Behavioral Ecology and Sociobiology

, Volume 63, Issue 11, pp 1635–1641 | Cite as

Hierarchical perception of fertility signals and nestmate recognition cues in two dolichoderine ants

Original Paper

Abstract

In social insects, queens are likely to “honestly” inform their nestmates of their presence and fertility status through pheromonal communication. Cuticular hydrocarbons (CHCs) have been reported to be effective nestmate discriminators and strongly suspected to act as fertility signals, at least in some species. The use of the same chemical bouquet (i.e., the CHC profile) to convey two fundamentally different information seems puzzling. However, a recent threshold model proposes a hierarchy in the discriminating processes, i.e., fertility signals can only be perceived if nestmate recognition has been reached (Le Conte and Hefetz, Annu Rev Entomol 53:523–542, 2008). Here, we developed a simple behavioral bioassay based on chemical recruitment toward a queen placed outside the nest in two dolichoderine ants (Linepithema humile and Tapinoma erraticum), which allowed us to investigate the interplay between fertility signaling and colonial recognition. Using queen corpses of various origins (nestmates or aliens) and physiological states (fertile or infertile; mated or unmated), we demonstrated that nestmate recognition cues clearly override fertility signals under our experimental conditions. Indeed, while nestmate infertile queens were largely ignored by the workers, nestmate fertile queens (mated or not) induced worker recruitment, whereas alien fertile queens did not and were aggressed by the workers.

Keywords

Queen pheromone Fertility Nestmate recognition Virgin egg-laying queens Queen retrieval 

References

  1. Aron S (1992) Queen retrieval in the Argentine ant. Experientia 48:694–697CrossRefGoogle Scholar
  2. Beckers R, Goss S, Deneubourg JL, Pasteels JM (1989) Colony size, communication and ant foraging strategy. Psyche 96:239–256CrossRefGoogle Scholar
  3. Berndt KP, Nitschmann J (1979) The physiology of reproduction in the Pharaoh’s ant (Monomorium pharaonis L.). 2. The unmated queens. Insect Soc 26:137–145CrossRefGoogle Scholar
  4. Boulay R, Hefetz A, Cerdá X, Devers S, Francke W, Twele R, Lenoir A (2007) Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size. Behav Ecol Sociobiol 61:1531–1541CrossRefGoogle Scholar
  5. Cariou A, Passera L (1990) Données préliminaires sur le pouvoir attractif des reines de la fourmi d’Argentine, Iridomyrmex humilis (Mayr). Actes Coll Insect Soc 6:203–210Google Scholar
  6. Cariou-Etienne A, Passera L (1993) Queen power in relation to age and mating status in the Argentine ant Iridomyrmex humilis (Mayr). Insect Soc 40:87–94CrossRefGoogle Scholar
  7. Crozier RH, Dix MW (1979) Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav Ecol Sociobiol 4:217–224CrossRefGoogle Scholar
  8. de Biseau JC, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Insect Physiol 50:585–593PubMedCrossRefGoogle Scholar
  9. Dietemann V, Peeters C, Hölldobler B (2005) Role of the queen in regulating reproduction in the bulldog ant Myrmecia gulosa: control or signalling? Anim Behav 69:777–784CrossRefGoogle Scholar
  10. Fletcher DJC, Blum MS (1983) The inhibitory pheromone of queen fire ants: effects of disinhibition on dealation and oviposition by virgin queens. J Comp Physiol A Neuroethol Sens Neur Behav Physiol 153:467–475CrossRefGoogle Scholar
  11. Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci U S A 99:6075–6079PubMedCrossRefGoogle Scholar
  12. Glancey BM, Lofgren CS, Rocca JR, Tumlinson JH (1983) Behavior of disrupted colonies of Solenopsis invicta towards queens and pheromone-treated surrogate queens placed outside the nest. Sociobiol 7:283–288Google Scholar
  13. Greene MJ, Gordon DM (2007) Structural complexity of chemical recognition cues affect the perception of group membership in the ants Linepithema humile and Aphaenogaster cockerelli. J Exp Biol 210:897–905PubMedCrossRefGoogle Scholar
  14. Hannonen M, Sledge MF, Turillazi S, Sundström L (2002) Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim Behav 64:477–485CrossRefGoogle Scholar
  15. Hefetz A (2007) The evolution of hydrocarbon pheromone parsimony in ants (Hymenoptera: Formicidae)—interplay of colony odor uniformity and odor idiosyncrasy. A review. Myrmecol News 10:59–68Google Scholar
  16. Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant. Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65CrossRefGoogle Scholar
  17. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393PubMedCrossRefGoogle Scholar
  18. Keller L, Nonacs P (1993) The role of queen pheromones in social insects—queen control or queen signal? Anim Behav 45:787–794CrossRefGoogle Scholar
  19. Le Conte Y, Hefetz A (2008) Primer pheromone in social hymenoptera. Annu Rev Entomol 53:523–542PubMedCrossRefGoogle Scholar
  20. Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants. In: Detrain C, Deneubourg JL, Pasteels J (eds) Information processing in social insects. Birkhauser, Basel, pp 219–237Google Scholar
  21. Lommelen E, Johnson CA, Drijfhout FP, Billen J, Wenseleers T, Gobin B (2006) Cuticular hydrocarbons provide reliable cues of fertility in the ant Gnamptogenys striatula. J Chem Ecol 32:2023–2034PubMedCrossRefGoogle Scholar
  22. Meudec M (1979) Comportement d'émigration chez la fourmi Tapinoma erraticum (Form. Dolichoderinae). Un exemple de régulation sociale. PhD thesis, University of Tours (France)Google Scholar
  23. Meudec M (1982) Some aspects of individual behaviour during nest moving in the ant Tapinoma erraticum. Behav Proc 7:377–382CrossRefGoogle Scholar
  24. Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530Google Scholar
  25. Ortius D, Heinze J (1999) Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151–159CrossRefGoogle Scholar
  26. Passera L (1969) Biologie de la reproduction chez Plagiolepis pygmaea Latr. et ses deux parasites sociaux Plagiolepis grassei Le Mas. et Plagiolepis xene St. (Hymenoptera : Formicidae). Ann Sci Nat Zool Biol Anim (12ème série) 11:327–482Google Scholar
  27. Passera L, Aron S (1993) Factors controlling dealation and egg laying in virgin queens of the Argentine ant Linepithema humile (Mayr) (=Iridomyrmex humilis). Psyche 100:51–63CrossRefGoogle Scholar
  28. Passera L, Keller L, Suzzoni JP (1988a) Control of brood male production in the Argentine ant Iridomyrmex humilis (Mayr). Insect Soc 35:19–33CrossRefGoogle Scholar
  29. Passera L, Keller L, Suzzoni JP (1988b) Queen replacement in dequeened colonies of the Argentine ant Iridomyrmex humilis (Mayr). Psyche 95:59–65CrossRefGoogle Scholar
  30. Peeters C (1991) The occurrence of sexual reproduction among ant workers. Biol J Linn Soc 44:141–152CrossRefGoogle Scholar
  31. Peeters C, Liebig J (2009) Fertility signaling as a general mechanism of regulating reproductive division of labour in ants. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to socio-complexity. Harvard University Press, CambridgeGoogle Scholar
  32. Sommer K, Hölldobler B (1995) Colony founding by queen association and determinants of reduction in queen number in the ant Lasius niger. Anim Behav 50:287–294CrossRefGoogle Scholar
  33. Torres CW, Brandt M, Tsutsiu ND (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insect Soc 54:363–373CrossRefGoogle Scholar
  34. Vander Meer RK, Alonso LE (1998) Pheromone directed behavior in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, pp 159–192Google Scholar
  35. Vander Meer RK, Glancey BM, Lofgren CS, Glover A, Tumlinson JH, Rocca J (1980) The poison sac of red imported fire ant queens: source of a pheromone attractant. Ann Entomol Soc Am 73:609–612Google Scholar
  36. Vargo EL (1998) Primer pheromones in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, pp 293–313Google Scholar
  37. Vargo EL (1999) Reproductive development and ontogeny of queen pheromone production in the fire ant Solenopsis invicta. Physiol Entomol 24:370–376CrossRefGoogle Scholar
  38. Vargo EL, Hulsey CD (2005) Multiple glandular origins of queen pheromones in the fire ant Solenopsis invicta. J Insect Physiol 46:1151–1159CrossRefGoogle Scholar
  39. Vargo EL, Passera L (1991) Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr). Behav Ecol Sociobiol 28:161–169CrossRefGoogle Scholar
  40. Vásquez GM, Silverman J (2008) Queen acceptance and the complexity of nestmate discrimination in the Argentine ant. Behav Ecol Sociobiol 62:537–548CrossRefGoogle Scholar
  41. Vásquez GM, Schal C, Silverman J (2008) Cuticular hydrocarbons as queen adoption cues in the invasive Argentine ant. J Exp Biol 211:1249–1256PubMedCrossRefGoogle Scholar
  42. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Behavioral and Evolutionary Ecology, Faculty of SciencesUniversité Libre de BruxellesBrusselsBelgium

Personalised recommendations