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

Differential responses to chemical cues correlate with task performance in ant foragers


Division of labor in social insects has been explained by response threshold models which are based on differential responses to task-specific stimuli. In the present study, we argue that other types of stimuli, such as location-related cues, which are correlated with but not directly linked to task performance, may be significant. Using the black garden ant Lasius niger as a model, we focused on three groups of workers that perform extranidal tasks: (1) scouts, which explore new and unmarked areas remote from the nest; (2) patrollers, which are not recruited by other ants, but nonetheless walk outside in the nest vicinity; and (3) recruits, which are temporary foragers whose exit is triggered by recruitment. We used standardized tests to investigate, in a context-independent way, whether differences in task performance by these three groups could be correlated to intrinsic differences in their responsiveness to trail pheromone or to nest-related stimuli such as the presence of nestmates or colony odor. Overall, we found that the task profile of workers was correlated neither with their tendency to explore unmarked areas nor with their social attraction to nestmates. Scouts showed a lower attraction to colony odor and lower scores of trail following than recruits. Conversely, recruits were more attracted to colony chemical cues and showed lower response threshold to trail pheromone. Patrollers displayed behaviors between those of recruits and scouts. Our study thus shows that differences in ant responsiveness to location-related cues and recruitment trails contribute to the regulation of extranidal tasks in ants.

Significance statement

Work organization in insect societies has been explained by models of differential response thresholds to stimuli that are directly linked to the performance of specific tasks. However, the task performance of individuals could also depend on their responsiveness to social and location-related cues that are correlated but not directly linked to these tasks. Using standardized context-independent tests, we found that scout ants, which explore unknown areas, display a lower responsiveness to colony area marking and trail pheromone. Conversely, recruits, which forage outside the nest only during food exploitation, are the most attracted to nestmates, colony area marking and trail pheromone. Patrollers display intermediate levels of attraction. Location-related cues could therefore play a role in determining the level of task performance by ants and should be taken into consideration in threshold models of task allocation.

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

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


  1. Aron S, Beckers R, Deneubourg JL, Pasteels JM (1993) Memory and chemical communication in the orientation of two mass-recruiting ant species. Insectes Soc 40:369–380

  2. Beckers R, Deneubourg JL, Goss S (1993) Modulation of trail-laying in the ant Lasius niger (Hymeoptera, Formicidae) and its role in the collective selection of a food source. J Insect Behav 6:751–759

  3. Bernadou A, Busch J, Heinze J (2015) Diversity in identity: behavioral flexibility, dominance, and age polyethism in a clonal ant. Behav Ecol Sociobiol 69:1365–1375. https://doi.org/10.1007/s00265-015-1950-9

  4. Bernadou A, Czaczkes T, Heinze J (2018a) From inside to outside and back again: changing waste dump formation, defecation and worker localization in a clonal ant. Insectes Soc 65:133–140. https://doi.org/10.1007/s00040-017-0594-3

  5. Bernadou A, Schrader L, Pable J, Hoffacker E, Meusemann K, Heinze J (2018b) Stress and early experience underlie dominance status and division of labour in a clonal insect. Proc Roy Soc B-Biol Sci 285:20181468. https://doi.org/10.1098/rspb.2018.1468

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

  7. Besson M, Martin RJ (2005) Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. J Neurobiol 62:386–396. https://doi.org/10.1002/neu.20111

  8. Bockoven AA, Coates CJ, Eubanks MD (2017) Colony-level behavioural variation correlates with differences in expression of the foraging gene in red imported fire ants. Mol Ecol 26:5953–5960. https://doi.org/10.1111/mec.14347

  9. 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 Roy Soc B-Biol Sci 263:1565–1569. https://doi.org/10.1098/rspb.1996.0229

  10. Chapman B, Thain H, Coughlin J, Hughes W (2011) Behavioural syndromes at multiple scales in Myrmica ants. Anim Behav 82:391–397. https://doi.org/10.1016/j.anbehav.2011.05.019

  11. Czaczkes TJ, Castorena M, Schürch R, Heinze J (2017) Pheromone trail following in the ant Lasius niger: high accuracy and variability but no effect of task state. Physiol Entomol 42:91–97. https://doi.org/10.1111/phen.12174

  12. D’Eustacchio D, Solida L, Profico A, Centorame M, Grasso DA, Castracani C, Mori A, Fanfani A (2019) Tasks performed by different groups of foragers and regulation of foraging activity in the Mediterranean harvest ant Messor wasmanni (Hymenoptera, Formicidae). J Insect Behav 32:38–46. https://doi.org/10.1007/s10905-019-09710-3

  13. Deneubourg JL, Pasteels JM, Verhaeghe JC (1983) Probabilistic behaviour in ants: a strategy of errors? J Theor Biol 105:259–271. https://doi.org/10.1016/S0022-5193(83)80007-1

  14. Depickère S, Fresneau D, Detrain C, Deneubourg JL (2005) Marking as a decision factor in a choice of a new resting site in ants. Insect Soc 51:243–246. https://doi.org/10.1007/s00040-004-0739-z

  15. Detrain C, Deneubourg JL (2009) Social cues and adaptive foraging strategies in ants. In: Jarau S, Hrncir M (eds) Food exploitation by social insects: ecological, behavioral, and theoretical approaches. CRC Press, Boca Raton London New York, pp 29–52

  16. Detrain C, Pasteels JM (1991) Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant Pheidole pallidula. J Insect Behav 4:157–177. https://doi.org/10.1007/BF01054609

  17. Detrain C, Deneubourg JL, Pasteels JM (1999) Decision-making in foraging by social insects. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser Verlag, Basel, pp 331–354. https://doi.org/10.1007/978-3-0348-8739-7_18

  18. Devigne C, Detrain C (2002) Collective exploration and area marking in the ant Lasius niger. Insectes Soc 49:357–362. https://doi.org/10.1007/PL00012659

  19. Devigne C, Detrain C (2006) How does food distance influence foraging in the ant Lasius niger: the importance of home-range marking. Insectes Soc 53:46–55. https://doi.org/10.1007/s00040-005-0834-9

  20. Dolezal AG (2013) Division of labor is associated with age-independent changes in ovarian activity in Pogonomyrmex californicus harvester ants. J Insect Physiol 59:519–524. https://doi.org/10.1016/j.jinsphys.2013.02.008

  21. Dolezal AG, Brent CS, Hölldobler B, Amdam GV (2012) Worker division of labor and endocrine physiology are associated in the harvester ant, Pogonomyrmex californicus. J Exp Biol 215:454–460. https://doi.org/10.1242/jeb.060822

  22. Fahrbach SE, Moore D, Capaldi EA (1998) Experience-expectant plasticity in the mushroom bodies of the honeybee. Learn Mem 5:115–123. https://doi.org/10.1101/lm.5.1.115

  23. Giraldo YM, Traniello JFA (2014) Worker senescence and the sociobiology of aging in ants. Behav Ecol Sociobiol 68:1901–1919. https://doi.org/10.1007/s00265-014-1826-4

  24. Giraldo YM, Kamhi JF, Fourcassié V, Moreau M, Robson SKA, Rusakov A, Traniello JFA (2016) Lifespan behavioural and neural resilience in a social insect. Proc Roy Soc B-Biol Sci 283:20152603. https://doi.org/10.1098/rspb.2015.2603

  25. Gordon DM (2010) Ant encounters: interaction networks and collective behavior. Princeton University Press, Princeton NJ

  26. Gordon DM (2016) From division of labor to collective behavior of social insects. Behav Ecol Sociobiol 70:1101–1108. https://doi.org/10.1007/s00265-015-2045-3

  27. Gordon DG, Moreau M, Fourcassie V, Traniello JFA (2018) Limited size-related variation in behavioral performance among workers of the exceptionally polymorphic ant Pheidole rhea. Insectes Soc 65: 431-438 https://doi.org/10.1007/s00040-018-0629-4

  28. Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011–2019. https://doi.org/10.2307/2937655

  29. Grüter C, Czaczkes TJ, Ratnieks FLW (2011) Decision making in ant foragers (Lasius niger) facing conflicting private and social information. Behav Ecol Sociobiol 65:141–148. https://doi.org/10.1007/s00265-010-1020-2

  30. Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, Cambridge, MA

  31. Jeanson R, Weidenmüller A (2014) Interindividual variability in social insects - proximate causes and ultimate consequences. Biol Rev 89:671–687. https://doi.org/10.1111/brv.12074

  32. Kühn-Bühlmann S, Wehner R (2006) Age-dependent and task-related volume changes in the mushroom bodies of visually guided desert ants, Cataglyphis bicolor. J Neurobiol 66:511–521. https://doi.org/10.1002/neu.20235

  33. Larsen J, Nehring V, d’Ettorre P, Bos N (2016) Task specialization influences nestmate recognition ability in ants. Behav Ecol Sociobiol 70:1433–1440. https://doi.org/10.1007/s00265-016-2152-9

  34. Lenoir A, Depickère S, Devers S, Christidès JP, Detrain C (2009) Hydrocarbons in the ant Lasius niger: from the cuticle to the nest and home range marking. J Chem Ecol 35:913–921. https://doi.org/10.1007/s10886-009-9669-6

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

  36. Morgan ED (2009) Trail pheromones of ants. Physiol Entomol 34:1–17. https://doi.org/10.1111/j.1365-3032.2008.00658.x

  37. Moroń D, Witek M, Woyciechowski M (2008) Division of labour among workers with different life expectancy in the ant Myrmica scabrinodis. Anim Behav 75:345–350. https://doi.org/10.1016/j.anbehav.2007.06.005

  38. Muscedere ML, Traniello JF (2012) Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization. PLoSOne 7(1-12):e31618. https://doi.org/10.1371/journal.pone.0031618

  39. Muscedere M, Traniello J, Gronenberg W (2011) Coming of age in an ant colony: cephalic muscle maturation accompanies behavioral development in Pheidole dentata. Naturwissenschaften 98:783–793. https://doi.org/10.1007/s00114-011-0828-6

  40. Muscedere ML, Johnson N, Gillis BC, Kamhi JF, Traniello JFA (2012) Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata. J Comp Physiol A 198:219-227. https://doi.org/10.1007/s00359-011-0701-2

  41. Norman VC, Hughes WOH (2016) Behavioural effects of juvenile hormone and their influence on division of labour in leaf-cutting ant societies. J Exp Biol 219:8–11. https://doi.org/10.1242/jeb.132803

  42. Norman VC, Hoppé M, Hughes WOH (2014) Old and wise but not size: factors affecting threat response behaviour and nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Insectes Soc 61:289–296

  43. Oettler J, Johnson RA (2009) (2008). The old ladies of the seed harvester ant Pogonomyrmex Rugosus: foraging performed by two groups of workers. J Insect Behav 22:217–226. https://doi.org/10.1007/s10905-008-9167-7

  44. Oettler J, Nachtigal AL, Schrader L (2015) Expression of the foraging gene is associated with age polyethism, not task preference, in the ant Cardiocondyla obscurior. PLoS One 10(12):1–7. https://doi.org/10.1371/journal.pone.0144699

  45. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton, NJ

  46. Pamminger T, Foitzik S, Kaufmann KC, Schützler N, Menzel F (2014) Worker personality and its association with spatially structured division of labor. PLoS One 9(1): e79616, 1-8 https://doi.org/10.1371/journal.pone.0079616

  47. Powell S (2016) A comparative perspective on the ecology of morphological diversification in complex societies: nesting ecology and soldier evolution in the turtle ants. Behav Ecol Sociobiol 70:1075–1085. https://doi.org/10.1007/s00265-016-2080-8

  48. Ravary F, Lecoutey E, Kaminski G (2007) Individual experience alone can generate lasting division of labor in ants. Curr Biol 17:1308–1312. https://doi.org/10.1016/j.cub.2007.06.047

  49. Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665. https://doi.org/10.1146/annurev.en.37.010192.003225

  50. Robinson EJH (2009) Physiology as a caste-defining feature. Insectes Soc 56:1–6. https://doi.org/10.1007/s00040-008-1035-0

  51. Robinson EJH, Feinerman O, Franks NR (2012) Experience, corpulence and decision making in ant foraging. J Exp Biol 215:2653–2659. https://doi.org/10.1242/jeb.071076

  52. Robson SKA, ·Traniello JFA (2002) Transient division of labor and behavioral specialization in the ant Formica schaufussi. Naturwissenschaften 89:128–131. https://doi.org/10.1007/s00114-002-0300-8

  53. Schwander T, Rosset H, Chapuisat M (2005) Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol 59:215–222. https://doi.org/10.1007/s00265-005-0027-6

  54. Seid MA, Traniello JFA (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. https://doi.org/10.1007/s00265-006-0207-zz

  55. Sempo G, Depickère S, Detrain C (2006) Spatial organization in a dimorphic ant: caste specificity of clustering patterns and area marking. Behav Ecol 17:642–650. https://doi.org/10.1093/beheco/ark011

  56. Silberman RE, Gordon D, Ingram KK (2016) Nutrient stores predict task behaviors in diverse ant species. Insectes Soc 63:299–307. https://doi.org/10.1007/s00040-016-0469-z

  57. Tschinkel WR (2011) The Organization of Foraging in the fire ant, Solenopsis invicta. J Insect Sci 11:1–30. https://doi.org/10.1673/031.011.0126

  58. Von Thienen W, Metzler D, Choe DH, Witte V (2014) Pheromone communication in ants: a detailed analysis of concentration dependent decisions in three species. Behav Ecol Sociobiol 68:1611–1627. https://doi.org/10.1007/s00265-014-1770-3

  59. Waddington SJ, Santorelli LA, Ryan FR, Hughes WHO (2011) Genetic polyethism in leaf-cutting ants. Behav Ecol 21:1165–1169. https://doi.org/10.1093/beheco/arq128

  60. Wagle M, Nguyen J, Lee S, Zzitlen N, Guo S (2017) Heritable natural variation of an anxiety like behavior in larval zebrafish. J Neurogenet 31:138–148. https://doi.org/10.1080/01677063.2017.1343827

  61. Whitfield CW, Cziko AM, Robinson GE (2003) Gene expression profiles in the brain predict behavior in individual honey bees. Science 302:296–299. https://doi.org/10.1126/science.1086807

  62. Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238–240. https://doi.org/10.1038/364238a0

  63. Wnuk A, Wiater M, Gidzinska EJ (2011) Effect of past and present behavioural specialization on brain levels of biogenic amines in workers of the red wood ant Formica polyctena. Physiol Entomol 36:54–61. https://doi.org/10.1111/j.1365-3032.2010.00762.x

  64. Wright CM, Lichtenstein JLL, Doering GN, Pretorius J, Meunier J, Pruitt JN (2019) Collective personalitites: present knowledge and new frontiers. Behav Ecol Sociobiol 73. https://doi.org/10.1007/s00265-019-2639-2

Download references


Claire Detrain is a Research Director from the Belgian National Fund for Scientific Research (F.N.R.S) and Hugo Pereira is supported by a Belgian PhD grant from the F.R.I.A. (Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture). The authors warmly thank Nell Foster for proofreading the English as well as two anonymous referees and the editor for providing constructive comments on the manuscript.


Hugo Pereira was financially supported by a Belgian PhD grant from the F.R.I.A. (Fonds pour la formation à la Recherche dans l’Industrie et dans l’Agriculture). Claire Detrain is Research Director from the Belgian National Fund for Scientific Research (F.N.R.S).

Author information

Correspondence to Claire Detrain.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by W. Hughes

Electronic supplementary material


(DOCX 1000 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Detrain, C., Pereira, H. & Fourcassié, V. Differential responses to chemical cues correlate with task performance in ant foragers. Behav Ecol Sociobiol 73, 107 (2019). https://doi.org/10.1007/s00265-019-2717-5

Download citation


  • Ants
  • Foraging
  • Division of labor
  • Social cues
  • Colonial marking
  • Trail pheromone