Insectes Sociaux

, 58:487 | Cite as

Description of an ancient social bee trapped in amber using diagnostic radioentomology

  • M. K. Greco
  • P. M. Welz
  • M. Siegrist
  • S. J. Ferguson
  • P. Gallmann
  • D. W. Roubik
  • M. S. Engel
Research Article


The application of non-invasive imaging technologies using X-radiation (diagnostic radioentomology, ‘DR’) is demonstrated for the study of amber-entombed social bees. Here, we examine the external and internal morphology of an Early Miocene (Burdigalian) stingless bee (Apinae: Meliponini) from the Dominican Republic using non-destructive X-ray microtomography analysis. The study permits the accurate reconstruction of features otherwise obscured or impossible to visualize without destroying the sample and allows diagnosis of the specimen as a new species, Proplebeia adbita Greco and Engel.


Proplebeia Stingless bees Diagnostic radioentomology Miocene Burdigalian MicroCT Amber 



This work is dedicated to the memory of Prof. J.M.F. Camargo, leading authority on the systematics of stingless bees and who had initially participated in this work, suggesting that the specimen belonged to a new species. We regret his untimely passing. The authors would like also to thank Giuliana Tromba, Lucia Mancini and Nicola Sodini for their contribution to the experimental work. We are grateful to DISECT Systems Ltd for donating their 3D rendering and telelinking software for this study, and to the two anonymous reviewers for their positive feedback on an earlier draft of the manuscript.


  1. Abrami A., Arfelli F., Barroso R.C., Bergamaschi A., Billè F., Bregant P., Brizzi F., Casarin K., Castelli E., Chenda V., Dalla Palma L., Dreossi D., Fava C., Longo R., Mancini L., Menk R., Montanari F., Olivo A., Pani S., Pillon A., Quai E., Kaiser S.R., Rigon L., Rokvic T., Tonutti M., Tromba G., Vascotto A., Venanzi C., Zanconati F., Zanetti A. and Zanini F. 2005. Medical applications of synchrotron radiation at the SYRMEP beamline of ELETTRA. Nuclear Instruments and Methods in Physics Research, Section A: Accelerators, Spectrometers, Detectors and Associated Equipment 548: 221-227Google Scholar
  2. Araujo V.A. Zama U., Dolder H. and Lino-Neto J. 2005. Morphology and ultrastructure of the spermatozoa of Scaptotrigona xanthotricha Moure (Hymenoptera: Apidae: Meliponini). Braz. J. Morph. Sci. 22: 137-141Google Scholar
  3. Bänziger H. and Bänziger S. 2010. Mammals, birds and reptiles as hosts of Lisotrigona bees, the tear drinkers with the broadest host range (Hymenoptera, Apidae). Mitt. Schweiz. Entomol. Ges. 83: 271-282Google Scholar
  4. Bänziger H., Boongird S., Sukumalanand P. and Bänziger S. 2009. Bees (Hymenoptera: Apidae) that drink human tears. J. Kansas Entomol. Soc. 82: 135-150Google Scholar
  5. Bettuzzi M.S., Casali F., Cornacchia S., Rossi M., Paltrinieri E., Morigi M.P., Brancaccio R. and Romani D. 2004. A new linear array detector for high resolution and low dose digital radiography. Nucl. Instr. Method. B 213: 227-230Google Scholar
  6. Betz O., Wegst U., Weide D., Heethoff M., Helfen L., Lee W.-K. and Cloetens P. 2007. Imaging applications of synchrotron X-ray phase-contrast microtomography in biological morphology and biomaterials science. I. General aspects of the technique and its advantages in the analysis of millimetre-sized arthropod structure. J. Microsc. 227: 51-71Google Scholar
  7. Camargo J.M.F. 2008. Biogeografia histórica dos Meliponini (Hymenoptera, Apidae, Apinae) da região Neotropical, In: Abejas sin Aguijón y Valorización Sensorial de su Miel (P. Vit, Ed), APIBA-DIGECEX, Universidad de Los Andes, Merida. pp 13-26Google Scholar
  8. Camargo J.M.F. and Roubik D.W. 1991. Systematics and bionomics of the apoid obligate necrophages: The Trigona hypogea group (Hymenoptera: Apidae; Meliponinae). Biol. J. Linn. Soc. 44: 13-39Google Scholar
  9. Camargo J.M.F., Grimaldi D.A. and Pedro S.R.M. 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). Am. Mus. Novitates 3293: 1-24Google Scholar
  10. Cardinal S. and Packer L. 2007. Phylogenetic analysis of the corbiculate Apinae based on morphology of the sting apparatus (Hymenoptera: Apidae). Cladistics 23: 99-118Google Scholar
  11. Engel M.S. 1995. Neocorynura electra, a new fossil bee species from Dominican amber (Hymenoptera: Halictidae). J. N.Y. Entomol. Soc. 103: 317-323.Google Scholar
  12. Engel M.S. 1996. New augochlorine bees (Hymenoptera: Halictidae) in Dominican amber, with a brief review of fossil Halictidae. J. Kansas Entomol. Soc., Suppl. 69: 334-345Google Scholar
  13. Engel M.S. 1997. A new fossil bee from the Oligo-Miocene Dominican amber (Hymenoptera: Halictidae). Apidologie 28: 97-102Google Scholar
  14. Engel M.S. 2000. A new interpretation of the oldest fossil bee (Hymenoptera: Apidae). Am. Mus. Novitates 3296: 1-11Google Scholar
  15. Engel M.S. 2001a. A monograph of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bull. Am. Mus. Nat. Hist. 259: 1-192Google Scholar
  16. Engel M.S. 2001b. Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proc. Natl Acad. Sci. U.S.A. 98: 1661-1664Google Scholar
  17. Engel M.S. 2004. Geological history of the bees (Hymenoptera: Apoidea). Rev. Tecnol. Amb. 10: 9-33Google Scholar
  18. Engel M.S. 2005. Family-group names for bees (Hymenoptera: Apoidea). Am. Mus. Novitates 3476: 1-33Google Scholar
  19. Engel M.S. 2011. Systematic melittology: Where to from here? Syst. Entomol. 36: 2-15Google Scholar
  20. Feeney D.S., Crawford J.W., Daniell T., Hallett P.D., Nunan N., Ritz K., Rivers M. and Young I.M. 2006. Three-dimensional microorganization of the soil–root–microbe system. Microbiol. Ecol. 52: 151-158Google Scholar
  21. Fuchs A., Schreyer A., Feuerbach S. and Korb J. 2004. A new technique for termite monitoring using computer tomography and endoscopy. Int. J. Pest Manag. 50: 63-66Google Scholar
  22. Gerling D. and Hermann H.R. 1978. Biology and mating behavior of Xylocopa virginica L. (Hymenoptera: Anthophoridae). Behav. Ecol. Sociobiol. 3: 99-111Google Scholar
  23. Gerling D., Hurd P.D. Jr. and Hefetz A. 1981. In-nest behavior of the carpenter bee, Xylocopa pubescens Spinola (Hymenoptera: Anthophoridae). J. Kansas Entomol. Soc. 54: 209-218Google Scholar
  24. Greco M.K., Bell M., Spooner-Hart R. and Holford P. 2006. X-ray computerized tomography as a new method for monitoring Amegilla holmesi nest structure, nesting behaviour and adult female activity. Entomol. Exper. Appl. 120: 71-76Google Scholar
  25. Greco M.K., Hoffmann D., Dollin A., Duncan M., Spooner-Hart R. and Neumann P. 2009. The alternative Pharaoh approach: Stingless bees encapsulate beetle parasites alive. Naturwissenschaften 97: 319-323Google Scholar
  26. Greco M.K., Jones A., Spooner-Hart R. and Holford P. 2008. X-ray computerised microtomography (MicroCT): A new technique for assessing external and internal morphology of bees. J. Apicult. Res. 47: 286-291Google Scholar
  27. Greco M.K., Spooner-Hart R. and Holford P. 2005. A new technique for monitoring Trigona carbonaria nest contents, brood and activity using X-ray computerised tomography. J. Apicult. Res. 44: 97-100Google Scholar
  28. Grimaldi D. 1995. The age of Dominican amber. In: Amber, Resinite, and Fossil Resins (Anderson K.B. and Crelling J.C., Eds). American Chemical Society, Washington, DC: pp 203-217Google Scholar
  29. Grimaldi D. and Engel M.S. 2005. Evolution of the Insects. Cambridge University Press; Cambridge, UK.Google Scholar
  30. Grimaldi D., Bonwich E., Delannoy M. and Doberstein S. 1994. Electron microscopic studies of mummified tissues in amber fossils. Am. Mus. Novitates 3097: 1-31Google Scholar
  31. Heethoff M., Helfen L. and Norton R.A. 2009. Description of Neoliodes dominicus n.sp. (Acari, Oribatida) from Dominican amber, aided by synchrotron X-ray microtomography. J. Paleontol. 83: 153-159Google Scholar
  32. Hinojosa-Díaz I.A. and Engel M.S. 2008. Juxtocellar structures in euglossine bees: A new character for corbiculate studies (Hymenoptera: Apidae). Beitr. Entomol. 58: 97-105Google Scholar
  33. Hörnschemeyer T., Beutel R.G. and Pasop F. 2002. Head structures of Priacma serrata LeConte (Coleoptera, Archostemata) inferred from X-ray tomography. J. Morphol. 252: 298-314Google Scholar
  34. Iturralde-Vinent M.E. and MacPhee R.D.E. 1996. Age and paleogeographical origin of Dominican amber. Science 273: 1850-1852Google Scholar
  35. Johnson S.N., Read D.B. and Gregory P.J. 2004. Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecol. Entomol. 29: 117-122Google Scholar
  36. Kawakita A., Ascher J.S., Sota T., Kato M. and Roubik D.W. 2008. Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein-coding genes (Hymenoptera: Apoidea: Apidae). Apidologie 39: 163-175Google Scholar
  37. Lak M., Néraudeau D., Nel A., Cloetens P., Perrichot V. and Tafforeau P. 2008. Phase contrast X-ray synchrotron imaging: Opening access to fossil inclusions in opaque amber. Microsc. Microanal. 14: 251-259Google Scholar
  38. Lak M., Fleck G., Azar D., Engel M.S., Kaddumi H.F., Neraudeau D., Tafforeau P. and Nel A. 2009. Phase contrast x-ray synchrotron microtomography and the oldest damselflies in amber (Odonata: Zygoptera: Hemiphlebiidae). Zool. J. Linn. Soc. 156: 913-923Google Scholar
  39. Lambert J.B., Frye J.S. and Poinar G.O. Jr 1985. Amber from the Dominican Republic: An analysis by nuclear magnetic resonance spectroscopy. Archaeometry 27: 43-51Google Scholar
  40. Mateus S. and Noll F. 2004. Predatory behavior in a necrophagous bee Trigona hypogea (Hymenoptera; Apidae, Meliponini). Naturwissenschaften 91: 94-96Google Scholar
  41. Michener C.D. 1974. The Social Behavior of the Bees: A Comparative Study. Belknap Press; Cambridge, MA.Google Scholar
  42. Michener C.D. 1982. A new interpretation of fossil social bees from the Dominican Republic. Sociobiology 7: 37-45Google Scholar
  43. Michener C.D. 1990. Classification of the Apidae (Hymenoptera). Univ. Kansas Science Bull. 54: 75-164Google Scholar
  44. Michener C.D. 2007. The Bees of the World [2 nd Edition]. Johns Hopkins University Press; Baltimore, MD.Google Scholar
  45. Noll F. 1997. Foraging behavior on carcasses in the necrophagic bee Trigona hypogea (Hymenoptera: Apidae). J. Insect Behav. 10: 463-467Google Scholar
  46. Noll F.B., Zucchi R., Jorge J.A. and Mateus S. 1996. Food collection and maturation in the necrophagous stingless bee, Trigona hypogea (Hymenoptera: Meliponinae). J. Kansas Entomol. Soc. Suppl. 69: 287-293Google Scholar
  47. Ohl M. and Bleidorn C. 2006. The phylogenetic position of the enigmatic wasp family Heterogynaidae based on molecular data, with description of a new, nocturnal species (Hymenoptera: Apoidea). Syst. Entomol. 31: 321-337Google Scholar
  48. Ohl M. and Engel M.S. 2007. Die Fossilgeschichte der Bienen und ihrer nächsten Verwandten (Hymenoptera: Apoidea). Denisia 20: 687-700Google Scholar
  49. Oliveira F.F. 2002. The mesotibial spur in stingless bees: A new character for the systematics of Meliponini (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 75: 194-202Google Scholar
  50. Perna A., Jost C., Couturier E., Valverde S., Douady S. and Theraulaz G. 2008. The structure of gallery networks in nests of termite Cubitermes spp. revealed by x-ray tomography. Naturwissenschaften 95: 877-884Google Scholar
  51. Pohl H., Wipfler B., Grimaldi D., Beckmann F. and Beutel R.G. 2010. Reconstructing the anatomy of the 42-million-year-old fossil †Mengea tertiaria (Insecta, Strepsiptera). Naturwissenschaften 97: 855-859Google Scholar
  52. Rasmussen C. and Cameron S.A. 2010. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol. J. Linn. Soc. 99: 206-232Google Scholar
  53. Roubik D.W. 1982. Obligate necrophagy in a social bee. Science 217: 1059-1060Google Scholar
  54. Roubik D.W. 1989. Ecology and Natural History of Tropical Bees. Cambridge University Press, New York.Google Scholar
  55. Rozen J.G. Jr 1996. A new species of the bee Heterosarus from Dominican amber (Hymenoptera: Andrenidae; Panurginae). J. Kansas Entomol. Soc. Suppl. 69: 346-352 Google Scholar
  56. Schlüter T. and Stürmer W. 1982. X-ray examination of fossil insects in Cretaceous amber of N.W.-France. Ann. Soc. Entomol. France 18: 527-529Google Scholar
  57. Serrão J.E. 2001. A comparative study of the proventricular structure in corbiculate Apinae (Hymenoptera, Apidae). Micron 32: 379-385Google Scholar
  58. Serrão J.E. 2005. Proventricular structure in solitary bees (Hymenoptera: Apoidea). Organisms, Diversity & Evolution 5: 125-133Google Scholar
  59. Soltis D.E., Senters A.E., Zanis M.J., Kim S., Thompson J.D., Soltis P.S., Ronse de Craene L., Endress P.K. and Farris J.S. 2003. Gunnerales are sister to other core eudicots, and exhibit floral features of early-diverging eudicots. Am. J. Bot. 90: 461-470Google Scholar
  60. Soltis D.E., Soltis P.S., Endress P.K. and Chase M.W. 2005. Phylogeny and Evolution of Angiosperms. Sunderland Sinauer Associates, MA.Google Scholar
  61. Tafforeau P., Boistel R., Boller E., Bravin A., Brunet M., Chaimanee Y., Cloetens P., Feist M., Hoszowska J., Jaeger J.J., Kay R.F., Lazzari V., Marivaux L., Nel A., Nemoz C., Thibault X., Vignaud P. and Zabler S. 2006. Applications of X-ray synchrotron microtomography for non destructive 3D studies of paleontological specimens. Applied Physics A 83: 195-202Google Scholar
  62. Thorp R.W. 1979. Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Annals Missouri Bot. Gard. 66: 788-812Google Scholar
  63. Tollner E.W. 1991. X-ray computerised tomography applications in soil ecology. Agriculture, Ecosystems and Environment 34: 251-260Google Scholar
  64. Velthuis H.H.W. and Gerling D. 1983. At the brink of sociality: Interactions between adults of the carpenter bee Xylocopa pubescens Spinola. Behav. Ecol. Sociobiol. 12: 209-214Google Scholar
  65. Wille A. and Chandler L.C. 1964. A new stingless bee from the Tertiary amber of the Dominican Republic (Hymenoptera; Meliponini). Rev. Biol. Trop. 12: 187-195Google Scholar
  66. Wirkner C.S. and Richter S. 2004. Improvement of microanatomical research by combining corrosion cast with MicroCT and 3D reconstruction, exemplified in the circulatory organs of the woodlouse. Micr. Res. Techn. 64: 250-254Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2011

Authors and Affiliations

  • M. K. Greco
    • 1
    • 2
  • P. M. Welz
    • 4
  • M. Siegrist
    • 5
  • S. J. Ferguson
    • 4
  • P. Gallmann
    • 3
  • D. W. Roubik
    • 6
  • M. S. Engel
    • 7
    • 8
  1. 1.INVERT Group, Department of Electrical and Electronic EngineeringUniversity of BathBathUK
  2. 2.Departement für Klinische VeterinärmedizinVetsuisse-Fakultät, Universität BernBernSwitzerland
  3. 3.Swiss Bee Research CentreAgroscope Liebefeld-Posieux Research Station (ALP)BernSwitzerland
  4. 4.Institute for Surgical Technology and BiomechanicsUniversity of BernBernSwitzerland
  5. 5.Bone Biology Group, Department of Clinical ResearchUniversity of BernBernSwitzerland
  6. 6.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  7. 7.Division of Entomology (Paleoentomology), Natural History Museum, Department of Ecology & Evolutionary BiologyUniversity of KansasLawrenceUSA
  8. 8.Division of Invertebrate Zoology (Entomology)American Museum of Natural HistoryNew YorkUSA

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