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Apidologie

, Volume 50, Issue 4, pp 454–462 | Cite as

The effect of conspecific cues on honey bee foraging behavior

  • Eva S. Horna LowellEmail author
  • Julie A. Morris
  • Mayra C. Vidal
  • Catherine S. Durso
  • Shannon M. Murphy
Original article

Abstract

Foraging honey bees (Apis mellifera) seem to use the presence of conspecific foragers as cues for flower quality. However, there is disagreement regarding how a conspecific cue is perceived by other foragers (enhancement or inhibition). Most studies manipulate the total number of bees foraging in an arena or the presence or absence of a bee on a flower and then observe the behavior of one forager in response to a single conspecific, which does not reflect natural foraging. We tested how a range of conspecifics on flowers affected on which flowers foraging honey bees landed. We trained students from a biology class for non-STEM majors to collect data and tested whether the number of conspecifics on flowers influences on which flower foragers land. We found that foragers land more frequently on flowers occupied by more conspecifics, which supports the hypothesis that conspecifics are cues for local enhancement. Our results increase our understanding of how honey bees forage once at a flower patch.

Keywords

foraging behavior honey bee Apis mellifera floral resource social cue 

Notes

Acknowledgments

We thank the students from the “Sustaining Life” undergraduate class at the University of Denver for helping to collect data and the teaching assistants from all the lab sections of the course who helped the students run the experiment (Faith Lierheimer, Lisa Clark, Claudia Hallagan, and lab director, Angie Hebel). We thank the Murphy lab, the University of Denver Ecology and Evolutionary Biology (DUEEB) group, and Amy Toth for helpful suggestions on earlier versions that greatly improved our manuscript.

Authors’ contributions

ESHL and SM conceived the project and designed the experiment. ESHL, SM, and JM trained students to perform the experiment. ESHL, SM, JM, and MV performed data collection. CD and MV performed statistical analysis. ESHL wrote the first draft of the paper, and all authors helped write sections of the paper or contributed substantially to revisions. All authors have read and approved the final version of this paper.

Funding information

We thank the University of Denver Undergraduate Research Center for funding our research with an award to ESHL.

Supplementary material

13592_2019_657_Fig3_ESM.png (22 kb)
Supplementary Fig. 3

The amount of sugar water left in Eppendorf tubes after leaving a small array of 8 fake flowers outside for 0.5, 1, 1.5, 2, 3, and 4 minutes. The red dotted-line marks 1.75 mL and any points below this line represent an amount of sugar water in the tube for which the honeybees had to compete for access to sugar water resource. (PNG 22.0 kb)

13592_2019_657_MOESM1_ESM.tif (167 kb)
ESM 1 (TIFF 167 kb)
13592_2019_657_Fig4_ESM.png (270 kb)
Supplementary Fig. 4

The two principal components (PCA1 and PCA2) that summarize our climatic variables, which were percent cloud cover, percent humidity, temperature, and time of day. The figure on the left shows the eigenvalues for each individual data point we collected of our climatic variables, and the figure on right shows the average eigenvalues for each of our climatic variables. (PNG 270 kb)

13592_2019_657_MOESM2_ESM.tif (1.3 mb)
ESM 2 (TIFF 1.33 mb)
13592_2019_657_Fig5_ESM.png (42 kb)
Supplementary Fig. 5

Result from generalized additive models showing a linear relationship for the smooth term # of bees recruited as a function of the initial # of bees on the flowers. (PNG 41.8 kb)

13592_2019_657_MOESM3_ESM.tif (145 kb)
ESM 3 (TIFF 144 kb)

References

  1. Auchincloss, L.C., Laursen, S.L., Branchaw, J.L., Eagan, K., Graham, M., et al. (2014) Assessment of course-based undergraduate research experiences: Ameeting report. CBE Life Sci. Educ., 13, 29–40.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Avarguès-Weber, A. & Chittka, L. (2014) Local enhancement or stimulus enhancement? Bumblebee social learning results in a specific pattern of flower preference. Anim. Behav., 97, 185–191.CrossRefGoogle Scholar
  3. Ballen, C.J., Blum, J.E., Brownell, S., Hebert, S., Hewlett, J., et al (2017) A call to develop course-based undergraduate research experiences (CUREs) for Nonmajors courses. CBE Life Sci. Educ., 16, 1–7.Google Scholar
  4. Bangera, G. & Brownell, S.E. (2014) Course-based undergraduate research experiences can make scientific research more inclusive. CBE Life Sci. Educ., 13, 602–606.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bates, D., Machler, M., Bolker, B. & Walkter, S. (2015) Fitting linear mixed-effects models using lme4. J. Stat. Softw., 1–48.Google Scholar
  6. Beekman, M. & Ratnieks, F.L.W. (2000) Long-range foraging by the honey-bee, Apis mellifera L. Funct. Ecol., 14, 490–496.CrossRefGoogle Scholar
  7. Bolnick, D. & Preisser, E. (2005) Resource Competition Modifies the Strength of Trait-Mediated Predator-Prey Interactions: A Meta Analysis. Ecology, 86, 2771–2779.CrossRefGoogle Scholar
  8. Calderone, N.W. (2012) Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period 1992-2009. PLoS One, 7, 24–28.CrossRefGoogle Scholar
  9. Dukas, R. (2001) Effects of perceived danger on flower choice by bees. Ecol. Lett., 4, 327–333.CrossRefGoogle Scholar
  10. Ferguson, A.W. & Free, J.B. (1979) Production of a Forage-Marking Pheromone by the Honeybee. J. Apic. Res., 18, 128–135.CrossRefGoogle Scholar
  11. Free, J.B. & Williams, I.H. (1983) Scent-Marking of Flowers by Honeybees. J. Apic. Res., 22, 86–90.CrossRefGoogle Scholar
  12. von Frisch, K. (1967) The Dance Language and Orientation of Bees. The Belknap Press of Harvard University Press, Cambridge.Google Scholar
  13. Horna Lowell, E.S., Morris, J.A., Vidal, M.C., Durso, C.S. & Murphy, S.M. (2019) Data from: The effect of conspecific cues on honey bee foraging behavior. Dyrad Digital Repository.  https://doi.org/10.5061/dryad.3rn48cm.
  14. Howard, S.R., Garcia, J.E., Greentree, A.D. & Dyer, A.G. (2018) Numerical ordering of zero in honey bees. Science (80-. )., 360, 1124–1126.CrossRefGoogle Scholar
  15. Kalmus, H. (1954) The clustering of honeybees at a food source. Br. J. Anim. Behav., 2, 63–71.CrossRefGoogle Scholar
  16. Kalmus, H. & Ribbands, C.R. (1952) The origin of the odours by which honeybees distinguish their companions. Proc. R. Soc. B Biol. Sci., 140, 50–59.CrossRefGoogle Scholar
  17. Kawaguchi, L.G., Ohashi, K. & Toquenaga, Y. (2006) Do bumble bees save time when choosing novel flowers by following conspecifics? Funct. Ecol., 20, 239–244.CrossRefGoogle Scholar
  18. Murphy, S.M., Battocletti, A.H., Tinghitella, R.M., Wimp, G.M. & Ries, L. (2016) Complex community and evolutionary responses to habitat fragmentation and habitat edges: what can we learn from insect science? Curr. Opin. Insect Sci., 14, 61–65.CrossRefPubMedGoogle Scholar
  19. Pastor, K.A. & Seeley, T.D. (2005) The Brief Piping Signal of the Honey Bee: Begging Call or Stop Signal? Ethology, 111, 775–784.CrossRefGoogle Scholar
  20. Preisser, E.L., Bolnick, D.I. & Benard, M.E. (2005) Scared to Death ? The Effects of Intimidation and Consumption in Predator-Prey Interactions Published by : Ecological Society of America SCARED TO DEATH ? THE EFFECTS OF INTIMIDATION AND CONSUMPTION IN PREDATOR-PREY INTERACTIONS. Ecology, 86, 501–509.CrossRefGoogle Scholar
  21. R Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed June 2018.
  22. Reeve, J.D. & Cronin, J.T. (2010) Edge behaviour in a minute parasitic wasp. J. Anim. Ecol., 79, 483–490.CrossRefPubMedGoogle Scholar
  23. Ribbands, C.R. (1949) The Foraging Method of Individual Honey-Bees. J. Anim. Ecol., 18, 47–66.CrossRefGoogle Scholar
  24. Ries, L., Murphy, S.M., Wimp, G.M. & Fletcher, R.J. Jr (2017) Closing Persistent Gaps in Knowledge About Edge Ecology. Curent Landsc. Ecol. Rep., 2, 30–41.CrossRefGoogle Scholar
  25. Riley, J.R., Greggers, U., Smith, A.D., Reynolds, D.R. & Menzel, R. (2005) The flight paths of honeybees recruited by the waggle dance. Nature, 435, 205–207.CrossRefPubMedGoogle Scholar
  26. Seeley, T.D. (1986) Social foraging by honeybees: how colonies allocate foragers among patches of flowers. Behav. Ecol. Sociobiol., 19, 343–354.CrossRefGoogle Scholar
  27. Seeley, T.D., Camazine, S. & Sneyd, J. (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behav. Ecol. Sociobiol., 28, 277–290.CrossRefGoogle Scholar
  28. Slaa, E.J., Wassenberg, J. & Biesmeijer, J.C. (2003) The use of field-based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees. Ecol. Entomol., 28, 369–379.CrossRefGoogle Scholar
  29. Stout, J.C. & Goulson, D. (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim. Behav., 62, 183–189.CrossRefGoogle Scholar
  30. Sumpter, D. & Pratt, S. (2003) A modelling framework for understanding social insect foraging. Behav. Ecol. Sociobiol., 53, 131–144.Google Scholar
  31. Tautz, J. & Sandeman, D.C. (2003) Recruitment of honeybees to non-scented food sources. J. Comp. Physiol. A, 189, 293–300.Google Scholar
  32. Visscher, P.K. & Seeley, T.D. (1982) Foraging Strategy of Honeybee Colonies in a Temperate Deciduous Forest. Ecology, 63, 1790–1801.CrossRefGoogle Scholar
  33. Wilson, E.O. (1975) Sociobiology: The new Synthesis. In Sociobiology: The New Synthesis. Harvard University Press, Cambridge.Google Scholar
  34. Wood, S.N. (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc. Series B. 73, 3–36.Google Scholar
  35. Yokoi, T. & Fujisaki, K. (2011) To Forage or Not: Responses of Bees to the Presence of Other Bees on Flowers. Ann. Entomol. Soc. Am., 104, 353–357.CrossRefGoogle Scholar
  36. Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009) Mixed effects models and extensions in ecology with R. Springer, Berlin.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of DenverDenverUSA
  2. 2.Department of Biology, 358 Life Sciences ComplexSyracuse UniversitySyracuseUSA
  3. 3.Center for Statistics and VisualizationUniversity of DenverDenverUSA

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