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Apidologie

, Volume 45, Issue 6, pp 653–663 | Cite as

Distinguishing feral and managed honeybees (Apis mellifera) using stable carbon isotopes

  • Lucy M. Anderson
  • Travis M. Dynes
  • Jennifer A. Berry
  • Keith S. Delaplane
  • Lydia L. McCormick
  • Berry J. Brosi
Original article

Abstract

The ability to distinguish feral and managed honeybees (Apis mellifera) has applications in studies of population genetics, parasite transmission, pollination, interspecific interactions, and bee breeding. We evaluated a diagnostic test based on theoretical differences in stable carbon isotope ratios generated by supplemental feeding. We evaluated (1) if carbon isotope ratios can distinguish feral and managed honeybees and (2) the temporal persistence of the signal after discontinuation of supplemental feeding. We compared carbon isotope ratios from four types of experimental colonies: feral, managed with and without supplemental feed, and managed with 13C-labeled glucose added to supplemental feed. There was a significant difference between the isotopic signatures of colonies receiving supplemental feed and unfed feral colonies. This difference, however, only persisted for a few weeks after supplemental feeding was discontinued, suggesting that this method may work best under a narrow range of conditions. This work highlights the potential for exploiting temporal turnover of carbon in bee tissues as a tool for studying nutrient flow in honeybee colonies.

Keywords

feral honeybees stable isotopes carbon photosynthesis pathways isotopic fractionation 

Notes

Acknowledgments

We thank B. Nolan, P. Quinn, and N. Weaver for their contributions to the apiary management and B. Tran, E. Lake, and D. Gruenewald for their assistance in pinning bees in the lab. H. Briggs, E. Dobbs, D. Tarpy, and two anonymous reviewers provided constructive comments on the manuscript. B. Ryan and D. Barr both provided helpful discussion on analytic chemistry and the use of a microbalance. We are grateful to the Chattahoochee-Oconee National Forest for permission to collect feral swarms. This work was funded by the US Department of Agriculture (NIFA 2011-67013-30131 to BJB, KSD, and J. De Roode), the US National Institutes of Health (R01-109501-01, part of the joint NIH-NSF-USDA Ecology and Evolution of Infectious Diseases program, to J. De Roode, BJB, and KSD), Emory University (Scholarly Inquiry and Research at Emory grants and the James G. Lester Environmental Studies Research Grant, both to LMA), and the North American Pollinator Protection Campaign (Honey Bee Health Grant to BJB, KSD, and LLM).

References

  1. Bates, D. Maechler, M., Bolker, B. (2011). lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4. Accessed March 2013
  2. Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H., White, J.S. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135PubMedCrossRefGoogle Scholar
  3. Brosi, A.R., Harkins, W.D. (1937) The abundance ratio of the isotopes in natural or isotopically separated carbon. Phys. Rev. 52, 472–474CrossRefGoogle Scholar
  4. Brosi, B.J., Daily, G.C., Chamberlain, C.P., Mills, M. (2009) Detecting changes in habitat-scale bee foraging in a tropical fragmented landscape using stable isotopes. Forest Ecol. Manag. 258, 1846–1855CrossRefGoogle Scholar
  5. Craig, H. (1957) Isotopic standards for mass spectrometric analysis of carbon dioxide. Geochim. Cosmochim. Acta. 12, 113–140Google Scholar
  6. Daniele, G., Wytrychowski, M., Batteau, M., Guibert, S., Casabianca, H. (2011) Stable isotope ratio measurements of royal jelly samples for controlling production procedures: impact of sugar feeding. Rapid Commun. Mass Spectrom. 25, 1929–1932PubMedCrossRefGoogle Scholar
  7. Doner, L.W., White, J.W. (1977) Carbon-13/Carbon-12 ratio is relatively uniform among honeys. Science 197, 891–892PubMedCrossRefGoogle Scholar
  8. Elflein, L., Raezke, K. (2008) Improved detection of honey adulteration by measuring differences between 13C/12C stable carbon isotope ratios of protein and sugar compounds with a combination of elemental analyzer-isotope ratio mass spectrometry and liquid chromatography-isotope ratio mass spectrometry (δ13 C-EA/LC-IRMS). Apidologie 39, 574–587CrossRefGoogle Scholar
  9. Farquhar, G.D., Ehleringer, J.R., Hubick, K.T. (1989) Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Phys. 40, 503–537CrossRefGoogle Scholar
  10. Graham, J.M. (1992) The Hive and the Honey Bee. Dadant & Sons, HamiltonGoogle Scholar
  11. Hobson, K.A. (1999) Tracing origins and migration of wildflower using stable isotopes: a review. Oecologia 120, 314–326CrossRefGoogle Scholar
  12. Hothorn, T., Bretz, F., Westfall, P. (2008) Simultaneous Inference in General Parametric Models. Biom. J. 50(3), 346–363PubMedCrossRefGoogle Scholar
  13. Kelly, J.F. (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 78, 1–27CrossRefGoogle Scholar
  14. Kennedy, B.P., Folt, C.L., Blum, J.D., Chamberlain, C.P. (1997) Natural isotopic markers in salmon. Nature 387, 766–767CrossRefGoogle Scholar
  15. Koziet, J., Rossmann, A., Martin, G.J., Ashurst, P.R. (1993) Determination of carbon-13 content of sugars of fruit and vegetable juices: A European inter-laboratory comparison. Anal. Chim. Acta 271, 31–38CrossRefGoogle Scholar
  16. Martin, S.J., Highfield, A.C., Bretell, L., Villalobos, E.M., Buge, G.E., Powell, M., Nikaido, S., Schroeder, D.C. (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306PubMedCrossRefGoogle Scholar
  17. O’Brien, D.M., Schrag, D.P., del-Rio, C.M. (2000) Allocation to reproduction in a hawkmoth: a quantitative analysis using stable carbon isotopes. Ecology 81, 2822–2831CrossRefGoogle Scholar
  18. Oldroyd, B.P. (2007) What’s killing American honey Bees? PLoS Biol 5, 1195–1199CrossRefGoogle Scholar
  19. Ostrom, P.H., Colunga-Garcia, M., Gage, S.H. (1997) Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence. Oecologia 109, 108–113CrossRefGoogle Scholar
  20. Overmyer, J.P., MacNeil, M.A., Fisk, A.T. (2008) Fractionation and metabolic turnover of carbon and nitrogen stable isotopes in black fly larvae. Rapid Commun. Mass Spectrom. 22, 694–700PubMedCrossRefGoogle Scholar
  21. Oxley, P., Spivak, M., Oldroyd, B. (2010) Six quantitative trait loci influence task thresholds for hygienic behavior in honeybees (Apis mellifera). Mol. Ecol. 19, 1452–1461PubMedCrossRefGoogle Scholar
  22. Peterson, B.J., Fry, B. (1987) Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18, 293–320CrossRefGoogle Scholar
  23. Phillips, D.L. (2001) Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia 127, 166–170PubMedCrossRefGoogle Scholar
  24. Potts, S.G., Beismeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E. (2010) Global pollinator declines: trends, impacts, and drivers. Trends Ecol. Evol. 25, 345–353PubMedCrossRefGoogle Scholar
  25. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/. Accessed March 2013
  26. Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119PubMedCrossRefGoogle Scholar
  27. Sakagami, S.F. (1953) Untersuchungen ber die Arbeitsteilung in einem Zwergvolk der Honigbiene. Beitr ge zue Biologie des Bienenvolkes, Apis mellifera L. I. Jap. J. Zool. 11, 117–185Google Scholar
  28. Schmidt, J. (1994) Attraction of reproductive honey-bee swarms to artificial nests by Nasonov pheromone. J. Chem. Ecol. 20, 1053–1056PubMedCrossRefGoogle Scholar
  29. Seeley, T.D. (2007) Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38, 19–29CrossRefGoogle Scholar
  30. Spivak, M., Mader, E., Vaughan, M., Euliss Jr., N.H. (2011) The plight of the bees. Environ. Sci. & Technol. 45, 1–34CrossRefGoogle Scholar
  31. Venables, W.N., Ripley, B.D. (2002) Modern Applied Statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  32. Winston, M.L., Fergusson, L.A. (1985) The effect of worker loss on temporal caste structure in colonies of the honey bee (Apis mellifera L.). Can. J. Zool. 63, 777–780CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France 2014

Authors and Affiliations

  • Lucy M. Anderson
    • 1
  • Travis M. Dynes
    • 1
  • Jennifer A. Berry
    • 2
  • Keith S. Delaplane
    • 2
  • Lydia L. McCormick
    • 1
  • Berry J. Brosi
    • 1
  1. 1.Department of Environmental StudiesEmory UniversityAtlantaUSA
  2. 2.Department of EntomologyUniversity of GeorgiaAthensUSA

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