Workers ‘specialized’ on inactivity: Behavioral consistency of inactive workers and their role in task allocation

Abstract

Social insect colonies are often considered to be highly efficient collective systems, with division of labor at the root of their ecological success. However, in many species, a large proportion of a colony’s workers appear to spend their time completely inactive. The role of this inactivity for colony function remains unclear. Here, we investigate how inactivity is distributed among workers and over time in the ant Temnothorax rugatulus. We show that the level of inactivity is consistent for individual workers, but differs significantly among workers, that is, some workers effectively specialize on ‘inactivity’. We also show that workers have circadian rhythms, although intra-nest tasks tend to be performed uniformly across the whole day. Differences in circadian rhythms, or workers taking turns resting (i.e., working in shifts), cannot explain the observation that some workers are consistently inactive. Using extensive individual-level data to describe the overall structure of division of labor, we show that ‘inactive workers’ form a group distinct from other task groups. Hierarchical clustering suggests that inactivity is the primary variable in differentiating both workers and tasks. Our results underline the importance of inactivity as a behavioral state and the need for further studies on its evolution.

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References

  1. Becker GS, Murphy KM (1992) The division of labor, coordination costs, and knowledge. Q J Econ 107:1137–1160

    Article  Google Scholar 

  2. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    PubMed Central  Article  PubMed  Google Scholar 

  3. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440

    CAS  Article  PubMed  Google Scholar 

  4. Boi S, Couzin ID, Del Buono N et al (1999) Coupled oscillators and activity waves in ant colonies. Proc R Soc Lond B Biol Sci 266:371–378

    Article  Google Scholar 

  5. Bowens SR., Glatt DP., Pratt SC. (2013) Visual navigation during colony emigration by the ant temnothorax rugatulus.

  6. Calabi P (1988) Behavioral flexibility in hymenoptera: a re-examination of the concept of caste. Adv Myrmecol 237–258

  7. Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire ant, solenopsis invicta. Anim Behav 50:801–813

    Article  Google Scholar 

  8. Charbonneau D, Dornhaus A (In revision) When doing nothing is something. How task allocation mechanisms compromise between flexibility, efficiency, and inactive agents.

  9. Charbonneau D, Hillis N, Dornhaus A (2015) “Lazy” in nature: ant colony time budgets show high’inactivity’ in the field as well as in the lab.

  10. Cole BJ (1986) The social behavior of leptothorax allardycei (hymenoptera, formicidae): Time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173

    Article  Google Scholar 

  11. Cole BJ (1981) Dominance hierarchies in leptothorax ants. Sci NY 212:83

    CAS  Article  Google Scholar 

  12. Cole BJ (1991) Short-term activity cycles in ants: Generation of periodicity by worker interaction. Am Nat 137:244–259

    Article  Google Scholar 

  13. Corbara B, Lachaud J-P, Fresneau D (1989) Individual variability, social structure and division of labour in the ponerine ant ectatomma ruidum roger (hymenoptera, formicidae). Ethology 82:89–100

    Article  Google Scholar 

  14. Dall SR, Griffith SC (2014) An empiricist guide to animal personality variation in ecology and evolution. Behav Evol Ecol 2:3

    Google Scholar 

  15. Dingemanse NJ, Both C, Drent PJ et al (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64:929–938

    Article  Google Scholar 

  16. Dornhaus A (2008) Specialization does not predict individual efficiency in an ant. PLoS Biol 6, e285

    PubMed Central  Article  PubMed  Google Scholar 

  17. Dornhaus A, Holley JA, Franks NR (2009) Larger colonies do not have more specialized workers in the ant temnothorax albipennis. Behav Ecol 20:922–929

    Article  Google Scholar 

  18. Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Annu Rev Ecol Evol Syst 42:91–110

    Article  Google Scholar 

  19. Durkheim E (1997) The division of labor in society. Simon and Schuster, New York, NY

    Google Scholar 

  20. Dyer FC, Could JL (1983) Honey Bee navigation: the honey bee’s ability to find its way depends on a hierarchy of sophisticated orientation mechanisms. Am Sci 71:587–597

    Google Scholar 

  21. Fellers JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78:69–76

    Article  Google Scholar 

  22. Fewell JH, Winston ML (1992) Colony state and regulation of pollen foraging in the honey bee, apis mellifera L. Behav Ecol Sociobiol 30:387–393

    Article  Google Scholar 

  23. Franks N, Tofts C (1994) Foraging for work—How tasks allocate workers. Anim Behav 48:470–472. doi:10.1006/anbe.1994.1261

    Article  Google Scholar 

  24. Fresneau D (1984) Développement ovarien et statut social chez une fourmi primitiveNeoponera obscuricornis emery (Hym. Formicidae, ponerinae). Insect Soc 31:387–402

    Article  Google Scholar 

  25. Frisch B, Koeniger N (1994) Social synchronization of the activity rhythms of honeybees within a colony. Behav Ecol Sociobiol 35:91–98

    Article  Google Scholar 

  26. Gadagkar R, Joshi NV (1984) Social organisation in the Indian wasp ropalidia cyathiformis (Fab.) (hymenoptera: vespidae). Z Für Tierpsychol 64:15–32

    Article  Google Scholar 

  27. Gerkey BP, Matarić MJ (2004) A formal analysis and taxonomy of task allocation in multi-robot systems. Int J Robot Res 23:939–954

    Article  Google Scholar 

  28. Gordon DM (2002) The organization of work in social insect colonies. Complexity 8:43–46

    Article  Google Scholar 

  29. Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124

    CAS  Article  Google Scholar 

  30. Gorelick R, Bertram SM (2007) Quantifying division of labor: borrowing tools from sociology, sociobiology, information theory, landscape ecology, and biogeography. Insect Soc 54:105–112

    Article  Google Scholar 

  31. Gorelick R, Bertram SM, Killeen PR, Fewell JH (2004) Normalized mutual entropy in biology: quantifying division of labor. Am Nat 164:677–682

    Article  PubMed  Google Scholar 

  32. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45

    CAS  Article  PubMed  Google Scholar 

  33. Guttman L (1954) Some necessary conditions for common-factor analysis. Psychometrika 19:149–161

    Article  Google Scholar 

  34. Herbers JM (1981) Time resources and laziness in animals. Oecologia 49:252–262

    Article  Google Scholar 

  35. Herbers JM (1983) Social organization in leptothorax ants: within-and between-species patterns. Psychol J Entomol 90:361–386

    Article  Google Scholar 

  36. Hillis N, Charbonneau D, Nguyen H, et al. (In prep.) Are “lazy” ants selfish? Testing whether inactive ant workers invest more in their own reproduction.

  37. Hölldobler B, Wilson EO (1990) The ants. Belknap press of harvard university press. MA, Cambridge

    Google Scholar 

  38. Ishii Y, Hasgeawa E (2013) The mechanism underlying the regulation of work-related behaviors in the monomorphic ant, myrmica kotokui. J Ethol 31:61–69

    Article  Google Scholar 

  39. Jandt JM, Dornhaus A (2011) Competition and cooperation: bumblebee spatial organization and division of labor may affect worker reproduction late in life. Behav Ecol Sociobiol 65:2341–2349

    Article  Google Scholar 

  40. Jandt JM, Huang E, Dornhaus A (2009) Weak specialization of workers inside a bumble bee (bombus impatiens) nest. Behav Ecol Sociobiol 63:1829–1836

    Article  Google Scholar 

  41. Jandt J, Robins N, Moore R, Dornhaus A (2012) Individual bumblebees vary in response to disturbance: a test of the defensive reserve hypothesis. Insect Soc 59:313–321

    Article  Google Scholar 

  42. Jeanson R, Fewell JH, Gorelick R, Bertram SM (2007) Emergence of increased division of labor as a function of group size. Behav Ecol Sociobiol 62:289–298

    Article  Google Scholar 

  43. Johnson BR (2008) Global information sampling in the honey bee. Naturwissenschaften 95:523–530

    CAS  Article  PubMed  Google Scholar 

  44. Johnson BR (2002) Reallocation of labor in honeybee colonies during heat stress: the relative roles of task switching and the activation of reserve labor. Behav Ecol Sociobiol 51:188–196. doi:10.1007/s00265-001-0419-1

    Article  Google Scholar 

  45. Johnson S (2012) Emergence: the connected lives of ants, brains, cities, and software. Simon and Schuster, New York, NY

    Google Scholar 

  46. Klein BA, Gibbs AG, Larsen KMF (2003) Signatures of sleep in the paper wasp Polistes flavus. The 2003 ESA Annual Meeting and Exhibition.

  47. Klein BA, Klein A, Wray MK et al (2010) Sleep deprivation impairs precision of waggle dance signaling in honey bees. Proc Natl Acad Sci 107:22705–22709

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  48. Klein BA, Olzsowy KM, Klein A et al (2008) Caste-dependent sleep of worker honey bees. J Exp Biol 211:3028–3040

    Article  PubMed  Google Scholar 

  49. Klein BA, Seeley TD (2011) Work or sleep? honeybee foragers opportunistically nap during the day when forage is not available. Anim Behav 82:77–83

    Article  Google Scholar 

  50. Kraus FB, Gerecke E, Moritz RFA (2011) Shift work has a genetic basis in honeybee pollen foragers.

  51. Kwapich CL, Tschinkel WR (2013) Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 67:2011–2027

    Article  Google Scholar 

  52. Lenoir A, Ataya H (1983) Polyéthisme et répartition des niveaux d’activité chez la fourmi lasius niger L. Z Für Tierpsychol 63:213–232

    Google Scholar 

  53. Lenoir A, Mardon JC (1978) Note sur l’application de l’analyse des correspondances a la division du travail chez les fourmis.

  54. Lindauer M (1952) Ein beitrag zur frage der arbeitsteilung im bienenstaat. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 34:299–345

    Google Scholar 

  55. Lone SR, Sharma VK (2011) Timekeeping through social contacts: social synchronization of circadian locomotor activity rhythm in the carpenter Ant camponotus paria. Chronobiol Int 28:862–872

    Article  PubMed  Google Scholar 

  56. Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a Key regulator of Ant social organization. Science 340:1090–1093. doi:10.1126/science.1234316

    CAS  Article  PubMed  Google Scholar 

  57. Mirenda JT, Vinson SB (1981) Division of labour and specification of castes in the red imported fire ant solenopsis invicta Buren. Anim Behav 29:410–420

    Article  Google Scholar 

  58. Moore D (2001) Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J Insect Physiol 47:843–857

    CAS  Article  Google Scholar 

  59. Moore D, Angel JE, Cheeseman IM et al (1995) A highly specialized social grooming honey bee (hymenoptera: apidae). J Insect Behav 8:855–861

    Article  Google Scholar 

  60. Moore D, Angel JE, Cheeseman IM et al (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160

    Article  Google Scholar 

  61. Nakagawa S, Schielzeth H (2010) Repeatability for gaussian and non-gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  62. North RD (1987) Circadian rhythm of locomotor activity in individual workers of the wood ant Formica rufa. Physiol Entomol 12:445–454

    Article  Google Scholar 

  63. North RD (1993) Entrainment of the circadian rhythm of locomotor activity in wood ants by temperature. Anim Behav 45:393–397

    Article  Google Scholar 

  64. O’Donnell S, Bulova SJ (2007) Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies. Insect Soc 54:203–210

    Article  Google Scholar 

  65. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Univ Pr, Princeton

    Google Scholar 

  66. Pamminger T, Foitzik S, Kaufmann KC et al (2014) Worker personality and its association with spatially structured division of labor. PLoS ONE 9, e79616

    PubMed Central  Article  PubMed  Google Scholar 

  67. Pearish S, Hostert L, Bell AM (2013) Behavioral type–environment correlations in the field: a study of three-spined stickleback. Behav Ecol Sociobiol 1–10

  68. Pinter-Wollman N, Hubler J, Holley J-A et al (2012) How is activity distributed among and within tasks in temnothorax ants? Behav Ecol Sociobiol 66:1407–1420

    Article  Google Scholar 

  69. Pol R, de Casenave JL (2004) Activity patterns of harvester ants pogonomyrmex pronotalis and pogonomyrmex rastratus in the central monte desert, Argentina. J Insect Behav 17:647–661

    Article  Google Scholar 

  70. Retana J, Cerdá X (1991) Behavioural variability and development of cataglyphis cursor ant workers (hymenoptera, formicidae) 1). Ethology 89:275–286

    Article  Google Scholar 

  71. Retana J, Cerdá X (1990) Social organization of cataglyphis cursor ant colonies (hymenoptera, formicidae): inter-, and intraspecific comparisons. Ethology 84:105–122

    Article  Google Scholar 

  72. Robinson GE, Huang Z-Y (1998) Colony integration in honey bees: genetic, endocrine and social control of division of labor. Apidologie 29:159–170

    Article  Google Scholar 

  73. Rosengaus RB, Traniello JF (1991) Biparental care in incipient colonies of the dampwood termiteZootermopsis angusticollis Hagen (isoptera: termopsidae). J Insect Behav 4:633–647

    Article  Google Scholar 

  74. Samways MJ (1993) Insects in biodiversity conservation: some perspectives and directives. Biodivers Conserv 2:258–282

    Article  Google Scholar 

  75. Schmid-Hempel P (1990) Reproductive competition and the evolution of work load in social insects. Am Nat 501–526

  76. Seeley TD (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293. doi:10.1007/BF00299306

    Article  Google Scholar 

  77. Seid MA, Traniello JF (2006) Age-related repertoire expansion and division of labor in pheidole dentata (hymenoptera: formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644

    Article  Google Scholar 

  78. Sendova-Franks AB, Hayward RK, Wulf B et al (2010) Emergency networking: famine relief in ant colonies. Anim Behav 79:473–485

    Article  Google Scholar 

  79. Sharma VK, Lone SR, Goel A, Chandrashekaran MK (2004) Circadian consequences of social organization in the ant species camponotus compressus. Naturwissenschaften 91:386–390

    CAS  PubMed  Google Scholar 

  80. Stamps J, Groothuis TG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325

    Article  PubMed  Google Scholar 

  81. Wilson EO (1991) Ants. Bull Am Acad Arts Sci 45:13–23

    Article  Google Scholar 

  82. Wilson EO (1976) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 1:141–154

    Article  Google Scholar 

  83. Yerushalmi S, Bodenhaimer S, Bloch G (2006) Developmentally determined attenuation in circadian rhythms links chronobiology to social organization in bees. J Exp Biol 209:1044–1051

    Article  PubMed  Google Scholar 

  84. Zhang J, Chen G (2011) The influence of logistics development on manufacturing division. Artificial Intelligence, Management Science and Electronic Commerce (AIMSEC), 2011 2nd International Conference on. pp 791–794

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Acknowledgments

We thank Alex Downs, Andrew Scott, Mary Levandowski, Matthew Velazquez, Neil Hillis, and Nicole Fischer for their help with ant painting and maintenance, and data collection. We also thank the entire Dornhaus lab for their ongoing feedback. Research supported through the GIDP-EIS and EEB Department at University of Arizona, as well as NSF grants no. IOS-1045239, IOS-0841756, and DBI-1262292 (to A.D.).

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Correspondence to Daniel Charbonneau.

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Communicated by L. Keller

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Charbonneau, D., Dornhaus, A. Workers ‘specialized’ on inactivity: Behavioral consistency of inactive workers and their role in task allocation. Behav Ecol Sociobiol 69, 1459–1472 (2015). https://doi.org/10.1007/s00265-015-1958-1

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Keywords

  • Task allocation
  • Specialization
  • Inactivity
  • Colony organization
  • Shift work
  • Circadian rhythm
  • Social insect
  • Temnothorax
  • Division of labor