Letter

Widespread exploitation of the honeybee by early Neolithic farmers

  • Nature volume 527, pages 226230 (12 November 2015)
  • doi:10.1038/nature15757
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Abstract

The pressures on honeybee (Apis mellifera) populations, resulting from threats by modern pesticides, parasites, predators and diseases, have raised awareness of the economic importance and critical role this insect plays in agricultural societies across the globe. However, the association of humans with A. mellifera predates post-industrial-revolution agriculture, as evidenced by the widespread presence of ancient Egyptian bee iconography dating to the Old Kingdom (approximately 2400 bc)1. There are also indications of Stone Age people harvesting bee products; for example, honey hunting is interpreted from rock art2 in a prehistoric Holocene context and a beeswax find in a pre-agriculturalist site3. However, when and where the regular association of A. mellifera with agriculturalists emerged is unknown4. One of the major products of A. mellifera is beeswax, which is composed of a complex suite of lipids including n-alkanes, n-alkanoic acids and fatty acyl wax esters. The composition is highly constant as it is determined genetically through the insect’s biochemistry. Thus, the chemical ‘fingerprint’ of beeswax provides a reliable basis for detecting this commodity in organic residues preserved at archaeological sites, which we now use to trace the exploitation by humans of A. mellifera temporally and spatially. Here we present secure identifications of beeswax in lipid residues preserved in pottery vessels of Neolithic Old World farmers. The geographical range of bee product exploitation is traced in Neolithic Europe, the Near East and North Africa, providing the palaeoecological range of honeybees during prehistory. Temporally, we demonstrate that bee products were exploited continuously, and probably extensively in some regions, at least from the seventh millennium cal bc, likely fulfilling a variety of technological and cultural functions. The close association of A. mellifera with Neolithic farming communities dates to the early onset of agriculture and may provide evidence for the beginnings of a domestication process.

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Acknowledgements

We thank the UK Natural Environment Research Council for partial funding of the mass spectrometry facilities at Bristol (contract no. R8/H10/63; http://www.lsmsf.co.uk) and English Heritage, European Research Council, Leverhulme Trust, Ministère de la Culture et de la Communication, Ministère de l’Enseignement Supérieur et de la Recherche (ACI Jeunes Chercheurs), Natural Environment Research Council, Région PACA, Royal Society and Wellcome Trust for funding.

Author information

Author notes

    • Sigrid Mirabaud
    • , Lucija Šoberl
    •  & Miriam Cubas

    Present addresses: Département des restaurateurs, Institut National du Patrimoine, 124 rue Henri Barbusse, 93300 Aubervilliers, France (S.M.); Laboratório HERCULES, Universidade de Évora, Palácio do Vimioso, Largo Marquês de Marialva 8, 7000-809 Évora, Portugal (L.S.); BioArCh–University of York, York YO10 5DD, UK (M.C).

    • Lydia Zapata-Peña

    Deceased.

Affiliations

  1. Organic Geochemistry Unit, School of Chemistry, University of Bristol, Cantock’s Close, Bristol BS8 1TS, UK

    • Mélanie Roffet-Salque
    • , Richard P. Evershed
    • , Lucy J. E. Cramp
    • , Julie Dunne
    • , Simona Mileto
    • , Mirva Pääkkönen
    • , Jessica Smyth
    • , Lucija Šoberl
    •  & Helen L. Whelton
  2. CEPAM – Cultures et Environnements. Préhistoire, Antiquité, Moyen Âge, UMR 7264, Université Nice Sophia Antipolis – CNRS, 06300 Nice, France

    • Martine Regert
  3. Department of Archaeology, University of Exeter, Laver Building, North Park Road, Exeter, Devon EX4 4QE, UK

    • Alan K. Outram
  4. Department of Archaeology and Anthropology, University of Bristol, 43 Woodland Road, Bristol BS8 1UU, UK

    • Lucy J. E. Cramp
    •  & Jessica Smyth
  5. Université Bordeaux Montaigne, 33607 Pessac, France

    • Orestes Decavallas
  6. Laboratoire du Centre de Recherche et de Restauration des Musées de France (C2RMF), UMR 171, Palais du Louvre, Porte des Lions, 14 Quai François Mitterrand, 75001 Paris, France

    • Orestes Decavallas
    •  & Sigrid Mirabaud
  7. Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK

    • Pascale Gerbault
  8. Department of Anthropology, University College London, London WC1H 0BW, UK

    • Pascale Gerbault
  9. Institut für Prähistorische Archäologie, Freie Universität Berlin, Altensteinstr. 15, Berlin 14195, Germany

    • Simona Mileto
  10. Department of Archaeology, University of Turku, 20014 Turun Yliopisto, Finland

    • Mirva Pääkkönen
    •  & Henrik Asplund
  11. University of Ljubljana, Faculty of Arts, Department of Archaeology, Aškerčeva 2, box 580, 1000 Ljubljana, Slovenia

    • Lucija Šoberl
    •  & Mihael Budja
  12. Department of Geography, Prehistory and Archaeology. University of Basque Country (EHU-UPV), Francisco Tomás y Valiente s/n, 01006 Vitoria-Gasteiz, Spain

    • Alfonso Alday-Ruiz
    •  & Lydia Zapata-Peña
  13. Institute of Prehistory, Adam Mickiewicz University, Umultowska 89d, 61-614 Poznań, Poland

    • Marta Bartkowiak
    •  & Arkadiusz Marciniak
  14. Museum Quintana – Archäologie in Künzing, Partnermuseum der Archäologischen Staatssammlung München, Osterhofener Str. 2, 94550 Künzing, Germany

    • Eva Bayer-Niemeier
  15. Musée Archéologique de Sousse, Rue Marshall Tito, 4000 Sousse, Tunisia

    • Lotfi Belhouchet
  16. Centro Fermi, Museo Storico della Fisica e Centro di Studi e Ricerche Enrico Fermi, 00184 Rome, Italy

    • Federico Bernardini
  17. Multidisciplinary Laboratory, The Abdus Salam International Centre for Theoretical Physics, 34151 Trieste, Italy

    • Federico Bernardini
  18. UCD School of Archaeology, University College Dublin, Dublin 4, Ireland

    • Gabriel Cooney
  19. International Institute for Prehistoric Research of Cantabria, University of Cantabria, Avd de los Castros s/n, 39005 Santander, Spain

    • Miriam Cubas
    •  & Jesus E. González-Urquijo
  20. Department of Archaeology, University College Galway, Galway, Ireland

    • Ed M. Danaher
  21. UNIARQ-Departamento de História, Faculdade de Letras de Lisboa, Universidade de Lisboa, 1600-214 Lisboa, Portugal

    • Mariana Diniz
  22. István Dobó Castle Museum, Vár út 1, 3300 Eger, Hungary

    • László Domboróczki
  23. Dipartimento Civiltà e Forme del Sapere, Università di Pisa, Via Galvani 1, 56126 Pisa, Italy

    • Cristina Fabbri
    •  & Giovanna Radi
  24. CNRS – UMR 5608 – TRACES, Maison de la recherche, Université Toulouse Jean Jaurès, 5 Allée Antonio Machado, 31058 Toulouse cedex 9, France

    • Jean Guilaine
    •  & Claire Manen
  25. CNRPAH, Centre National de Recherche Préhistorique, Anthropologique et Historique, Algiers, Algeria

    • Slimane Hachi
    •  & Farid Kherbouche
  26. School of Geography, Archaeology and Palaeoecology, Queen’s University Belfast, Belfast BT7 1NN, UK

    • Barrie N. Hartwell
    •  & James P. Mallory
  27. Universität Hamburg, Archäologisches Institut, Edmund-Siemers-Allee 1, Flügel West, 20146 Hamburg, Germany

    • Daniela Hofmann
  28. a.r.t.e.s. Graduate School for the Humanities Cologne, Graduiertenschule der Philosophischen Fakultät, Aachener Str. 217, 50931 Cologne, Germany

    • Isabel Hohle
  29. IMF-CSIC, Egipciacas 15, 08001 Barcelona, Spain

    • Juan J. Ibáñez
  30. Istanbul University, Faculty of Letters, Department of Prehistory, 34434 Laleli Istanbul, Turkey

    • Necmi Karul
    •  & Mehmet Özdoğan
  31. Eachtra Archaeological Projects, Lickybeg, Clashmore, County Waterford, Ireland

    • Jacinta Kiely
  32. School of History and Archaeology, Faculty of Philosophy, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece

    • Kostas Kotsakis
  33. German Archaeological Institute, Podbielskiallee 69-71, 14 195 Berlin, Germany

    • Friedrich Lueth
  34. Musée Rolin, 3 rue des Bancs, 71400 Autun, France

    • Brigitte Maurice-Chabard
  35. John Cronin & Associates, 28 Upper Main Street, Buncrana, County Donegal, Ireland

    • Martin A. Mc Gonigle
  36. Aix-Marseille Université, CNRS, Ministère de la Culture et de la Communication, UMR 7269 LAMPEA, LabexMed, 13284 Marseille, France

    • Simone Mulazzani
  37. Dipartimento di Biologia Ambientale, Università degli Studi di Roma La Sapienza, Rome 00185, Italy

    • Simone Mulazzani
  38. Institute of Archaeology Belgrade, Kneza Mihaila 35/4 11000 Belgrade, Serbia

    • Olga S. Perić
    •  & Slaviša R. Perić
  39. Eberhard-Karls-Universität Tübingen, Institut für Ur- und Frühgeschichte und Archäologie des Mittelalters - Abt. Jüngere Urgeschichte und Frühgeschichte - Schloß Hohentübingen, 72070 Tübingen, Germany

    • Jörg Petrasch
  40. Maison des Sciences de l’Homme et de l’Environnement C.N. Ledoux, CNRS & Université de Franche-Comté, 32 rue Mégevand, 25030 Besançon Cedex, France

    • Anne-Marie Pétrequin
    •  & Pierre Pétrequin
  41. Kämpfenstr. 20, 78315 Radolfzell, Germany

    • Ulrike Poensgen
  42. Department of Archaeology, Faculty of Humanities, University of Southampton, Avenue Campus, Highfield, Southampton SO17 1BF, UK

    • C. Joshua Pollard
  43. Muséum National d’Histoire Naturelle, 55 rue de Buffon, 75005 Paris, France

    • François Poplin
  44. Department of Pre- and Protohistory, University of Vienna, 1190 Vienna, Austria

    • Peter Stadler
  45. Landesamt für Archaeologie, Zur Wetterwarte 7, 01109 Dresden, Germany

    • Harald Stäuble
  46. Department of Archaeology, Faculty of Philosophy, Belgrade University, 18–20 Čika Ljubina Street, 11000 Belgrade, Serbia

    • Nenad Tasić
    •  & Jasna B. Vuković
  47. Department of History and Ethnology, Democritus University of Thrace, Komotini, Greece

    • Dushka Urem-Kotsou
  48. Irish Archaeological Consultancy, Unit G1, Network Enterprise Park, Kilcoole, County Wicklow, Ireland

    • Fintan Walsh
  49. Department of Archaeology and Conservation, Cardiff University, John Percival Building, Colum Drive, Cardiff CF10 3EU, UK

    • Alasdair Whittle
  50. State Museum of Archaeology Chemnitz, Stefan-Heym-Platz 1, 09111 Chemnitz, Germany

    • Sabine Wolfram
  51. Institut National du Patrimoine de Tunis - Musée archéologique de Carthage, Carthage, Tunisia

    • Jamel Zoughlami

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Contributions

M.R.-S., M.R., R.P.E. and A.K.O. conceived and planned the project about beeswax in prehistory. M.R.-S., M.R. and R.P.E. wrote the paper. M.R.-S., M.R., L.J.E.C., O.D., J.D., S.Mil., S.Mir., M.P., J.S., L.S., H.L.W., M.Bart. and D.U.-K. undertook planning of regional lipid residue analyses projects, sampling, analytical work and data analysis. P.G. created Figure 4 and Supplementary Information section 3. All other authors either directed excavations or provided expertise in relation to pottery collections and essential insights into the study region and sites.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Mélanie Roffet-Salque or Martine Regert or Richard P. Evershed.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Information sections 1-3. Section 1 contains a table showing Neolithic sites from which sherds were analysed with summary of results of lipid residue analyses. Mesolithic sites were added where available. Section 2 contains a table showing archaeological contexts for sherds containing beeswax. Section 3 contains statistical analysis of the lipid residue dataset.

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