Skip to main content
SpringerLink
Log in

Opportunist slave-making ants Myrmoxenus ravouxi discriminate different host species from a non-host species

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Slave-making ants exploit the worker force of host colonies permanently and have to make recurrent raids in order to replenish the slave’s stock. Some of these parasite species exploit different host species and few studies so far have been devoted to host species recognition mechanisms. Here, we tried to determine if opportunist slave-making ants using different host species rely on innate or experience-induced preferences to discriminate host from non-host species. We show that Myrmoxenus ravouxi slave-making workers are not only more aggressive toward heterocolonial host and potential host species workers when compared with non-host species workers, but also toward heterocolonial host workers than toward heterocolonial conspecifics. Moreover, M. ravouxi workers display more antennations and contacts toward the heterocolonial host species when compared with the non-host species. We also show that they do not discriminate between homocolonial and heterocolonial conspecifics. Together, our results suggest that this opportunistic slave-making ant species may have a complex social recognition template based on both innate and experience-based mechanisms.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alloway T.M. 1980. The origins of slavery in leptothoracine ants (Hymenoptera: Formicidae). Am. Nat. 115: 247-261

    Google Scholar 

  • Baur A., Chalwatzis N., Buschinger A. and Zimmermann F.K. 1995. Mitochondrial DNA sequences reveal close relationships between social parasitic ants and their host species. Curr. Genet. 28: 242-247

    Google Scholar 

  • Beibl J., Stuart R.J., Heinze J. and Foitzik S. 2005. Six origins of slavery in formicoxenine ants. Insect. Soc. 52: 291-297

    Google Scholar 

  • Blatrix R. and Herbers J.M. 2003. Coevolution between slave-making ants and their hosts: host specificity and geographical variation. Mol. Ecol. 12: 2809-2816

    Google Scholar 

  • Bonavita-Cougourdan A., Rivière G., Provost E., Bagnères A.G., Roux M., Dusticier G. and Clément J.L. 1996. Selective adapation of the cuticular hydrocarbon profiles of the slave-making ants Polyergus rufescens Latr. and their Formica rufibarbis Fab. and F. cunicularia Latr. slaves. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 113: 313-329

  • Bonavita-Cougourdan A., Bagnères A.G., Provost E., Dusticier G. and Clément J.L. 1997. Plasticity of the cuticular hydrocarbon profile of the slave-making ant Polyergus rufescens depending on the social environment. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 116: 287-302

    Google Scholar 

  • Brandt M. and Foitzik S. 2004. Community context and specialization influence coevolution between a slavemaking ant and its hosts. Ecology 85: 2997-3009

    Google Scholar 

  • Brandt M., Heinze J., Schmitt T. and Foitzik S. 2005. A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J. Evol. Biol. 18: 576-586

    Google Scholar 

  • Buschinger A., Ehrhardt W. and Winter U. 1980. The organization of slave raids in dulotic ants - a comparative study (Hymenoptera; Formicidae). Z. Tierpsychol. 53: 245-264

    Google Scholar 

  • Buschinger A. and Winter U. 1983. Population studies of the dulotic ant, Epimyrma ravouxi, and the degenerate slavemaker, E. kraussei (Hymenoptera: Formicidae). Entomol. Gen. 8: 251-266

  • Buschinger A. 1986. Evolution of social parasitism in ants. Trends Ecol. Evol. 1: 155-160

    Google Scholar 

  • Buschinger A. 1989. Evolution, speciation, and inbreeding in the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). J. Evol. Biol. 2: 265-283

    Google Scholar 

  • Buschinger A. 1997. Socially parasitic formicoxenine ants from Western Europe—a review (Hymenoptera, Formicidae). In: Proc. Int. Coll. Social Insects (Kipyatkov V.E., Ed), vol 3-4. Russian Language Section of the IUSSI, Socium, St. Petersburg, pp 1-9

  • Buschinger A. 2009. Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol. News 12: 219-235

    Google Scholar 

  • Cao T.T. and Dornhaus A. 2012. Ants use pheromone markings in emigrations to move closer to food-rich areas. Insect. Soc. 59: 87-92

    Google Scholar 

  • Crosland M.W.J. 1989. Kin recognition in the ant Rhytidoponera confusa. I. Environmental odour. Anim. Behav. 37: 912-919

    Google Scholar 

  • Crozier R.H. and Dix M.W. 1979. Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav. Ecol. Sociobiol. 4: 217-224

    Google Scholar 

  • d’Ettorre P., Mondy N., Lenoir A. and Errard C. 2002. Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature. Proc. R. Soc. London B Biol. Sci. 269: 1911-1918

    Google Scholar 

  • Emery C. 1909. Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol. Centralbl. (Berlin) 29: 352-362

    Google Scholar 

  • Errard C. 1994. Development of interspecific recognition behavior in the ants Manica rubida and Formica selysi (Hymenoptera: Formicidae) reared in mixed-species groups. J. Insect Behav. 7: 83-99

    Google Scholar 

  • Errard C. and Hefetz A. 1997. Label familiarity and discriminatory ability of ants reared in mixed groups. Insect. Soc. 44: 189-198

    Google Scholar 

  • Errard C., Hefetz A. and Jaisson P. 2006. Social discrimination tuning in ants: template formation and chemical similarity. Behav. Ecol. Sociobiol. 59: 353-363

    Google Scholar 

  • Fischer B. and Foitzik S. 2004. Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system. J. Evol. Biol. 17: 1026-1034

    Google Scholar 

  • Fischer-Blass B., Heinze J. and Foitzik S. 2006. Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species. Mol. Ecol. 15: 863-872

    Google Scholar 

  • Foitzik S. and Heinze J. 1998. Nest site limitation and colony take over in the ant, Leptothorax nylanderi. Behav. Ecol. 9: 367-375

    Google Scholar 

  • Foitzik S., Deheer C.J., Hunjan D.N. and Herbers J.M. 2001. Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts. Proc. R. Soc. London B Biol. Sci. 268: 1139-1146

    Google Scholar 

  • Foitzik S., Fischer B. and Heinze J. 2003. Arms-races between social parasites and their hosts: Geographic patterns of manipulation and resistance. Behav. Ecol. 14: 80-88

    Google Scholar 

  • Franks N., Blum M., Smith R.K. and Allies A.B. 1990. Behavior and chemical disguise of cuckoo ant Leptothorax kutteri in relation to its host Leptothorax acervorum. J. Chem. Ecol. 16: 1431-1444

    Google Scholar 

  • Franks N.R, Dornhaus A., Hitchcock G., Guillem R., Hooper J. and Webb C. 2007a. Avoidance of conspecific colonies during nest choice by ants. Anim. Behav. 73: 525-534

  • Franks N.R, Hooper J.W, Dornhaus A., Aukett P.J, Hayward A.L. and Berghoff S.M. 2007b. Reconnaissance and latent learning in ants. Proc. R. Soc. London B Biol. Sci. 274: 1505-1509

  • Hare J.F. and Alloway T.M. 2001. Prudent Protomognathus and despotic Leptothorax duloticus: differential costs of ant slavery. Proc. Natl Acad. Sci. U.S.A. 98: 12093-12096

    Google Scholar 

  • Heinze J., Foitzik S., Hippert A. and Hölldobler B. 1996. Apparent dear-enemy phenomenon and environment-based recognition cues in the ant Leptothorax nylanderi. Ethology 102: 510-522

    Google Scholar 

  • Isingrini M., Lenoir A. and Jaisson P. 1985. Preimaginal learning as a basis of colony-brood recognition in the ant Cataglyphis cursor. Proc. Natl Acad. Sci. U.S.A. 82: 8545-8547

  • Kaib M., Heinze J. and Ortius D. 1993. Cuticular hydrocarbons profiles in the slave-making ant Harpogoxenus sublaevis and its hosts. Naturwissenschaften 80: 281-285

    Google Scholar 

  • Knaden M. and Wehner R. 2003. Nest defense and conspecific enemy recognition in the desert ant Cataglyphis fortis. J. Insect Behav. 16: 717-730

    Google Scholar 

  • Kronauer D.J.C., Gadau J. and Hölldobler B. 2003. Genetic evidence for intra- and interspecific slavery in honey ants (genus Myrmecocystus). Proc. R. Soc. London B Biol. Sci. 270: 805-810

    Google Scholar 

  • Le Moli F., Grasso D.A, d’Ettorre P. and Mori A. 1993. Intraspecific slavery in Polyergus rufescens Latr. (Hymenoptera, Formicidae): field and laboratory observations. Insect. Soc. 40: 433-437

    Google Scholar 

  • Lenoir A., Fresneau D., Errard C. and Hefetz A. 1999. Individuality and colonial identity in ants: the emergence of the social representation concept. In: Information Processing in Social Insects (Detrain C., Deneubourg J.L. and Pasteels J., Eds), Birkhäuser Verlag, Basel. pp 219-237

  • Lenoir A., D’Ettorre P., Errard C. and Hefetz A. 2001. Chemical ecology and social parasitism in ants. Annu. Rev. Entomol. 46: 573-599

    Google Scholar 

  • Liang D. and Silverman J. 2000. “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87: 412-416

    Google Scholar 

  • Parker J.D. and Rissing S.W. 2002. Molecular evidence for the origin of workerless social parasites in the ant genus Pogonomyrmex. Evolution 56: 2017-2028

    Google Scholar 

  • Pollock G.B. and Rissing S. W. 1989. Intraspecific brood raiding, territoriality, and slavery in ants. Am. Nat. 133: 61-70

    Google Scholar 

  • Reeve H.K. 1989. The evolution of conspecific acceptance thresholds. Am. Nat. 133: 407-435

    Google Scholar 

  • Sanada-Morimura S., Minai M., Yokoyama M., Hirota T., Satoh T. and Obara Y. 2003. Encounter-induced hostility to neighbors in the ant Pristomyrmex pungens. Behav. Ecol. 14: 713-718

  • Schumann R.D. 1992: Raiding behavior of the dulotic ant Chalepoxenus muellerianus (Finzi) in the field (Hymenoptera: Formicidae, Myrmicinae). Insect. Soc. 39: 325-333

  • Schumann R.D. and Buschinger A. 1995. Imprinting effects on host-selection behavior of slave-raiding Chalepoxenus muellerianus (Finzi) workers (Hymenoptera: Formicidae). Ethology 99: 243-251

    Google Scholar 

  • Seifert B. 2007. Die Ameisen Mittel- und Nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, Tauer

  • Soroker V., Vienne C., Hefetz A. and Nowbahari E. 1994. The postpharyngeal gland as a “Gestalt” organ for nestmate recognition in the ant Cataglyphis niger. Naturwissenschaften 81: 510-513

    Google Scholar 

  • Soroker V., Lucas C., Simon T., Fresneau D., Durand J.L. and Hefetz A. 2003. Hydrocarbon distribution and colony odour homogenisation in Pachycondyla apicalis. Insect. Soc. 50: 212-217

    Google Scholar 

  • Stuart R.J. and Alloway T.M. 1982. Territoriality and the origin of slave raiding in leptothoracine ants. Science 215: 1262-1263

    Google Scholar 

  • Sturgis S.J. and Gordon D.M. 2012. Nestmate recognition in ants (Hymenoptera: Formicidae): a review. Myrmecol. News 16: 101-110

    Google Scholar 

  • Sumner S., Aanen D.K., Delabie J. and Boomsma J.J. 2004. The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Insect. Soc. 51: 37-42

    Google Scholar 

  • Thompson J.N. 1994. The Coevolutionary Process. The University of Chicago Press, Chicago

  • van Zweden J.S., Dreier S. and d’Ettorre P. 2009a. Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J. Insect Physiol. 55: 158-163

  • van Zweden J.S., Heinze J., Boomsma J.J. and d'Ettorre P. 2009b. Ant queen egg-marking signals: matching deceptive laboratory simplicity with natural complexity. PLoS ONE 4: e4718

  • van Zweden J.S. and d’Ettorre P. 2010. Nestmate recognition in social insects and the role of hydrocarbons. In: Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology (Blomquist G.J. and Bagnères A.G., Eds). Cambridge University Press, Cambridge. pp 222-243

  • Wilson E.O. 1975. Slavery in ants. Sci. Am. 232: 32-36

    Google Scholar 

  • Winter U. 1979. Epimyrma goesswaldi Menozzi, eine sklavenhaltende Ameise. Naturwissenschaften 66: 581-582

    Google Scholar 

Download references

Acknowledgments

Olivier Delattre was supported by the French Ministry of Research. Nicolas Châline and Stéphane Chameron were supported by the ANR project SEUILS ANR-09-JCJC-0031.

Author information

Authors and Affiliations

  1. Laboratoire d’Ethologie Expérimentale et Comparée, EA 4443, Université Paris 13, 99 avenue Jean-Baptiste Clément, 93430, Villetaneuse, France

    O. Delattre, N. Châline, S. Chameron, E. Lecoutey & P. Jaisson

Authors
  1. O. Delattre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Châline
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Chameron
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Lecoutey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Jaisson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. Delattre.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Delattre, O., Châline, N., Chameron, S. et al. Opportunist slave-making ants Myrmoxenus ravouxi discriminate different host species from a non-host species. Insect. Soc. 60, 7–13 (2013). https://doi.org/10.1007/s00040-012-0257-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-012-0257-3

Keywords

Search

Navigation