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The Social Integration of a Myrmecophilous Spider Does Not Depend Exclusively on Chemical Mimicry

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Abstract

Numerous animals have evolved effective mechanisms to integrate into and exploit ant societies. Chemical integration strategies are particularly widespread among ant symbionts (myrmecophiles), probably because social insect nestmate recognition is predominantly mediated by cuticular hydrocarbons (CHCs). The importance of an accurate chemical mimicry of host CHCs for social acceptance recently has been demonstrated in a myrmecophilous silverfish. In the present study, we investigated the role of chemical mimicry in the myrmecophilous spider Gamasomorpha maschwitzi that co-occurs in the same host, Leptogenys distinguenda, as the silverfish. To test whether spiders acquire mimetic CHCs from their host or not, we transferred a stable isotope-labeled hydrocarbon to the cuticle of workers and analyzed the adoption of this label by the spiders. We also isolated spiders from hosts in order to study whether this affects: 1) their chemical host resemblance, and 2) their social integration. If spiders acquired host CHCs, rather than biosynthesizing them, they would be expected to lose these compounds during isolation. Spiders acquired the labeled CHC from their host, suggesting that they also acquire mimetic CHCs, most likely through physical contact. Furthermore, isolated spiders lost considerable quantities of their CHCs, indicating that they do not biosynthesize them. However, spiders remained socially well integrated despite significantly reduced chemical host similarity. We conclude that G. maschwitzi depends less on chemical mimicry to avoid recognition and aggressive rejection than the silverfish previously studied, suggesting that the two myrmecophiles possess different adaptations to achieve social integration.

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References

  • Akino, T. 2008. Chemical strategies to deal with ants: a review of mimicry, camouflage, propaganda, and phytomimesis by ants (Hymenoptera:Formicidae) and other arthropods. Myrmecol. News 11:173–181

    Google Scholar 

  • Allan, R. A., Capon, R. J., Brown, W.V., and Elgar, M.A. 2002. Mimicry of host cuticular hydrocarbons by salticid spider Cosmophasis bitaeniata that preys on larvae of tree ants Oecophylla smaragdina. J. Chem. Ecol. 28:835–848

    Article  PubMed  CAS  Google Scholar 

  • Anderson, M. J., Gorley, R. N., and Clarke, K. R. 2008. PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Baer, B., Den Boer, S. P. A., Kronauer, D. J. C., Nash, D.R., and Boomsma, J. J. 2009. Fungus gardens of the leafcutter ant Atta colombica function as egg nurseries for the snake Leptodeira annulata. Insectes Soc. 56:289–291

    Article  Google Scholar 

  • Bagnères, A.-G., and Lorenzi, M. 2010. Chemical deception/mimicry using cuticular hydrocarbons. in: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: Biology, Biochemistry and Chemical ecology. Cambridge University Press, New York, USA

  • Bates, H.W. 1862. Contributions to an insect fauna of the Amazon Valley. Lepidoptera: Heliconidae. Trans. Linn. Soc. 23:495–566

    Article  Google Scholar 

  • Bauer, S., Boehm, M., Witte, V., and Foitzik, S. 2010. An ant social parasite in-between two chemical disparate host species. Evol. Ecol. 24:317–332

    Article  Google Scholar 

  • Brower, L. P. 1988. Mimicry and the evolutionary process. Amer. Nat. 131: Supplement S1-S121

    Article  Google Scholar 

  • Ceccarelli, F. S. 2007. Contact between Myrmarache (Araneae: Salticidae) and ants. Bull. Br. Arachnol. Soc. 14:54–58

    Google Scholar 

  • Cushing, P. E. 1997. Myrmecomorphy and myrmecophily in spiders: a review. Florida Entomol. 80:165–193

    Article  Google Scholar 

  • Dettner, K. and Liepert, C. 1994. Chemical mimicry and camouflage. Annu. Rev. Entomol. 39:129–154

    Article  CAS  Google Scholar 

  • Emery, C. 1887. Catalogo dello formiche esistenti nelle collezioni del Museo Civico. Gen Insect Fasc 118:1–124

    Google Scholar 

  • Fisher, R. A. 1927. On some objections to mimicry theory: statistical and genetic. Trans. Ent. Soc. London 75:269–278

    Article  Google Scholar 

  • Gotwald, W. H. Jr. 1995. Army Ants: The Biology of Social Predation. Cornell University Press, New York

    Google Scholar 

  • Hölldobler, B. and Carlin, N. F. 1989. Colony founding, queen control and worker reproduction in the ant Aphaenogaster (=Novomessor) cockerelli (Hymenoptera: Formicidae). Psyche 96:131–151

    Article  Google Scholar 

  • Hölldobler, B. and Wilson, E.O. 1990. The Ants. Harvard University Press, Cambridge

    Google Scholar 

  • Kistner, D. H. 1979. Social and evolutionary significance of social insect symbionts. pp 339–413 in: Hermann HR (ed) Social insects. Academic Press, New York.

    Google Scholar 

  • Kroiss, J., Schmitt, T., and Strohm, E. 2009. Low level of cuticular hydrocarbons in a parasitoid of a solitary digger wasp and its potential for concealment. J. Entomol. Sci. 12:9–16

    Article  Google Scholar 

  • Kronauer, D. J. C. 2009. Recent advances in army ant biology (Hymenoptera: Formicidae). Myrmecol. News 12:51–65

    Google Scholar 

  • Lambardi, D., Dani, F.R., Turillazzi, S., and Boomsma, J. J. 2007. Chemical mimicry in an incipient leaf-cutting ant social parasite. Behav. Ecol. Sociobiol. 61:843–851

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lenoir, A., Malosse, C., and Yamaoka, R. 1997. Chemical mimicry between parasitic ants of the genus Formicoxenus and their host Myrmica (Hymenoptera, Formicidae). Biochem. Syst. Ecol. 25:379–389

    Article  CAS  Google Scholar 

  • Mendes, L., Von Beeren, C., and Witte, V. 2011. Malayatelura ponerophila - a new genus and species of silverfish (Zygentoma, Insecta) from Malaysia, living in Leptogenys army-ant colonies (Formicidae). Dtsch. Ent. Z. 58:193–200

    Article  Google Scholar 

  • Müller, J. 1878. Über die Vortheile der Mimikry bei Schmetterlingen. Zoolog. Anz. 1: 54–55

    Google Scholar 

  • Nash, D. R., Als, T. D., Maile, R., Jones, G. R., and Boomsma, J. J. 2008. A mosaic of chemical coevolution in a large blue butterfly. Science 319:88–90

    Article  PubMed  CAS  Google Scholar 

  • Nash, D. R., and Boomsma, J. J. 2008. Communiction between hosts and social parasites. in: d'Ettorre P, Hughes DP (eds) Sociobiology of communication an interdisciplinary approach. Oxford University Press, New York

    Google Scholar 

  • Nelson, X. J. 2011. A predator’s perspective of the accuracy of ant mimicry in spiders. Psyche 2012; doi:10.1155/2012/168549

  • Ruxton, G. D., Sheratt, T., and Speed, M. 2004. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford University Press, New York

    Google Scholar 

  • Steghaus-Kovac, S. 1994. Wanderjäger im Regenwald- Lebensstrategien im Vergleich: Ökologie und Verhalten südostasiatischer Ameisenarten der Gattung Leptogenys (Hymenoptera: Formicidae: Ponerinae). Dissertation, University Frankfurt, Germany

  • Steiger, S., Schmitt, T., and Schäfer, H. M. 2011. The origin and dynamic evolution of chemical information transfer. Proc. R. Soc. B. 278:970–979

    Article  PubMed  Google Scholar 

  • Stein, S. E. 1999. An Integrated Method for Spectrum Extraction and Compound Identification from GC/MS Data. J. Am. Soc. Mass Spectrom. 10:770–781

    Article  CAS  Google Scholar 

  • Symonds, M. R. E. and Elgar, M. A. 2008. The evolution of pheromone diversity. Trends Ecol. Evol. 23:220–228

    Article  PubMed  Google Scholar 

  • Tanner, C. J. and Adler, F. R. 2009. To fight or not to fight: context-dependent interspecific aggression in competing ants. Anim. Behav. 77:297–305

    Article  Google Scholar 

  • Van Zweden, J. S. and D’ettorre, P. 2010. Nestmate recognition in social insects and the role of hydrocarbons. pp 222–243 in: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: Biology, Biochemistry and Chemical Ecology. Cambridge University Press, New York.

    Chapter  Google Scholar 

  • Vander Meer, R.K., Jouvenaz, D. P., and Wojcik, D. P. 1989. Chemical mimicry in a parasitoid (Hymenoptera: Eucharitidae) of fire ants (Hymenoptera: Formicidae). J. Chem. Ecol. 15:2247–2261

    Article  Google Scholar 

  • VANDER MEER, R.K. and WOJCIK, D. P. 1982. Chemical mimicry in the myrmecophilous beetle Myrmecaphodius excavaticollis. Science 218:806–808

    Article  PubMed  CAS  Google Scholar 

  • Von Beeren, C., Maruyama, M., Hashim, R., and Witte, V. 2011a. Differential host defense against multiple parasites in ants. Evol. Ecol. 25:259–276

    Article  Google Scholar 

  • Von Beeren, C., Pohl, S., and Witte, V. 2012. On the use of adaptive resemblance terms in chemical ecology. Psyche, Article ID 635761, doi:10.1155/2012/635761

  • Von Beeren, C., Schulz, S., Hashim, R., and Witte, V. 2011b. Acquisition of chemical recognition cues facilitates integration into ant societies. BMC Ecology 11:30

    Article  PubMed  Google Scholar 

  • Wasmann, E. 1895. Die Ameisen-und Termitengäste von Brasilien. I. Teil. Mit einem Anhange von Dr. August Forel. Verh K K Zool Bot Ges Wien 45:137–179

    Google Scholar 

  • Wickler, W. 1968. Mimikry. Nachahmung und Täuschung in der Natur. Kindlers Universitäts Bibliothek, München

    Google Scholar 

  • Wilson, E. O. 1990. Success and dominance in ecosystems: the case of the social insects. Excellence in ecology, 2. Ecology Institute, Oldendorf/Luhe

    Google Scholar 

  • Witte, V., Foitzik, S., Hashim, R., Maschwitz, U., and Schulz, S. 2009. Fine tuning of social integration by two myrmecophiles of the ponerine army ant, Leptogenys distinguenda. J. Chem. Ecol. 35:355–367

    Article  PubMed  CAS  Google Scholar 

  • Witte, V., Hänel, H., Weissflog, A., Hashim, R., and Maschwitz, U. 1999. Social integration of the myrmecophilic spider Gamasomorpha maschwitzi (Araneae: Oonopidae) in colonies of the South East Asian army ant, Leptogenys distinguenda (Formicidae: Ponerinae). Sociobiology 34:145–159

    Google Scholar 

  • Witte, V., Leingärtner, A., Sabaß, L., Hashim, R., and Foitzik, S. 2008. Symbiont microcosm in an ant society and the diversity of interspecific interactions. Anim. Behav. 76:1477–1486

    Article  Google Scholar 

  • Wunderlich, J. 1994. Beschreibung bisher unbekannter Spinnenarten und -gattungen aus Malaysia und Indonesien (Arachnida: Araneae: Oonopidae, Tetrablemmidae, Telemidae, Pholcidae, Linyphiidae, Nesticidae, Theridiidae und Dictynidae). Beiträge Araneologie 4:559–579

    Google Scholar 

Download references

Acknowledgements

We thank the behavioral ecology group at the LMU Munich for helpful comments on the manuscript, with special thanks to Sebastian Pohl and Andrew Bruce. Many thanks also to Sofia Lizon à l’Allemand, Max Kölbl, Magdalena Mair, and Deborah Schweinfest for assistance in the field. We are grateful for financial support from the DFG (Deutsche Forschungsgemeinschaft, project WI 2646/3).

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Correspondence to Volker Witte.

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von Beeren, C., Hashim, R. & Witte, V. The Social Integration of a Myrmecophilous Spider Does Not Depend Exclusively on Chemical Mimicry. J Chem Ecol 38, 262–271 (2012). https://doi.org/10.1007/s10886-012-0083-0

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