Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Collective foraging decision in a gregarious insect

Abstract

Group foraging by eusocial insects implies sophisticated recruitment processes that often result in collective decisions to exploit the most profitable sources. These advanced levels of cooperation, however, remain limited to a small range of species, and we still know little about the mechanisms underlying group foraging behaviours in the great mass of animals exhibiting lower levels of social complexity. In this paper, we report, for the first time in a gregarious insect, the cockroach Blattella germanica (L.), a collective foraging decision whereby the selection of food sources is reached without requiring active recruitment. Groups of cockroaches given a binary choice between identical food sources exhibited exploitation asymmetries whose amplitude increases with group size. By coupling behavioural observations to computer simulations, we demonstrate that selection of food sources relies uniquely on a retention effect of feeding individuals on newcomers without comparison between available opportunities. This self-organised pattern presents similarities with the foraging dynamics of eusocial species, thus stressing the generic dimension of collective decision-making mechanisms based on social amplification rules despite fundamental differences in recruitment processes. We hypothesise that such parsimony could apply to a wide range of species and help understand the emergence of collective behaviours in simple social systems.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Amé JM, Rivault C, Deneubourg JL (2004) Cockroach aggregation based on strain odour recognition. Anim Behav 68:793–801. doi:10.1016/j.anbehav.2004.01.009

  2. Amé JM, Halloy J, Rivault C, Detrain C, Deneubourg JL (2006) Collegial decision making based on social amplification leads to optimal group formation. Proc Natl Acad Sci USA 103:5835–5840. doi:10.1073/pnas.0507877103

  3. Beckers R, Deneubourg JL, Goss S (1992) Trails and U-turns in the selection of a path by the ant Lasius niger. J Theor Biol 159:397–415

  4. Beekman M, Sumpter DJT, Ratnieks FLW (2001) Phase transition between disordered and ordered foraging in Pharaoh’s ants. Proc Natl Acad Sci USA 98:9703–9706. doi:10.1073/pnas.161285298

  5. Boulinier T, Danchin E (1997) The use of conspecific reproductive success for breeding patch selection in territorial migratory species. Evol Ecol 11:505–517. doi:10.1007/s10682-997-1507-0

  6. Buhl J, Sumpter DJT, Couzin ID, Hale JJ, Despland E, Miller ER, Simpson SJ (2006) From disorder to order in marching locusts. Science 312:1402–1406. doi:10.1126/science.1125142

  7. Camazine S, Sneyd J (1991) A model of collective nectar source selection by honey bees: self-organization through simple rules. J Theor Biol 149:547–571

  8. Camazine S, Deneubourg JL, Franks N, Sneyd J, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, Princeton

  9. Cocroft RB (2005) Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. Proc R Soc B 272:1023–1029. doi:10.1098/rspb.2004.3041

  10. Conradt L, Roper TJ (2005) Consensus decision making in animals. Trends Ecol Evol 20:449–456. doi:10.1016/j.tree.2005.05.008

  11. Costa JT (2006) The other insect societies. Harvard University Press, Cambridge

  12. Couzin ID, Krause J, Franks NR, Levin S (2005) Effective leadership and decision-making in animal groups on the move. Nature 433:513–516. doi:10.1038/nature03236

  13. Dall SRX, Giraldeau LA, Olson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193. doi:10.1016/j.tree.2005.01.010

  14. Dambach M, Goehlen B (1999) Aggregation density and longevity correlate with humidity in first instar nymphs of the cockroach Blattella germanica L. (Dictyoptera). J Insect Physiol 45:423–429. doi:10.1016/S0022-1910(98)00141-3

  15. Danchin E, Giraldeau LA, Valone TJ, Wagner RH (2004) Public information: from noisy neighbors to cultural evolution. Science 305:487–491. doi:10.1126/science.1098254

  16. Deneubourg JL, Goss S (1989) Collective patterns and decision-making. Ethol Ecol Evol 1:295–311

  17. Deneubourg JL, Gregoire JC, Le Fort E (1990) Kinetics of larval gregarious behavior in the bark beetle Dendroctonus micans (Coleoptera: Scolytidae). J Insect Behav 3:169–182. doi:10.1007/BF01417910

  18. Durier V, Rivault C (2000a) Comparisons of toxic baits for controlling the cockroach, Blattella germanica (L.): attractiveness and feeding stimulation. Med Vet Entomol 14:410–418. doi:10.1111/j.1365-2915.2000.00259.x

  19. Durier V, Rivault C (2000b) Learning and foraging efficiency in German cockroaches, Blattella germanica (L.) (Insecta: Dictyoptera). Anim Cogn 3:139–145. doi:10.1007/s100710000065

  20. Durier V, Rivault C (2001) Effects of spatial knowledge and feeding experience on foraging choices in German cockroaches. Anim Behav 62:681–688. doi:10.1006/anbe.2001.1807

  21. Dussutour A, Simpson SJ, Despland E, Colasuro N (2007) When the group denies nutritional wisdom. Anim Behav 74:931–939. doi:10.1016/j.anbehav.2006.12.022

  22. Dyer JRG, 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

  23. Fitzgerald D (1995) The tent caterpillars. Cornell University Press, Ithaca

  24. Fretwell SD (1972) Populations in a seasonal environment. Princeton University Press, Princeton

  25. Gautrais J, Michelena P, Sibbald A, Bon R, Deneubourg JL (2007) Allelomimetic synchronization in Merino sheep. Anim Behav 74:1443–1454. doi:10.1016/j.anbehav.2007.02.020

  26. Giraldeau LA, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton

  27. Grégoire JC (1988) The greater European spruce beetle. In: Berryman AA (ed) Dynamics of forest insect populations: patterns, causes, implications. Plenum, New York, pp 455–478

  28. Hemptinne JL, Gaudin M, Dixon AFG, Lognay G (2000) Social feeding in ladybird beetles: adaptive significance and mechanism. Chemoecology 10:149–152. doi:10.1007/PL00001817

  29. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

  30. Hölldobler B, Wilson EO (2008) The superorganisms: the beauty, elegance and strangeness of insect societies. Norton, New York

  31. Jeanson R, Deneubourg JL (2007a) Path selection in cockroaches. J Exp Biol 209:4768–4775. doi:10.1242/jeb.02562

  32. Jeanson R, Deneubourg JL (2007b) Conspecific attraction and shelter selection in gregarious insects. Am Nat 170:47–58. doi:10.1086/518570

  33. Jeanson R, Deneubourg JL, Theraulaz G (2004) Discrete dragline attachment induces aggregation in spiderlings of a solitary species. Anim Behav 67:531–537. doi:10.1016/j.anbehav.2003.06.013

  34. Jeanson R, Rivault C, Deneubourg JL, Blanco S, Fournier R, Jost C, Theraulaz G (2005) Self-organized aggregation in cockroaches. Anim Behav 69:169–180. doi:10.1016/j.anbehav.2004.02.009

  35. Korb J, Heinze J (2008) The ecology of social evolution. Springer, Berlin

  36. Krause J, Ruxton G (2002) Living in groups. Oxford University Press, London

  37. Krause J, Croft DP, James R (2007) Social network theory in the behavioural sciences: potential applications. Behav Ecol Sociobiol 62:15–27. doi:10.1007/s00265-007-0445-8

  38. Leadbeater E, Chittka L (2007) Social learning in insects—from miniature brains to consensus building. Curr Biol 17:R703–R713. doi:10.1016/j.cub.2007.06.012

  39. Lihoreau M, Rivault C (2008) Tactile stimuli triggers groups effects in cockroach aggregations. Anim Behav 75:1965–1972. doi:10.1016/j.anbehav.2007.12.006

  40. Lihoreau M, Rivault C (2009) Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav Ecol 20:46–53. doi:10.1093/beheco/arn113

  41. Lihoreau M, Brepson L, Rivault C (2009) The weight of the clan: even in insects, social isolation can induce a behavioural syndrome. Behav Processes 82:81–84. doi:10.1016/j.beproc.2009.03.008

  42. Marée FM, Hogeweg P (2001) How amoeboids self-organize into a fruiting body: multicellular coordination in Dictyostelium discoideum. Proc Natl Acad Sci USA 98:3879–3883. doi:10.1073/pnas.061535198

  43. Marshall JAR, Franks NR (2009) Colony-level cognition. Curr Biol 19:R395–R396. doi:10.1016/j.cub.2009.03.011

  44. Moody AL, Houston AI, McNamara JM (1996) Ideal free distributions under predation risk. Behav Ecol Sociobiol 38:131–143. doi:10.1007/s002650050225

  45. Nicolis SC, Deneubourg JL (1999) Emerging patterns and food recruitment in ants: an analytical study. J Theor Biol 4:575–592. doi:10.1006/jtbi.1999.0934

  46. Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99–101. doi:10.1126/science.284.5411.99

  47. 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

  48. Pratt SC, Sumpter DJT (2006) A tunable algorithm for collective decision-making. Proc Natl Acad Sci USA 103:15906–15910. doi:0.1073/pnas.0604801103

  49. R Development Core Team (2007) R: A language and environment for statistical computing, R Foundation for Statistical Computing edition. R Foundation for Statistical Computing, Vienna

  50. Rivault C (1989) Spatial distribution of the cockroach Blattella germanica in a swimming bath facility. Entomol Exp Appl 53:247–255

  51. Robinson EJH, Smith FD, Sullivan KME, Franks NR (2009) Do ants make direct comparisons? Proc R Soc B 276:2635–2641. doi:10.1098/rspb.2009.0350

  52. Rust MK, Owens JM, Reirson DA (1995) Understanding and controlling the German cockroach. Oxford University Press, New York

  53. Salganik MJ, Dodds PS, Watts DJ (2006) Experimental study of inequality and unpredictability in an artificial cultural market. Science 311:854–856. doi:10.1126/science.1121066

  54. Seeley TD (1995) The wisdom of the hive. Harvard University Press, Cambridge

  55. Sibbald AM, Hooper RJ (2004) Sociability and the willingness of individual sheep to move away from their companions in order to graze. Appl Anim Behav Sci 86:51–62. doi:10.1016/j.applanim.2003.11.010

  56. Simons AM (2004) Many wrongs: the advantage of group navigation. Trends Ecol Evol 19:453–455. doi:10.1016/j.tree.2004.07.001

  57. Sontag C, Wilson DS, Wilcox S (2006) Social foraging in Bufo americanus tadpoles. Anim Behav 72:1451–1456. doi:10.1016/j.anbehav.2006.05.006

  58. Sumpter DJT (2009) Collective animal behaviour. Princeton University Press, Princeton

  59. Sumpter DJT, Pratt BL (2003) A modelling framework for understanding social insect foraging. Behav Ecol Sociobiol 53:131–144. doi:10.1007/s00265-002-0549-0

  60. Sumpter DJT, Pratt BL (2009) Quorum responses and consensus decision making. Philos Trans R Soc B 364:743–753. doi:10.1098/rstb.2008.0204

  61. 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

  62. Valone TJJ, Templeton JJ (2002) Public information for the assessment of quality: a widespread social phenomenon. Philos Trans R Soc Lond B 357:1549–1557. doi:10.1098/rstb.2002.1064

  63. Ward JW, Sumpter DJT, Couzin ID, Hart PJB, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci USA 105:6948–6953. doi:10.1126/science.1098254

Download references

Acknowledgements

We thank C. Caillarec for having implemented the first steps of the model and F. Nassur for technical help. We are also grateful to A. Cloarec for comments on the manuscript. This work was supported by a grant from the French Ministry of Research and Education to M.L.

Author information

Correspondence to Mathieu Lihoreau.

Additional information

Communicated by M. Beekman

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 164 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lihoreau, M., Deneubourg, J. & Rivault, C. Collective foraging decision in a gregarious insect. Behav Ecol Sociobiol 64, 1577–1587 (2010). https://doi.org/10.1007/s00265-010-0971-7

Download citation

Keywords

  • Collective decision making
  • Foraging behaviour
  • Gregarious cockroaches
  • Retention effect