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Journal of Insect Behavior

, Volume 29, Issue 5, pp 557–577 | Cite as

Stop-Signaling Reduces Split Decisions without Impairing Accuracy in the Honeybee Nest-Site Selection Process

  • Teeraphan LaomettachitEmail author
  • Teerasit Termsaithong
  • Anuwat Sae-Tang
  • Orawan Duangphakdee
Article

Abstract

In the honeybee swarm nest-site selection process, individual bees gather information about available candidate sites and communicate the information to other bees. The swarm makes an agreement for a candidate site when the number of bees that supports the site reaches a threshold. This threshold is usually referred to as the quorum threshold and it is shown by many studies as a key parameter that is a compromise between the accuracy and speed of decisions. In the present work, we use a model of the honeybee Apis mellifera nest-site selection process to study how the quorum threshold and discovery time of candidate sites have major impact on two unfavorable situations in selecting a nest site: decision deadlock and decision split. We show that cross-inhibitory stop-signaling, delivered among bees supporting different sites, enables swarms to avoid the decision split problem in addition to avoiding the decision deadlock problem that has been previously proposed. We also show that stop-signaling improves decision speed, but compromises decision accuracy in swarms using high quorum thresholds by causing the swarms to be trapped in local optima (e.g., choosing a sub-optimal option that is encountered first). On the other hand, we demonstrate that stop-signaling can reduce split decisions without compromising decision accuracy in swarms using low quorum thresholds when it is compared to the accuracy of swarms using the same threshold values but not exhibiting stop-signaling. Based on our simulations, we suggest that swarms using low quorum thresholds (as well as swarms with large population sizes) would benefit more from exhibiting the stop-signaling activity than not exhibiting it.

Keywords

Nest-site selection decision split decision deadlock speed-accuracy trade-off local optima stochastic simulation 

Notes

Acknowledgments

The authors acknowledge the High Performance Computing unit, which is supported by Innovative Software and Computing Center at King Mongkut’s University of Technology Thonburi and Thailand’s National E-Science Infrastructure Consortium. We would like to thank the National Research University Project (NRU) of Thailand’s Office of the Higher Education Commission for financial support. We are grateful to Dr. Tomer Czaczkes and another anonymous reviewer for their advice in improving this paper.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10905_2016_9581_MOESM1_ESM.docx (1.8 mb)
ESM 1 (DOCX 1811 kb)

References

  1. Bogacz R, Brown E, Moehlis J, Holmes P, Cohen JD (2006) The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol Rev 113:700–765. doi: 10.1037/0033-295X.113.4.700 CrossRefPubMedGoogle Scholar
  2. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424:388–388. doi: 10.1038/424388a CrossRefPubMedGoogle Scholar
  3. Chittka L, Skorupski P, Raine NE (2009) Speed–accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407. doi: 10.1016/j.tree.2009.02.010 CrossRefPubMedGoogle Scholar
  4. Couzin ID (2009) Collective cognition in animal groups. Trends Cogn Sci 13:36–43. doi: 10.1016/j.tics.2008.10.002 CrossRefPubMedGoogle Scholar
  5. Czaczkes TJ (2014) How to not get stuck—negative feedback due to crowding maintains flexibility in ant foraging. J Theor Biol 360:172–180. doi: 10.1016/j.jtbi.2014.07.005 CrossRefPubMedGoogle Scholar
  6. Czaczkes TJ, Grüter C, Ellis L, Wood E, Ratnieks FLW (2013a) Ant foraging on complex trails: route learning and the role of trail pheromones in Lasius niger. J Exp Biol 216:188–197. doi: 10.1242/jeb.076570 CrossRefPubMedGoogle Scholar
  7. Czaczkes TJ, Grüter C, Ratnieks FLW (2013b) Negative feedback in ants: crowding results in less trail pheromone deposition. J R Soc Interface 10. doi: 10.1098/rsif.2012.1009
  8. Czaczkes TJ, Salmane AK, Klampfleuthner FAM, Heinze J (2016) Private information alone can trigger trapping of ant colonies in local feeding optima. J Exp Biol 219:744–751. doi: 10.1242/jeb.131847 CrossRefPubMedGoogle Scholar
  9. Dyer FC (2002) The biology of the dance language. Annu Rev Entomol 47:917–949. doi: 10.1146/Annurev.Ento.47.091201.145306 CrossRefPubMedGoogle Scholar
  10. Dyer JR, Ioannou CC, Morrell LJ, Croft DP, Couzin ID, Waters DA, Krause J (2008) Consensus decision making in human crowds. Anim Behav 75:461–470. doi: 10.1016/j.anbehav.2007.05.010 CrossRefGoogle Scholar
  11. Franks NR, Dornhaus A, Fitzsimmons JP, Stevens M (2003) Speed versus accuracy in collective decision making. Proc R Soc B 270:2457–2463. doi: 10.1098/rspb.2003.2527 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Franks NR et al. (2013) Speed–cohesion trade-offs in collective decision making in ants and the concept of precision in animal behaviour. Anim Behav 85:1233–1244. doi: 10.1016/j.anbehav.2013.03.010 CrossRefGoogle Scholar
  13. Gillespie DT (2007) Stochastic simulation of chemical kinetics. Annu Rev Phys Chem 58:35–55. doi: 10.1146/annurev.physchem.58.032806.104637 CrossRefPubMedGoogle Scholar
  14. Jack-McCollough RT, Nieh JC (2015) Honeybees tune excitatory and inhibitory recruitment signalling to resource value and predation risk. Anim Behav 110:9–17. doi: 10.1016/j.anbehav.2015.09.003 CrossRefGoogle Scholar
  15. Janson S, Middendorf M, Beekman M (2007) Searching for a new home - scouting behavior of honeybee swarms. Behav Ecol 18:384–392. doi: 10.1093/beheco/arl095 CrossRefGoogle Scholar
  16. Johnson BR, Nieh JC (2010) Modeling the adaptive role of negative signaling in honey bee intraspecific competition. J Insect Behav 23:459–471. doi: 10.1007/s10905-010-9229-5 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kietzman PM, Visscher PK (2015) The anti-waggle dance: use of the stop signal as negative feedback. Front Ecol Evol 3:14. doi: 10.3389/fevo.2015.00014 CrossRefGoogle Scholar
  18. Laomettachit T, Termsaithong T, Sae-Tang A, Duangphakdee O (2015) Decision-making in honeybee swarms based on quality and distance information of candidate nest sites. J Theor Biol 364:21–30. doi: 10.1016/j.jtbi.2014.09.005 CrossRefPubMedGoogle Scholar
  19. Lau CW, Nieh JC (2010) Honey bee stop-signal production: temporal distribution and effect of feeder crowding. Apidologie 41:87–95. doi: 10.1051/apido/2009052 CrossRefGoogle Scholar
  20. Lindauer M (1961) Communication among social bees. Harvard University Press, CambridgeGoogle Scholar
  21. Marshall JAR, Dornhaus A, Franks NR, Kovacs T (2006) Noise, cost and speed-accuracy trade-offs: decision-making in a decentralized system. J R Soc Interface 3:243–254. doi: 10.1098/rsif.2005.0075 CrossRefPubMedGoogle Scholar
  22. Marshall JAR, Bogacz R, Dornhaus A, Planque R, Kovacs T, Franks NR (2009) On optimal decision-making in brains and social insect colonies. J R Soc Interface 6:1065–1074. doi: 10.1098/rsif.2008.0511 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Masuda N, O’shea-Wheller TA, Doran C, Franks NR (2015) Computational model of collective nest selection by ants with heterogeneous acceptance thresholds. R Soc Open Sci 2:140533. doi: 10.1098/rsos.140533 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nieh JC (2010) A negative feedback signal that is triggered by peril curbs honey bee recruitment. Curr Biol 20:310–315. doi: 10.1016/j.cub.2009.12.060 CrossRefPubMedGoogle Scholar
  25. Niven JE (2012) How honeybees break a decision-making deadlock. Science 335:43–44. doi: 10.1126/science.1216563 CrossRefPubMedGoogle Scholar
  26. Pais D, Hogan PM, Schlegel T, Franks NR, Leonard NE, Marshall JAR (2013) A mechanism for value-sensitive decision-making. PLoS One 8:e73216. doi: 10.1371/journal.pone.0073216 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Passino KM, Seeley TD (2006) Modeling and analysis of nest-site selection by honeybee swarms: the speed and accuracy trade-off. Behav Ecol Sociobiol 59:427–442. doi: 10.1007/s00265-005-0067-y CrossRefGoogle Scholar
  28. Passino KM, Seeley TD, Visscher PK (2008) Swarm cognition in honey bees. Behav Ecol Sociobiol 62:401–414. doi: 10.1007/s00265-007-0468-1 CrossRefGoogle Scholar
  29. Perdriau BS, Myerscough MR (2007) Making good choices with variable information: a stochastic model for nest-site selection by honeybees. Biol Lett 3:140–143. doi: 10.1098/rsbl.2006.0599 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pirrone A, Stafford T, Marshall JAR (2014) When natural selection should optimize speed-accuracy trade-offs. Front Neurosci 8:73. doi: 10.3389/fnins.2014.00073 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pratt SC, Mallon EB, Sumpter DJ, Franks NR (2002) Quorum sensing, recruitment, and collective decision-making during colony emigration by the ant Leptothorax albipennis. Behav Ecol Sociobiol 52:117–127. doi: 10.1007/s00265-002-0487-x CrossRefGoogle Scholar
  32. Price RIA, Grüter C, Hughes WOH, Evison SEF (2016) Symmetry breaking in mass-recruiting ants: extent of foraging biases depends on resource quality. Behav Ecol Sociobiol:1–8. doi: 10.1007/s00265-016-2187-y
  33. Reina A, Valentini G, Fernández-Oto C, Dorigo M, Trianni V (2015) A design pattern for decentralised decision making. PLoS One 10:e0140950. doi: 10.1371/journal.pone.0140950 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Schaerf TM, Makinson JC, Myerscough MR, Beekman M (2013) Do small swarms have an advantage when house hunting? The effect of swarm size on nest-site selection by Apis mellifera. J R Soc Interface 10:20130533. doi: 10.1098/rsif.2013.0533 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Schürch R, Couvillon MJ, Burns DDR, Tasman K, Waxman D, Ratnieks FLW (2013) Incorporating variability in honey bee waggle dance decoding improves the mapping of communicated resource locations. J Comp Physiol A 199:1143–1152. doi: 10.1007/s00359-013-0860-4 CrossRefGoogle Scholar
  36. Seeley TD (2010) Honeybee democracy. Princeton University Press, PrincetonGoogle Scholar
  37. Seeley TD, Buhrman SC (1999) Group decision making in swarms of honey bees. Behav Ecol Sociobiol 45:19–31. doi: 10.1007/s002650050536 CrossRefGoogle Scholar
  38. Seeley TD, Buhrman SC (2001) Nest-site selection in honey bees: how well do swarms implement the "best-of-N″ decision rule? Behav Ecol Sociobiol 49:416–427. doi: 10.1007/s002650000299 CrossRefGoogle Scholar
  39. Seeley TD, Visscher PK (2003) Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making. Behav Ecol Sociobiol 54:511–520. doi: 10.1007/s00265-003-0664-6 CrossRefGoogle Scholar
  40. Seeley TD, Visscher PK (2004a) Group decision making in nest-site selection by honey bees. Apidologie 35:101–116. doi: 10.1051/apido:2004004 CrossRefGoogle Scholar
  41. Seeley TD, Visscher PK (2004b) Quorum sensing during nest-site selection by honeybee swarms. Behav Ecol Sociobiol 56:594–601. doi: 10.1007/s00265-004-0814-5 CrossRefGoogle Scholar
  42. Seeley TD, Visscher PK, Passino KM (2006) Group decision making in honey bee swarms. Am Sci 94:220–229CrossRefGoogle Scholar
  43. Seeley TD, Visscher PK, Schlegel T, Hogan PM, Franks NR, Marshall JAR (2012) Stop signals provide cross inhibition in collective decision-making by honeybee swarms. Science 335:108–111. doi: 10.1126/science.1210361 CrossRefPubMedGoogle Scholar
  44. Stewart KJ, Harcourt AH (1994) Gorillas’ vocalizations during rest periods: signals of impending departure? Behaviour 130:29–40. doi: 10.1163/156853994X00127 CrossRefGoogle Scholar
  45. Stroeymeyt N, Giurfa M, Franks NR (2010) Improving decision speed, accuracy and group cohesion through early information gathering in house-hunting ants PLoS One 5:e13059 doi: 10.1371/journal.pone.0013059
  46. Sueur C, Deneubourg J-L, Petit O (2010) Sequence of quorums during collective decision making in macaques. Behav Ecol Sociobiol 64:1875–1885. doi: 10.1007/s00265-010-0999-8 CrossRefGoogle Scholar
  47. Sumpter DJT, Beekman M (2003) From nonlinearity to optimality: pheromone trail foraging by ants. Anim Behav 66:273–280. doi: 10.1006/anbe.2003.2224 CrossRefGoogle Scholar
  48. Sumpter DJT, Pratt SC (2009) Quorum responses and consensus decision making. Philos Trans R Soc B 364:743–753. doi: 10.1098/rstb.2008.0204 CrossRefGoogle Scholar
  49. Sumpter DJT, Krause J, James R, Couzin ID, Ward AJW (2008) Consensus decision making by fish. Curr Biol 18:1773–1777. doi: 10.1016/j.cub.2008.09.064 CrossRefPubMedGoogle Scholar
  50. Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381:520–522. doi: 10.1038/381520a0 CrossRefPubMedGoogle Scholar
  51. Valentini G, Hamann H, Dorigo M (2015) Efficient decision-making in a self-organizing robot swarm: on the speed versus accuracy trade-off. In: Proceedings of the 2015 International Conference on Autonomous Agents and Multiagent Systems, International Foundation for Autonomous Agents and Multiagent Systems, pp 1305–1314Google Scholar
  52. Visscher PK (2007) Group decision making in nest-site selection among social insects. Annu Rev Entomol 52:255–275. doi: 10.1146/annurev.ento.51.110104.151025 CrossRefPubMedGoogle Scholar
  53. Visscher PK, Camazine S (1999) Collective decisions and cognition in bees. Nature 397:400–400. doi: 10.1038/17047 CrossRefGoogle Scholar
  54. Ward AJW, Sumpter DJT, Couzin ID, Hart PJB, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci U S A 105:6948–6953. doi: 10.1073/pnas.0710344105 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wickelgren WA (1977) Speed-accuracy tradeoff and information processing dynamics. Acta Psychol 41:67–85. doi: 10.1016/0001-6918(77)90012-9 CrossRefGoogle Scholar
  56. Yamaguchi M, Crump MJ, Logan GD (2013) Speed–accuracy trade-off in skilled typewriting: decomposing the contributions of hierarchical control loops. J Exp Psychol-Hum Percept Perform 39:678–699. doi: 10.1037/a0030512 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Bioinformatics and Systems Biology Program, School of Bioresources and TechnologyKing Mongkut’s University of Technology Thonburi (Bang Khun Thian Campus)BangkokThailand
  2. 2.Theoretical and Computational Physics (TCP) GroupKing Mongkut’s University of Technology ThonburiBangkokThailand
  3. 3.Learning InstituteKing Mongkut’s University of Technology ThonburiBangkokThailand
  4. 4.Department of Mathematics, Faculty of ScienceKing Mongkut’s University of Technology ThonburiBangkokThailand
  5. 5.King Mongkut’s University of Technology Thonburi (Ratchaburi Campus)RatchaburiThailand

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