales de la Société Entomologique de France 43(4): 505–508. https://doi.org/10.1080/00379271.2007.10697540
  • Porto DS, Almeida EAB, Vilhelmsen L (in press) Comparative morphology of internal structures of the mesosoma of bees with an emphasis on the corbiculate clade (Apidae: Apini). Zoological Journal of the Linnean Society. https://doi.org/10.1111/zoj.12466
  • Porto DS, Vilhelmsen L, Almeida EAB (2016) Comparative morphology of the mandibles and head structures of corbiculate bees (Hymenoptera: Apidae: Apini). Systematic Entomology 41(2): 339–368. https://doi.org/10.1111/syen.12156
  • Radloff SE, Hepburn C, Hepburn HR, Fuchs S, Hadisoesilo S, Tan K, Engel MS, Kuznetsov V (2010) Population structure and classification of Apis cerana. Apidologie 41(6): 589–601. https://doi.org/10.1051/apido/2010008
  • Rasnitsyn AP, Michener CD (1991) Miocene fossil bumble bee from the Soviet Far East with comments on the chronology and distribution of fossil bees (Hymenoptera: Apidae). Annals of the Entomological Society of America 85(6): 583–589. https://doi.org/10.1093/aesa/84.6.583
  • Rodriguez-Serrano E, Inostroza-Michael O, Avaria-Llautureo J, Hernandez CE (2012) Colony size evolution and the origin of eusociality in corbiculate bees (Hymenoptera: Apinae). PLoS ONE 7(7): e40838. https://doi.org/10.1371/journal.pone.0040838
  • Schultz TR, Engel MS, Ascher JS (2001) Evidence for the origin of eusociality in the corbiculate bees (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 74(1): 10–16.
  • Schultz TR, Engel MS, Prentice M (1999) Resolving conflict between morphological and molecular evidence for the origin of eusociality in the corbiculate bees (Hymenoptera: Apidae): A hypothesis-testing approach. University of Kansas Natural History Museum Special Publication 24: 125–138.
  • Stauffer PH (1979) A fossilized honeybee comb from Late Cenozoic cave deposits at Batu Caves, Malay Peninsula. Journal of Paleontology 53(6): 1416–1421.
  • Tan K, Fuchs S, Engel MS (2008) An adventitious distal abscissa in the forewing of honey bees (Hymenoptera: Apidae: Apis). Apidologie 39(6): 674–682. https://doi.org/10.1051/apido:2008052
  • Wappler T, De Meulemeester T, Aytekin AM, Michez D, Engel MS (2012) Geometric morphometric analysis of a new Miocene bumble bee from the Randeck Maar of southwestern Germany (Hymenoptera: Apidae). Systematic Entomology 37(4): 784–792. https://doi.org/10.1111/j.1365-3113.2012.00642.x
  • Wappler T, Labandeira CC, Engel MS, Zetter R, Grímsson F (2015) Specialized and generalized pollen-collection strategies in an ancient bee lineage. Current Biology 25(23): 3092–3098. https://doi.org/10.1016/j.cub.2015.09.021
  • Winston ML (1991) The Biology of the Honey Bee. Harvard University Press, Cambridge, vii i + [iv] + 281 pp.
  • Zeuner FE, Manning FJ (1976) A monograph on fossil bees (Hymenoptera: Apoidea). Bulletin of the British Museum (Natural History), Geology 27(3): 149–268, +4 pls.
  • Zhang CH (1976) The report to the regional geological survey (1/200,000) of Wenshan/Maguan Scope (F-48-3, F-48-9). Geological Bureau of Yunnan Province, Yunnan, 24 pp. [In Chinese]
  • Zhang JF (1989) Fossil Insects from Shanwang, Shandong, China. Shandong Science & Technology Publishing House, Jinan, 459 pp, 92 pls. [In Chinese]
  • Zhang JF (1990) New fossil species of Apoidea (Insecta: Hymenoptera). Acta Zootaxonomica Sinica 15(1): 83–91. [In Chinese]
  • Zhang JF, Sun B, Zhang XY (1994) Miocene Insects and Spiders from Shanwang, Shandong. Science Press, Beijing, v + 298 pp, 44 pls. [In Chinese]
  • Zhang JW, Huang J, D’Rozario A, Adams JM, Zhou ZK (2015a) Calocedrus shengxianensis, a late Miocene relative of C. macrolepis (Cupressaceae) from South China: Implications for paleoclimate and evolution of the genus. Review of Palaeobotany and Palynology 222: 1–15. https://doi.org/10.1016/j.revpalbo.2015.07.004
  • Zhang JW, D’Rozario A, Adams JM, Li Y, Liang XQ, Jacques FM, Su T, Zhou ZK (2015b) Sequoia maguanensis, a new Miocene relative of the coast redwood, Sequoia sempervirens, from China: Implications for paleogeography and paleoclimate. American Journal of Botany 102(1): 103–18. https://doi.org/10.3732/ajb.1400347
  • Zheng JJ, Liu SW, Huang XS, Chen F, Qiu ZD (1999) Chinese Stratigraphical Thesaurus, Tertiary. Geological Publishing House, Beijing, 163 pp. [In Chinese]