Double allomimesis of advancing and retreating individuals maintains cohesion in exploring groups of nomadic caterpillars

Original Article

Abstract

Group-living entails that animals maintain cohesion during collective locomotion: This cohesion often requires that each individual respond to cues from several neighbours. Social insects generally use pheromone trails to integrate information from multiple group members. We demonstrate mechanisms used by nomadic social caterpillars to maintain cohesion when exploring off-trail. Our results show that forest tent caterpillars (Malacosoma disstria) use double allomimesis, responding to cues from both advancing and retreating neighbours. A group-level experiment measured cohesion and persistence of locomotion according to caterpillar age and group size. An individual-level experiment quantified responses to cues from neighbours, and a model was used to predict the group-level patterns that emerge from these responses. We show that double allomimesis generates feedback that maintains group cohesion, but at the price of locomotion efficiency, particularly in small groups of young caterpillars. We also show that the importance of allomimesis decreases as caterpillars age and show lesser responses to social cues. Finally, we demonstrate that, especially in the early instars, efficient collective locomotion is only possible in the large group sizes typically of field colonies.

Significance statement

Simple do-what-your-neighbour-is-doing mechanisms underlie mass collective locomotion of gregarious animals. Social insects generally use pheromone trails to follow each other. How then to stay together when exploring away from these trails? Forest tent caterpillars provide an intriguing example: They follow trails faithfully, but on unexplored territory turn back frequently to rejoin the trail behind them. We show how direct physical contact with advancing and retreating neighbours provides an explanation. An off-trail caterpillar turns back less often if it is propelled by a forward-moving neighbour, but more often if that neighbour turns back. This dual imitation keeps the group together, but at the price of efficient movement, especially in small groups. Groups as large as natural colonies seldom turn back due to the steady supply of advancing neighbours to propel forward and eventually replace vanguard individuals.

Keywords

Collective locomotion Self-organization Emergence Lepidoptera Social 

References

  1. Addy ND (1969) Rearing the forest tent caterpillar on an artificial diet. J Econ Entomol 62:270–271CrossRefGoogle Scholar
  2. Astudillo Fernandez A, Deneubourg JL (2011) On following behaviour as a mechanism for collective movement. J Theor Biol 284:7–15CrossRefGoogle Scholar
  3. Ballerini M, Cabibbo N, Candelier R, Cavagna A, Cisbani E, Giardina I, Lecomte V, Orlandi A, Parisi G, Procaccini A, Viale M, Zdravkovic V (2008) Interaction ruling animal collective behavior depends on topological rather than metric distance: evidence from a field study. Proc Natl Acad Sci 105:1232–1237CrossRefPubMedPubMedCentralGoogle Scholar
  4. Buhl J, Sumpter DJ, Couzin ID, Hale J, Despland E, Miller E, Simpson SJ (2006) From disorder to order in marching locusts. Science 312:1402–1406CrossRefPubMedGoogle Scholar
  5. Colasurdo N, Dussutour A, Despland E (2007) Do food protein and carbohydrate content influence the pattern of feeding and the tendency to explore of forest tent caterpillars? J Insect Physiol 53:1160–1168CrossRefPubMedGoogle Scholar
  6. Colasurdo N, Despland E (2005) Social cues and following behavior in the forest tent caterpillar. J Insect Behav 18:77–87CrossRefGoogle Scholar
  7. Conradt L, Roper TJ (2005) Consensus decision making in animals. TREE 20:449–456PubMedGoogle Scholar
  8. Costa JT (2006) The other insect societies. Belknap Press, Cambridge, 812 pGoogle Scholar
  9. Costa JT, Ross KG (2003) Fitness effects of group merging in a social insect. Proc Roy Soc B 270:1697–1702CrossRefGoogle Scholar
  10. Costa JT, Ross KG (1993) Seasonal decline in the intracolony genetic relatedness of eastern tent caterpillars: implications for social evolution. Behav Ecol Sociobiol 32:47–54CrossRefGoogle Scholar
  11. Couzin ID, Krause J (2003) Self-organization and collective behavior in vertebrates. Adv Study Behav 32:1–75CrossRefGoogle Scholar
  12. Despland E (2013) Plasticity of collective behavior in a nomadic early spring folivore. Frontiers Physiol 4:54. doi:10.3389/fphys.2013.00054
  13. Despland E, Le Huu A (2007) Pros and cons of group-living in the forest tent caterpillar: separating the roles of silk and of grouping. Entomol Exp App 122:181–189CrossRefGoogle Scholar
  14. Despland E, Simpson SJ (2006) Resource distribution mediates synchronization of physiological rhythms in locust groups. Proc Roy Soc B 273:1517–1522CrossRefGoogle Scholar
  15. Despland E, Hamzeh S (2004) Ontogenetic changes in social behaviour in the forest tent caterpillar, Malacosoma disstria. Behav Ecol Sociobiol 56:177–184CrossRefGoogle Scholar
  16. Dostalkova I, Spinka M (2007) Synchronization of behaviour in pairs: the role of communication and consequences in timing. Anim Behav 74:1735–1742CrossRefGoogle Scholar
  17. Dussutour A, Nicolis SC, Despland E, Simpson SJ (2008) Individual differences influence collective behaviour in social caterpillars. Anim Behav 76:5–16CrossRefGoogle Scholar
  18. Dussutour A, Colasurdo N, Nicolis SC, Despland E (2007) How do ants and social caterpillars collectively make decisions? In: Hardy-Vallée B (ed) Cognitive decision-making: empirical and foundational issues. Cambridge Scholars Publishing, Newcastle, pp 48–65Google Scholar
  19. Fabre JH (1899) Souvenirs Entomologiques: La Processionnaire du Pin: la procession. Série VI, Chapitre 20. FranceGoogle Scholar
  20. Fitzgerald TD (1995) The tent caterpillars. Cornell University Press, Ithaca, 303 pGoogle Scholar
  21. Fitzgerald TD, Costa JT (1986) Trail-based communication and foraging behavior of young colonies of forest tent caterpillars (Lepidoptera: Lasiocampidae). Ann Entomol Soc Am 79:999–1007CrossRefGoogle Scholar
  22. Gautrais J, Michelina P, Sibbald A, Bon R, Deneubourg JL (2007) Allelomimetic synchronization in merino sheep. Anim Behav 74:1443–1454CrossRefGoogle Scholar
  23. Haccou P, Meelis E (1992) Statistical analysis of behavioural data: an approach based on time-structured models. Oxford University Press, OxfordGoogle Scholar
  24. Herbert-Read JE, Perna A, Mann RP, Schaerf TM, Sumpter DJT, Ward AJW (2001) Inferring the rules of interaction of shoaling fish. Proc Natl Acad Sci 108:18726–18731CrossRefGoogle Scholar
  25. Jeanson R, Dussutour A, Fourcassié V (2012) Key factors for the emergence of collective decisions in invertebrates. Frontiers Neurosci 6:121CrossRefGoogle Scholar
  26. Jeanson R, Rivault C, Deneubourg JL, Blanco S, Fournier R, Jost C, Theraulaz G (2005) Self-organized aggregation in cockroaches. Anim Behav 69:169–180CrossRefGoogle Scholar
  27. McClure M, Despland E (2011) Defensive responses by a social caterpillar are tailored to different predators and change with larval instar and group size. Naturwissenschaften 98:425–434CrossRefPubMedGoogle Scholar
  28. McClure M, Ralph M, Despland E (2011) Group leadership depends on energetic state in a nomadic collective foraging caterpillar. Behav Ecol Sociobiol 65:1573–1579CrossRefGoogle Scholar
  29. McClure M, Despland E (2010) Collective foraging pattern of field colonies of Malacosoma disstria caterpillars. Can Entomol 142:473–480CrossRefGoogle Scholar
  30. Miller J, Janzen D, Hallwachs W (2006) 100 Caterpillars. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  31. Nemiroff L, Despland E (2007) Do forest tent caterpillars (Malacosoma disstria) exhibit persistent individual differences in behaviour? Evidence for temperament in an outbreaking insect. Can J Zool 85:1117–1124CrossRefGoogle Scholar
  32. Peters MI, Despland E (2006) Plasticity in forest tent caterpillar self-organized collective foraging. Ethology 112:521–528CrossRefGoogle Scholar
  33. Petit O, Bon R (2010) Decision-making processes: the case of collective movements. Behav Process 84:635–647CrossRefGoogle Scholar
  34. Petit O, Gautrais J, Leca JB, Theraulaz G, Deneubourg J (2009) Collective decision-making in white-faced capuchin monkeys. Proc Roy Soc B 276:3495–3503CrossRefGoogle Scholar
  35. Pillot MH, Deneubourg JL (2010) Collective movements, initiation and stops: diversity of situations and law of parsimony. Behav Process 84:657–661Google Scholar
  36. Pillot MH, Gautrais J, Bon R, Deneubourg JL (2011) Scalable rules for coherent group motion in a gregarious vertebrate. PLoS ONE 6:e14487 Google Scholar
  37. Robison DJ (1993) The feeding ecology of the forest tent caterpillar, Malacosoma disstria Hübner, among hybrid poplar clones, Populus spp. PhD Thesis, University of WisconsinGoogle Scholar
  38. Santana AFK, McClure M, Ethier J, Despland E (2015) Exploration costs promote conservative collective foraging in the social caterpillar Malacosoma disstria. Anim Behav 105:245–250CrossRefGoogle Scholar
  39. Sumpter DJ (2010) Collective animal behavior. Princeton University Press, New Jersey, USACrossRefGoogle Scholar
  40. Viscido SV, Parrish JK, Grünbaum D (2005) The effect of population size and number of influential neighbors on the emergent properties of fish schools. Ecol Model 183:347–363CrossRefGoogle Scholar
  41. Ward A, Sumpter DJ, Couzin ID, Hart P, Krause J (2008) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci 105:6948–6953CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Biology DepartmentConcordia UniversityMontrealCanada

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