Behavioral Ecology and Sociobiology

, Volume 60, Issue 5, pp 631–644 | Cite as

Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants

  • Marc A. Seid
  • James F. A. Traniello
Original article


The controversy concerning the extent to which the organization of division of labor in social insects is a developmental process or is based on task allocation dynamics that emerge from colony need independent of worker age and endocrine or neural state has yet to be resolved. We present a novel analysis of temporal polyethism in the ant Pheidole dentata, demonstrating that task attendance by minor workers does not shift among spatially associated sets of behaviors that minimally overlap but rather expands with age. Our results show that the number of tasks performed by older minors increases through the addition and retention of behaviors, with up to a sixfold increase in repertoire size from day 1 to day 20 of adult life. We also show that older minors respond to colony needs by performing significantly more brood care as its demand increases, indicating that they can quickly upregulate nursing according to labor requirements. This level of plasticity was absent in younger siblings. The breadth of responsiveness to task-related olfactory stimuli increased with age. In a binary choice test in which young and old minor workers could orient toward odorants from brood or food, older workers responded to both brood and food, whereas young workers responded only to brood. These dissimilar responses to stimuli associated with nursing and foraging indicate age-related differences in sensory ability and provide a physiological basis for the age-related repertoire expansion model. We discuss repertoire expansion in P. dentata in light of behavioral development and caste flexibility in ants.


Caste Social insect Behavioral development Olfaction 



We thank Sam Beshers and anonymous reviewers for their valuable feedback on the manuscript, and we are grateful to Sanford Porter and Lloyd Davis for the assistance in the collection of colonies and the use of their laboratory facilities. This research was supported in part by NSF Grant IBN-0116857 (J. Traniello and R. Rosengaus, coPIs).


  1. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440PubMedCrossRefGoogle Scholar
  2. Beshers SN, Traniello JFA (1994) The adaptiveness of worker demography in the attine ant Trachymyrmex septentrionalis. Ecology 75:763–775CrossRefGoogle Scholar
  3. Bonabeau E (1998) Social insect colonies as complex adaptive systems. Ecosystems 1:437–443CrossRefGoogle Scholar
  4. Bonabeau E, Theraulaz G, Deneubourg JL (1996) Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc R Soc Lond B 263:1565–1569CrossRefGoogle Scholar
  5. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, NJGoogle Scholar
  6. Brown JJ, Traniello JFA (1998) Regulation of brood-care behavior in the dimorphic castes of the ant Pheidole morrisi (Hymenoptera: Formicidae): effects of caste ratio, colony size, and colony needs. J Insect Behav 11:209–219CrossRefGoogle Scholar
  7. Byrne RW, Byrne JME (1993) Complex leaf-gathering skills of mountain gorillas (Gorilla G-beringei) variability and standardization. Am J Primatol 31:241–261CrossRefGoogle Scholar
  8. Calabi P, Traniello JFA (1989a) Behavioral flexibility in age castes of the ant Pheidole dentata. J Insect Behav 2:663–677CrossRefGoogle Scholar
  9. Calabi P, Traniello JFA (1989b) Social organization in the ant Pheidole dentata—physical and temporal caste ratios lack ecological correlates. Behav Ecol Sociobiol 24:69–78CrossRefGoogle Scholar
  10. Calabi P, Traniello JFA, Werner MH (1983) Age polyethism: its occurrence in the ant Pheidole hortensis, and some general considerations. Psyche 90:395–412CrossRefGoogle Scholar
  11. Cammaerts-Tricot MC (1974) Production and perception of attractive pheromones by differently aged workers of Myrmica rubra (Hymenoptera Formicidae). Insectes Soc 21:235–248CrossRefGoogle Scholar
  12. Carey JR (2001) Demographic mechanisms for the evolution of long life in social insects. Exp Gerontol 36:713–722PubMedCrossRefGoogle Scholar
  13. Cassill DL, Tschinkel WR (1999) Effects of colony-level attributes on larval feeding in the fire ant, Solenopsis invicta. Insectes Soc 46:261–266CrossRefGoogle Scholar
  14. Changizi MA (2003) Relationship between number of muscles, behavioral repertoire size, and encephalization in mammals. J Theor Biol 220:157–168PubMedCrossRefGoogle Scholar
  15. Creemers B, Billen J, Gobin B (2003) Larval begging behaviour in the ant Myrmica rubra. Ethol Ecol Evol 15:261–272Google Scholar
  16. Detrain C, Pasteels JM (1991) Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant, Pheidole pallidula (Nyl.) Hymenoptera: Myrmicinae). J Insect Behav 4:157–176CrossRefGoogle Scholar
  17. Detrain C, Pasteels JM (1992) Caste polyethism and collective defense in the ant, Pheidole pallidula: the outcome of quantitative differences in recruitment. Behav Ecol Sociobiol 29:405–412CrossRefGoogle Scholar
  18. Franks NR, Tofts C (1994) Foraging for work: how tasks allocate workers. Anim Behav 48:470–472CrossRefGoogle Scholar
  19. Franks NR, Tofts C, Sendova-Franks AB (1997) Studies of the division of labour: neither physics nor stamp collecting. Anim Behav 53:219–224CrossRefGoogle Scholar
  20. Geberzahn N (2003) Is quantity of song type use in adult birds related to singing during development? Behaviour 140:593–602CrossRefGoogle Scholar
  21. Gil D, Cobb JLS, Slater PJB (2001) Song characteristics are age dependent in the willow warbler, Phylloscopus trochilus. Anim Behav 62:689–694CrossRefGoogle Scholar
  22. Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124CrossRefGoogle Scholar
  23. Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–377CrossRefGoogle Scholar
  24. Greene MJ, Gordon DM (2003) Social insects–cuticular hydrocarbons inform task decisions. Nature 423:32–32PubMedCrossRefGoogle Scholar
  25. Holldöbler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, MAGoogle Scholar
  26. Huang ZY, Robinson GE (1992) Honeybee colony integration: worker–worker interactions mediate hormonally regulated plasticity in division-of-labor. Proc Natl Acad Sci USA 89:11726–11729PubMedCrossRefGoogle Scholar
  27. Huang ZY, Robinson GE (1996) Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39:147–158CrossRefGoogle Scholar
  28. Huang ZY, Robinson GE, Borst DW (1994) Physiological correlates of division-of-labor among similarly aged honey bees. J Comp Physiol A 174:731–739PubMedCrossRefGoogle Scholar
  29. Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Can J Zool 80:16–23CrossRefGoogle Scholar
  30. Johnson BJ (2002) Organization of work in the honeybee: a compromise between division of labour and behavioural flexibility. Proc R Soc Lond B 270:147–152CrossRefGoogle Scholar
  31. Johnson BR (2005) Limited flexibility in the temporal caste system of the honey bee. Behav Ecol Sociobiol 58:219–226CrossRefGoogle Scholar
  32. Karsai I, Wenzel JW (1998) Productivity, individual-level and colony-level flexibility, and organization of work as consequences of colony size. Proc Natl Acad Sci U S A 95:8665–8669PubMedCrossRefGoogle Scholar
  33. LaPolla JS, Mueller UG, Seid M, Cover SP (2002) Predation by the army ant Neivamyrmex rugulosus on the fungus- growing ant Trachymyrmex arizonensis. Insectes Soc 49:251–256CrossRefGoogle Scholar
  34. MacDougall-Shackleton SA, Ball GF, Edmonds E, Sul R, Hahn TP (2005) Age- and sex-related variation in song-control regions in Cassin’s finches, Carpodacus cassinii. Brain Behav Evol 65:262–267PubMedCrossRefGoogle Scholar
  35. McDonald P, Topoff H (1985) Social regulation and behavioral development in the ant, Novomessor albisetosus (Mayr). J Comp Psychol 99:3–14CrossRefGoogle Scholar
  36. Naug D, Gadagkar R (1998) The role of age in temporal polyethism in a primitively eusocial wasp. Behav Ecol Sociobiol 42:37–47CrossRefGoogle Scholar
  37. Naug D, Gadagkar R (1999) Flexible division of labor mediated by social interactions in an insect colony—a simulation model. J Theor Biol 197:123–133PubMedCrossRefGoogle Scholar
  38. O’Donnell S (2001) Worker age, ovary development, and temporal polyethism in the swarm-founding wasp Polybia occidentalis (Hymenoptera: Vespidae). J Insect Behav 14:201–213CrossRefGoogle Scholar
  39. O’Donnell S, Donlan NA, Jones TA (2004) Mushroom body structural change is associated with division of labor in eusocial wasp workers (Polybia aequatorialis, Hymenoptera: Vespidae). Neurosci Lett 356:159–162PubMedCrossRefGoogle Scholar
  40. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton, NJGoogle Scholar
  41. Ott RL (1994) An introduction to statistical methods and data analysis, 4th edn. Duxbury Press, Belmont, CAGoogle Scholar
  42. Passera L, Roncin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630–631CrossRefGoogle Scholar
  43. Porter SD, Jorgensen CD (1981) Foragers of the harvester ant, Pogonomyrmex owyheei: a disposable caste? Behav Ecol Sociobiol 9:247–256CrossRefGoogle Scholar
  44. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  45. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665PubMedCrossRefGoogle Scholar
  46. Robinson GE (2002) Genomics and integrative analyses of division of labor in honeybee colonies. Am Nat 160:S160–S172CrossRefGoogle Scholar
  47. Rosengaus RB, Traniello JFA (1993) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis—a single multiage caste. J Insect Behav 6:237–252CrossRefGoogle Scholar
  48. Schmid-Hempel P (1991) The ergonomics of worker behavior in social Hymenoptera. Adv Study Behav 20:87–134CrossRefGoogle Scholar
  49. Seeley T (1982) Adaptive significance of the age polyethism schedule in honeybee colonies. Behav Ecol Sociobiol 11:287–293CrossRefGoogle Scholar
  50. Seid MA, Traniello JFA (2005) Age-related changes in biogenic amines in individual brains of the ant Pheidole dentata. Naturwissenschaften 92:198–201PubMedCrossRefGoogle Scholar
  51. Seid MA, Harris KM, Traniello JFA (2005) Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J Comp Neurol 488:269–277PubMedCrossRefGoogle Scholar
  52. Sempo G, Detrain C (2004) Between-species differences of behavioural repertoire of castes in the ant genus Pheidole: a methodological artifact? Insectes Soc 51:48–54CrossRefGoogle Scholar
  53. Sendova-Franks A, Franks NR (1993) Task allocation in ant colonies within variable environments (A study of temporal polyethism, experimental). Bull Math Biol 55:75–96CrossRefGoogle Scholar
  54. Tofts C (1993) Algorithms for task allocation in ants (A study of temporal polyethism: theory). Bull Math Biol 55:891–918Google Scholar
  55. Topoff H, Boshes M, Trakimas W (1972) A comparison of trail following between callow and adult workers of the army ant Neivamyrmex nigrescens (Formicidae: Dorylinae). Anim Behav 20:361–366CrossRefGoogle Scholar
  56. Traniello JFA, Rosengaus RB (1997) Ecology, evolution and division of labour in social insects. Anim Behav 53:209–213CrossRefGoogle Scholar
  57. Tschinkel WR (1988) Colony growth and the ontogeny of worker polymorphism in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 22:103–115CrossRefGoogle Scholar
  58. Tschinkel WR (1993) Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol Monogr 64:425–457CrossRefGoogle Scholar
  59. Tsuchida K (1991) Temporal behavioral variation and division-of-labor among workers in the primitively eusocial wasp Polistes jadwigae Dalla Torre. J Ethol 9:129–134CrossRefGoogle Scholar
  60. Wilson EO (1953) The origin and evolution of polymorphism in ants. Q Rev Biol 28:136–156PubMedCrossRefGoogle Scholar
  61. Wilson EO (1968) The ergonomics of caste in the social insects. Am Nat 102:41–66CrossRefGoogle Scholar
  62. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, MAGoogle Scholar
  63. Wilson EO (1976a) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 1:141–154CrossRefGoogle Scholar
  64. Wilson EO (1976b) The organization of colony defense in the ant Pheidole dentata Mayr (Hymenoptera: Formicidae). Behav Ecol Sociobiol 1:63–81CrossRefGoogle Scholar
  65. Wilson EO (1984) The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae). Behav Ecol Sociobiol 16:89–98CrossRefGoogle Scholar
  66. Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495PubMedCrossRefGoogle Scholar
  67. Wilson EO (2003) Pheidole in the New World: a dominant, hyperdiverse ant genus. Harvard University Press, Cambridge, MAGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of BiologyBoston UniversityBostonUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaPanama

Personalised recommendations