Abstract
Honey bees communicate to nestmates locations of resources, including food, water, tree resin and nest sites, by making waggle dances. Dances are composed of repeated waggle runs, which encode the distance and direction vector from the hive or swarm to the resource. Distance is encoded in the duration of the waggle run, and direction is encoded in the angle of the dancer’s body relative to vertical. Glass-walled observation hives enable researchers to observe or video, and decode waggle runs. However, variation in these signals makes it impossible to determine exact locations advertised. We present a Bayesian duration to distance calibration curve using Markov Chain Monte Carlo simulations that allows us to quantify how accurately distance to a food resource can be predicted from waggle run durations within a single dance. An angular calibration shows that angular precision does not change over distance, resulting in spatial scatter proportional to distance. We demonstrate how to combine distance and direction to produce a spatial probability distribution of the resource location advertised by the dance. Finally, we show how to map honey bee foraging and discuss how our approach can be integrated with Geographic Information Systems to better understand honey bee foraging ecology.
Similar content being viewed by others
References
Aizen M, Harder L (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19(11):915–918. doi:10.1016/j.cub.2009.03.071
Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. http://CRAN.R-project.org/package=lme4, r package version 0.999999-2
Beekman M, Ratnieks FLW (2000) Long-range foraging by the honey-bee, Apis mellifera L. Funct Ecol 14(4):490–496. doi:10.1046/j.1365-2435.2000.00443.x
Beekman M, Sumpter DJT, Seraphides N, Ratnieks FLW (2004) Comparing foraging behaviour of small and large honey-bee colonies by decoding waggle dances made by foragers. Funct Ecol 18(6):829–835. doi:10.1111/j.0269-8463.2004.00924.x
Biesmeijer JC, Slaa EJ (2006) The structure of eusocial bee assemblages in Brazil. Apidologie 37(2):240–258. doi:10.1051/apido:2006014
Boch R (1957) Rassenmässige Unterschiede bei den Tänzen der Honigbiene (Apis mellifica L.). Z vergl Physiol 40(3):289–320. doi:10.1007/BF00340572
Burnham K, Anderson D, Huyvaert K (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. doi:10.1007/s00265-010-1029-6
Carreck NL (2008) Are honey bees (Apis mellifera L.) native to the British Isles? J Apic Res 47(4):318. doi:10.3896/IBRA.1.47.4.15
Chittka L, Dornhaus A (1999) Comparisons in physiology and evolution, and why bees can do the things they do. Ciencia al Dia Int 2:1–17. http://www.ciencia.cl/CienciaAlDia/volumen2/numero2/articulos/articulo5-eng.html
Couvillon M (2012) The dance legacy of Karl von Frisch. Insect Soc 59(3):297–306. doi:10.1007/s00040-012-0224-z
Couvillon MJ, Phillipps HLF, Schürch R, Ratnieks FLW (2012a) Working against gravity: horizontal honeybee waggle runs have greater angular scatter than vertical waggle runs. Biol Lett 8(4):540–543. doi:10.1098/rsbl.2012.0182
Couvillon MJ, Riddell Pearce FC, Harris-Jones EL, Kuepfer AM, Mackenzie-Smith SJ, Rozario LA, Schürch R, Ratnieks FLW (2012b) Intra-dance variation among waggle runs and the design of efficient protocols for honey bee dance decoding. Biol Open 1(5):467–472. doi:10.1242/bio.20121099
Dacke M, Srinivasan MV (2008) Two odometers in honeybees? J Exp Biol 211:3281–3286. doi:10.1242/jeb.021022
De Marco RJ, Gurevitz JM, Menzel R (2008) Variability in the encoding of spatial information by dancing bees. J Exp Biol 211(10):1635–1644. doi:10.1242/jeb.013425
Duong N, Schneider SS (2008) Intra-patriline variability in the performance of the vibration signal and waggle dance in the honey bee, Apis mellifera. Ethology 114:646–55. doi: 10.1111/j.1439-0310.2008.01504.x
Dyer FC (2002) The biology of the dance language. Annu Rev Entomol 47(1):917–949. doi:10.1146/annurev.ento.47.091201.145306
Eckert JE (1933) The flight range of the honeybee. J Agric Res 47:257–285
Eisenhart C (1939) The interpretation of certain regression methods and their use in biological and industrial research. Ann Math Stat 10(2):162–186. http://www.jstor.org/stable/2235694
Esch HE, Zhang S, Srinivasan MV, Tautz J (2001) Honeybee dances communicate distances measured by optic flow. Nature 411(6837):581–583. doi:10.1038/35079072
Gardner KE, Seeley TD, Calderone NW (2008) Do honeybees have two discrete dances to advertise food sources? Anim Behav 75(4):1291–1300. doi:10.1016/j.anbehav.2007.09.032
Grüter C, Ratnieks FL (2011) Honeybee foragers increase the use of waggle dance information when private information becomes unrewarding. Anim Behav 81(5):949–954. doi:10.1016/j.anbehav.2011.01.014
Grüter C, Balbuena MS, Farina WM (2008) Informational conflicts created by the waggle dance. Proc R Soc B 275(1640):1321–1327. doi:10.1098/rspb.2008.0186
Hamada M, Pohl A, Spiegelman C, Wendelberger J (2003) A Bayesian approach to calibration intervals and properly calibrated tolerance intervals. J Qual Technol 35(2):194–205
Hijmans RJ, van Etten J (2013) raster: geographic data analysis and modeling. http://CRAN.R-project.org/package=raster, r package version 2.1-25
Jammalamadaka SR, SenGupta A (2001) Topics in directional statistics. Series on multivariate statistics 5. World Scientific, Singapore
Landes R, Loutzenhiser P, Vardeman SB (2006) Hierarchical Bayesian statistical analysis for a calibration experiment. IEEE Trans Instrum Meas 55(6):2165–2171. doi:10.1109/TIM.2006.884128
Tan K., Yang M.Radloff S. Hepburn H. Zhang Z. Luo L, Li, H (2008) Dancing to different tunes: heterospecific deciphering of the honeybee waggle dance. Naturwissenschaften 95:1165–1168. doi:10.1007/s00114-008-0437-1
Lindauer M (1955) Schwarmbienen auf Wohnungssuche. Z vergl Physiol 37(4):263–324. doi:10.1007/BF00303153
Lund U, Agostinelli C (2012) Circstats: circular statistics, from “topics in circular statistics” (2001). http://CRAN.R-project.org/package=CircStats, r package version 0.2-4
Mardia KV (1975) Statistics of directional data. J R Stat Soc B 37(3):349–393
Ng KH, Pooi AH (2008) Calibration intervals in linear regression models. Commun Stat Theory Methods 37(11):1688–1696. doi:10.1080/03610920701826120
Plummer M (2003) JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. In: Proceedings of the 3rd international workshop on distributed statistical computing (DSC 2003), pp 20–22
Plummer M (2013) rjags: Bayesian graphical models using MCMC. http://CRAN.R-project.org/package=rjags, r package version 3-10
R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/, ISBN 3-900051-07-0
Ribbands CR (1953) The behaviour and social life of honeybees. Bee Research Association Limited
Gelman A, Carlin JB, Stern HS, Rubin, DB (2003) Bayesian data analysis. 2nd edn. Chapman and Hall/CRC Texts in Statistical Science. Chapman and Hall/CRC
Schneider SS (1989) Spatial foraging patterns of the African honey bee, Apis mellifera scutellata. J Insect Behav 2(4):505–521. doi:10.1007/BF01053351
Schürch R, Couvillon M (2013) Too much noise on the dance floor: intra- and inter-dance angular error in honey bee waggle dances. Commun Integr Biol 6:1–3. doi:10.4161/cib.22298
Schweiger EM (1958) Über individuelle Unterschiede in der Entfernungs-und Richtungsangabe bei den Tänzen der Bienen. Z vergl Physiol 41(3):272–299. doi:10.1007/BF00365323
Seeley TD (1994) Honey bee foragers as sensory units of their colonies. Behav Ecol Sociobiol 34(1):51–62. doi:10.1007/BF00175458
Seeley T (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge
Seeley TD, Towne WF (1992) Tactics of dance choice in honey bees: do foragers compare dances? Behav Ecol Sociobiol 30:59–69. doi:10.1007/BF00168595
Seeley TD, Mikheyev AS, Pagano GJ (2000) Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability. J Comp Physiol A 186(9):813–819. doi:10.1007/s003590000134
Srinivasan MV, Zhang S, Altwein M, Tautz J (2000) Honeybee navigation: nature and calibration of the “odometer”. Science 287(5454):851–853. doi:10.1126/science.287.5454.851
Steche W (1957) Beiträge zur Analyse der Bienentänze (Teil I). Insect Soc 4(3):305–318. doi:10.1007/BF02222160
Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc R Soc B 270(1515):569–575. doi:10.1098/rspb.2002.2292
Tanner DA, Visscher K (2006) Do honey bees tune error in their dances in nectar-foraging and house-hunting? Behav Ecol Sociobiol 59(4):571–576. doi:10.1007/s00265-005-0082-z
Tanner D, Visscher P (2008) Do honey bees average directions in the waggle dance to determine a flight direction? Behav Ecol Sociobiol 62:1891–1898. doi:10.1007/s00265-008-0619-z
Tanner D, Visscher K (2009) Does the body orientation of waggle dance followers affect the accuracy of recruitment? Apidologie 40(1):55–62. doi:10.1051/apido:2008074
Towne WF, Gould JL (1988) The spatial precision of the honey bees’ dance communication. J Insect Behav 1(2):129–155. doi:10.1007/BF01052234
Visscher PK, Seeley TD (1982) Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63(6):1790–1801. doi:10.2307/1940121
von Frisch K (1946) Die Tänze der Bienen. Österr zool Z 1:1–148
von Frisch K (1967) The dance language and orientation of bees. Harvard University Press, Cambridge
von Frisch K, Jander R (1957) Über den Schwänzeltanz der Bienen. Z vergl Physiol 40:239–263. doi:10.1007/BF00340570
von Frisch K, Lindauer M (1961) Über die “Mißweisung” bei den richtungsweisenden Tänzen der Bienen. Naturwissenschaften 48:585–594. doi:10.1007/BF00601984
Waddington KD, Herbert TJ, Visscher PK, Richter MR (1994) Comparisons of forager distributions from matched honey bee colonies in suburban environments. Behav Ecol Sociobiol 35(6):423–429. doi:10.1007/BF00165845
Wang N, Lin X, Guttierrez RG (1999) A bias correction regression calibration approach in generalized linear mixed measurement error models. Commun Stat Theory Methods 28(1):217–232. doi:10.1080/03610929908832292
Wenner AM (1962) Sound production during the waggle dance of the honey bee. Anim Behav 10(1–2):79–95. doi:10.1016/0003-3472(62)90135-5
Acknowledgments
We thank Christoph Grüter for calibration videos, materials used in the data collection, and fruitful discussions, and Dik Heg for comments on earlier drafts of the manuscript. We also thank two anonymous reviewers for their helpful inputs. RS is funded by the Swiss National Science Foundation (Grant PA00P3_139731) and MJC is funded by the Nineveh Charitable Trust. Additional research funding was provided by Waitrose Ltd., Burt’s Bees, and the Body Shop Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schürch, R., Couvillon, M.J., Burns, D.D.R. et al. Incorporating variability in honey bee waggle dance decoding improves the mapping of communicated resource locations. J Comp Physiol A 199, 1143–1152 (2013). https://doi.org/10.1007/s00359-013-0860-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-013-0860-4