, Volume 97, Issue 10, pp 925–934 | Cite as

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

  • Alain Dejean
  • Céline Leroy
  • Bruno Corbara
  • Régis Céréghino
  • Olivier Roux
  • Bruno Hérault
  • Vivien Rossi
  • Roberto J. Guerrero
  • Jacques H. C. Delabie
  • Jérôme Orivel
  • Raphaël Boulay
Original Paper


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.


Ant–plant relationships Biotic defense Parasites of mutualisms Temporary social parasites Azteca Cecropia 



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.


  1. Beattie A (1989) Myrmecotrophy: plants fed by ants. Trends Ecol Evol 4:172–176CrossRefGoogle Scholar
  2. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  3. Cabrera M, Jaffe K (1994) A trophic mutualism between myrmecophytic melastomataceae Tococa guianensis Aublet and an Azteca ant species. Ecotropicos 7:1–10Google Scholar
  4. Calcaterra LA, Briano JA, Williams DF (1999) Field studies of the parasitic ant Solenopsis daguerrei (Hymenoptera: Formicidae) on fire ants in Argentina. Environ Entomol 28:88–95Google Scholar
  5. Clement LW, Köppen SCW, Brand WA, Heil M (2008) Strategies of a parasite of the ant-Acacia mutualism. Behav Ecol Sociobiol 62:953–962CrossRefPubMedGoogle Scholar
  6. Davidson DW (2005) Cecropia and its biotic defenses. Fl Neotrop Monog 94:214–226Google Scholar
  7. 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 14:251–257CrossRefGoogle Scholar
  8. Dejean A, Corbara B, Orivel J, Leponce M (2007) Rainforest canopy ants: the implications of territoriality and predatory behavior. Funct Ecosyst Commun 1:105–120Google Scholar
  9. 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 10:1225–1240Google Scholar
  10. 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 96:57–63CrossRefPubMedGoogle Scholar
  11. 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:e11331CrossRefPubMedGoogle Scholar
  12. Djiéto-Lordon C, Dejean A (1999a) Innate attraction supplants experience during host plant selection in an obligate plant-ant. Behav Proc 46:181–187CrossRefGoogle Scholar
  13. Djiéto-Lordon C, Dejean A (1999b) Tropical arboreal ant mosaic: innate attraction and imprinting determine nesting site selection in dominant ants. Behav Ecol Sociobiol 45:219–225CrossRefGoogle Scholar
  14. 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 1713:47–52Google Scholar
  15. 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 133:186–192CrossRefGoogle Scholar
  16. 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 91:126–134CrossRefGoogle Scholar
  17. 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 84:130–144CrossRefGoogle Scholar
  18. Guerrero RJ, Delabie JHC, Dejean A (2010) Taxonomic contribution to the aurita group of the ant genus Azteca (Formicidae: Dolichoderinae). J Hymenopt Res 19:51–65Google Scholar
  19. Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Ann Rev Ecol Syst Evol 34:425–553CrossRefGoogle Scholar
  20. Heil M, Baumann B, Krüger R, Linsenmair KE (2004) Main nutrient compounds in food bodies of Mexican Acacia ant-plants. Chemoecology 14:45–52CrossRefGoogle Scholar
  21. 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 106:18091–18096CrossRefPubMedGoogle Scholar
  22. Hölldobler B, Wilson EO (1990) The ants. Springer-Verlag, BerlinGoogle Scholar
  23. Janzen DH (1975) Pseudomyrmex nigropilosa: a parasite of a mutualism. Science 188:936–937CrossRefPubMedGoogle Scholar
  24. Jolivet P (1996) Ants and plants: an example of coevolution. Backhuys, The HagueGoogle Scholar
  25. Kautz SHT, Ward PS, Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant-ants to their ant-plant partners. Evolution 63:839–853CrossRefPubMedGoogle Scholar
  26. Longino JT (2007) A taxonomic review of the genus Azteca (Hymenoptera: Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa 1491:1–63Google Scholar
  27. 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 29:345–352CrossRefGoogle Scholar
  28. Rickson FR, Rickson MM (1986) Nutrient acquisition facilitated by litter collection and ant colonies on two Malaysian palms. Biotropica 18:337–343CrossRefGoogle Scholar
  29. Rico-Gray V, Oliveira P (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, ChicagoGoogle Scholar
  30. Sagers CL, Ginger SM, Evans RD (2000) Carbon and nitrogen isotopes trace nutrient exchange in an ant-plant mutualism. Oecologia 123:582–586CrossRefGoogle Scholar
  31. Solano PJ, Dejean A (2004) Ant-fed plants: comparison between three geophytic myrmecophytes. Biol J Linn Soc 83:433–439CrossRefGoogle Scholar
  32. Sumner S, Aanen DK, Delabie JHC, Boomsma JJ (2004) The evolution of social parasitism in leaf-cutting ants. Insect Soc 151:37–42CrossRefGoogle Scholar
  33. 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 21:253–263CrossRefGoogle Scholar
  34. Wilkinson DM, Sherratt TN (2001) Horizontally acquired mutualisms, an unsolved problem in ecology. Oikos 92:377–384CrossRefGoogle Scholar
  35. Wilson EO (1984) Tropical social parasites in the ant genus Pheidole, with an analysis of the anatomical parasitic syndrome (Hymenoptera: Formicidae). Insect Soc 31:316–334CrossRefGoogle Scholar
  36. Wilson EO (2003) Pheidole in the New World. A dominant, hyperdiverse ant genus. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Alain Dejean
    • 1
  • Céline Leroy
    • 1
  • Bruno Corbara
    • 2
    • 3
  • Régis Céréghino
    • 4
    • 5
  • Olivier Roux
    • 1
  • Bruno Hérault
    • 6
  • Vivien Rossi
    • 7
  • Roberto J. Guerrero
    • 8
  • Jacques H. C. Delabie
    • 9
  • Jérôme Orivel
    • 1
  • Raphaël Boulay
    • 10
    • 11
  1. 1.CNRS; Écologie des Forêts de Guyane (UMR-CNRS 8172), Campus AgronomiqueKourou CedexFrance
  2. 2.CNRS; UMR 6023, Laboratoire Microorganismes Génome et Environnement (LMGE)AubièreFrance
  3. 3.Clermont Université, Université Blaise Pascal, LMGEClermont-FerrandFrance
  4. 4.CNRS; UMR 5245, EcoLab (Laboratoire d’Ecologie Fonctionnelle)ToulouseFrance
  5. 5.Université de Toulouse; UPS, INPT; EcoLabToulouseFrance
  6. 6.Université des Antilles et de la Guyane; Écologie des Forêts de Guyane (UMR-UAG 43), Campus AgronomiqueKOUROU cedexFrance
  7. 7.CIRAD; Écologie des Forêts de Guyane (UMR-CIRAD 93), Campus AgronomiqueKOUROU CedexFrance
  8. 8.Grupo de Investigación en Insectos Neotropicales, INTROPICUniversidad del MagdalenaSanta MartaColombia
  9. 9.Laboratório de Mirmecología, Convênio UESC-CEPEC, Centro de Pesquisas do Cacau, CEPLACItabuna-BABrazil
  10. 10.Estación Biológica de Doñana, CSICSevillaSpain
  11. 11.Departamento de Biología Animal, Facultad de CienciasUniversidad de GranadaGranadaSpain

Personalised recommendations