Skip to main content
Log in

A temporary social parasite of tropical plant-ants improves the fitness of a myrmecophyte

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Myrmecophytes offer plant-ants a nesting place in exchange for protection from their enemies, particularly defoliators. These obligate ant–plant mutualisms are common model systems for studying factors that allow horizontally transmitted mutualisms to persist since parasites of ant–myrmecophyte mutualisms exploit the rewards provided by host plants whilst providing no protection in return. In pioneer formations in French Guiana, Azteca alfari and Azteca ovaticeps are known to be mutualists of myrmecophytic Cecropia (Cecropia ants). Here, we show that Azteca andreae, whose colonies build carton nests on myrmecophytic Cecropia, is not a parasite of AztecaCecropia mutualisms nor is it a temporary social parasite of A. alfari; it is, however, a temporary social parasite of A. ovaticeps. Contrarily to the two mutualistic Azteca species that are only occasional predators feeding mostly on hemipteran honeydew and food bodies provided by the host trees, A. andreae workers, which also attend hemipterans, do not exploit the food bodies. Rather, they employ an effective hunting technique where the leaf margins are fringed with ambushing workers, waiting for insects to alight. As a result, the host trees’ fitness is not affected as A. andreae colonies protect their foliage better than do mutualistic Azteca species resulting in greater fruit production. Yet, contrarily to mutualistic Azteca, when host tree development does not keep pace with colony growth, A. andreae workers forage on surrounding plants; the colonies can even move to a non-Cecropia tree.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Beattie A (1989) Myrmecotrophy: plants fed by ants. Trends Ecol Evol 4:172–176

    Article  Google Scholar 

  • Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287

    Article  Google Scholar 

  • Cabrera M, Jaffe K (1994) A trophic mutualism between myrmecophytic melastomataceae Tococa guianensis Aublet and an Azteca ant species. Ecotropicos 7:1–10

    Google Scholar 

  • Calcaterra LA, Briano JA, Williams DF (1999) Field studies of the parasitic ant Solenopsis daguerrei (Hymenoptera: Formicidae) on fire ants in Argentina. Environ Entomol 28:88–95

    Google Scholar 

  • Clement LW, Köppen SCW, Brand WA, Heil M (2008) Strategies of a parasite of the ant-Acacia mutualism. Behav Ecol Sociobiol 62:953–962

    Article  PubMed  Google Scholar 

  • Davidson DW (2005) Cecropia and its biotic defenses. Fl Neotrop Monog 94:214–226

    Google Scholar 

  • De Souza DJ, Fernandes Soares M, Castro Della Lucia TM (2007) Acromyrmex ameliae sp. n. (Hymenoptera: Formicidae): a new social parasite of leaf-cutting ants in Brazil. Insect Sci 14:251–257

    Article  Google Scholar 

  • Dejean A, Corbara B, Orivel J, Leponce M (2007) Rainforest canopy ants: the implications of territoriality and predatory behavior. Funct Ecosyst Commun 1:105–120

    Google Scholar 

  • Dejean A, Grangier J, Leroy C, Orivel J (2008) Host plant protection by arboreal ants: looking for a pattern in locally induced responses. Evol Ecol Res 10:1225–1240

    Google Scholar 

  • Dejean A, Grangier J, Leroy C, Orivel J (2009) Predation and aggressiveness in host plant protection: a generalization using ants of the genus Azteca. Naturwissenschaften 96:57–63

    Article  CAS  PubMed  Google Scholar 

  • Dejean A, Leroy C, Corbara B, Roux O, Céréghino C, Orivel J, Boulay R (2010) Arboreal ants use the “Velcro® Principle” to capture very large prey. PLoS ONE 5:e11331

    Article  PubMed  Google Scholar 

  • Djiéto-Lordon C, Dejean A (1999a) Innate attraction supplants experience during host plant selection in an obligate plant-ant. Behav Proc 46:181–187

    Article  Google Scholar 

  • Djiéto-Lordon C, Dejean A (1999b) Tropical arboreal ant mosaic: innate attraction and imprinting determine nesting site selection in dominant ants. Behav Ecol Sociobiol 45:219–225

    Article  Google Scholar 

  • Feitosa RM, Hora RR, Delabie JHC, Valenzuela J, Fresneau D (2008) A new social parasite in the ant genus Ectatomma F. Smith (Hymenoptera, Formicidae, Ectatomminae). Zootaxa 1713:47–52

    Google Scholar 

  • Fischer RC, Richter A, Wanek W, Mayer V (2002) Plants feed ants: food bodies of myrmecophytic Piper and their significance for the interaction with Pheidole bicornis ants. Oecologia 133:186–192

    Article  Google Scholar 

  • Fischer RC, Wanek W, Richter A, Mayer V (2003) Do ants feed plants? A 15N labelling study of nitrogen fluxes from ants to plants in the mutualism of Pheidole and Piper. J Ecol 91:126–134

    Article  Google Scholar 

  • Gaume L, McKey D (1999) An ant-plant mutualism and its host-specific parasite: activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant ants inhabiting the same myrmecophyte. Oikos 84:130–144

    Article  Google Scholar 

  • Guerrero RJ, Delabie JHC, Dejean A (2010) Taxonomic contribution to the aurita group of the ant genus Azteca (Formicidae: Dolichoderinae). J Hymenopt Res 19:51–65

    Google Scholar 

  • Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Ann Rev Ecol Syst Evol 34:425–553

    Article  Google Scholar 

  • Heil M, Baumann B, Krüger R, Linsenmair KE (2004) Main nutrient compounds in food bodies of Mexican Acacia ant-plants. Chemoecology 14:45–52

    Article  CAS  Google Scholar 

  • Heil M, González-Teuber M, Clement LW, Kautz S, Verhaagh M, Silva Bueno JC (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proc Natl Acad Sci USA 106:18091–18096

    Article  CAS  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Springer-Verlag, Berlin

    Google Scholar 

  • Janzen DH (1975) Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188:936–937

    Article  CAS  PubMed  Google Scholar 

  • Jolivet P (1996) Ants and plants: an example of coevolution. Backhuys, The Hague

    Google Scholar 

  • Kautz SHT, Ward PS, Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63:839–853

    Article  CAS  PubMed  Google Scholar 

  • Longino JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491:1–63

    Google Scholar 

  • Raine N, Gammans N, Macfadyen IJ, Scrivner GK, Stone GN (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant plant. Ecol Entomol 29:345–352

    Article  Google Scholar 

  • Rickson FR, Rickson MM (1986) Nutrient acquisition facilitated by litter collection and ant colonies on two Malaysian palms. Biotropica 18:337–343

    Article  Google Scholar 

  • Rico-Gray V, Oliveira P (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago

    Google Scholar 

  • Sagers CL, Ginger SM, Evans RD (2000) Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia 123:582–586

    Article  Google Scholar 

  • Solano PJ, Dejean A (2004) Ant-fed plants: comparison between three geophytic myrmecophytes. Biol J Linn Soc 83:433–439

    Article  Google Scholar 

  • Sumner S, Aanen DK, Delabie JHC, Boomsma JJ (2004) The evolution of social parasitism in leaf-cutting ants. Insect Soc 151:37–42

    Article  Google Scholar 

  • Ward PS (1996) A new workerless social parasite in the ant genus Pseudomyrmex (Hymenoptera: Formicidae), with a discussion of the origin of social parasitism in ants. Syst Entomol 21:253–263

    Article  Google Scholar 

  • Wilkinson DM, Sherratt TN (2001) Horizontally acquired mutualisms, an unsolved problem in ecology. Oikos 92:377–384

    Article  Google Scholar 

  • Wilson EO (1984) Tropical social parasites in the ant genus Pheidole, with an analysis of the anatomical parasitic syndrome (Hymenoptera: Formicidae). Insect Soc 31:316–334

    Article  Google Scholar 

  • Wilson EO (2003) Pheidole in the New World. A dominant, hyperdiverse ant genus. Harvard University Press, Cambridge

    Google Scholar 

Download references

Acknowledgements

We are grateful to Shawn M. Clark (Brigham Young University, Provo, Utah, USA) for the identification of the chrysomelid beetles, to Marie-Françoise Prévost (Herbier de Guyane, Cayenne, France) for the identification of the plants, and to Andrea Yockey-Dejean for proof-reading the manuscript. Financial support for this study was provided by the Programme Amazonie II of the French Centre National de la Recherche Scientifique (project 2ID) and the Programme Convergence 2007–2013, Région Guyane from the European Community (project DEGA). The experiments comply with the current laws of the country in which they were performed. The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alain Dejean.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dejean, A., Leroy, C., Corbara, B. et al. A temporary social parasite of tropical plant-ants improves the fitness of a myrmecophyte. Naturwissenschaften 97, 925–934 (2010). https://doi.org/10.1007/s00114-010-0710-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-010-0710-y

Keywords

Navigation