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Evolutionary Ecology

, Volume 26, Issue 1, pp 55–63 | Cite as

An ant symbiont directly and indirectly limits its host plant’s reproductive success

  • Pierre-Jean G. Malé
  • Céline Leroy
  • Alain Dejean
  • Angélique Quilichini
  • Jérôme Orivel
Original Paper

Abstract

In theory, mutualisms are intrinsically unstable, and the search for the maximum profit at the minimum cost should lead every mutualist to become a parasite. From an empirical point of view, mutualisms are ubiquitous and of major importance to ecosystems, suggesting the existence of mechanisms that enhance the maintenance of such relationships. We focused on the obligatory myrmecophytic association between the Neotropical plant Hirtella physophora (Chrysobalanaceae) and the ant Allomerus decemarticulatus (Myrmicinae). The plant shelters the ants in leaf pouches in exchange for protection from phytophagous insects. We experimentally demonstrated that the ants partially castrate their host plant by destroying almost two-thirds of its floral buds. The ants also impede pollination through their presence and interactions with pollinators. These results reveal that ant activity negatively affects the plant’s reproduction both directly and indirectly. This dual negative effect does not result in the complete castration of the plant. We also highlight major limitations to plant reproduction due to the spontaneous abscission of flowers and to the limited quantity and/or poor quality of the pollen. These limitations must not be overlooked since they can alter the outcome of the association of H. physophora with its ant partner. We therefore conclude that the evolutionary fate of the relationship depends on both ant castration intensity and obstacles to plant fertilization not related to the presence of ants.

Keywords

Evolutionary conflict Cheater Pollination Mutualism breakdown Myrmecophyte 

Notes

Acknowledgments

We are grateful to the Laboratoire Environnement de Petit Saut for furnishing logistical help, to Isabelle Henry for her help in the field, to Jean-Baptiste Ferdy for statistical help and to Andrea Yockey-Dejean for editing the manuscript. Financial support for this study was provided by a research program of the French Agence Nationale de la Recherche (research agreement n°ANR-06-JCJC-0109-01), by the ESF-EUROCORES/TECT/BIOCONTRACT program, by the Programme Convergence 2007-2013 Région Guyane from the European Community (Project DEGA), and by the Programme Amazonie II of the French Centre National de la Recherche Scientifique (Project 2ID).

References

  1. Atkinson B, Therneau T (2009) kinship: mixed-effects Cox models, sparse matrices, and modeling data from large pedigrees. R package version 1.1.0-23. Available from http://CRAN.R-project.org/package=kinship
  2. Bates D, Maechler M (2009) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-32. Available from http://CRAN.R-project.org/package=lme4
  3. Beattie AJ, Turnbull C, Knox RB, Williams EG (1984) Ant inhibition of pollen function: a possible reason why ant pollination is rare. Am J Bot 71:421–426CrossRefGoogle Scholar
  4. Beattie AJ, Turnbull C, Hough T, Jobson S, Knox RB (1985) The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. Am J Bot 72:606–614CrossRefGoogle Scholar
  5. Bonds MH (2006) Host life-history strategy explains pathogen-induced sterility. Am Nat 168:281–293PubMedCrossRefGoogle Scholar
  6. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  7. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol S 18:237–268CrossRefGoogle Scholar
  8. Cox DR (1972) Regression models and life-tables. Proc R Soc B 34:187–220Google Scholar
  9. Dejean A, Solano P-J, Belin-Depoux M, Cerdan P, Corbara B (2001) Predatory behavior of patrolling Allomerus decemarticulatus workers (Formicidae; Myrmicinae) on their host plant. Sociobiology 37:571–578Google Scholar
  10. Dejean A, Solano P-J, Ayroles J, Corbara B, Orivel J (2005) Arboreal ants build traps to capture prey. Nature 434:973PubMedCrossRefGoogle Scholar
  11. Edwards DP, Yu DW (2008) Tolerating castration by hiding flowers in plain sight. Behav Ecol Sociobiol 63:95–102CrossRefGoogle Scholar
  12. Frederickson ME (2009) Conflict over reproduction in an ant-plant symbiosis: why Allomerus octoarticulatus ants sterilize Cordia nodosa trees. Am Nat 173:675–681PubMedCrossRefGoogle Scholar
  13. Gaume L, Zacharias M, Borges RM (2005) Ant–plant conflicts and a novel case of castration parasitism in a myrmecophyte. Evol Ecol Res 7:435–452Google Scholar
  14. Ghazoul J (2001) Can floral repellents pre-empt potential ant-plant conflicts? Ecol Lett 4:295–299CrossRefGoogle Scholar
  15. Grangier J, Dejean A, Malé P-JG, Orivel J (2008) Indirect defense in a highly specific ant-plant mutualism. Naturwissenschaften 95:909–916PubMedCrossRefGoogle Scholar
  16. Grangier J, Dejean A, Malé P-JG, Solano P-J, Orivel J (2009) Mechanisms driving the specificity of a myrmecophyte-ant association. Biol J Linn Soc 97:90–97CrossRefGoogle Scholar
  17. Hull DA, Beattie AJ (1988) Adverse effects on pollen exposed to Atta texana and other North American ants: implications for ant pollination. Oecologia 75:153–155CrossRefGoogle Scholar
  18. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70CrossRefGoogle Scholar
  19. Izzo TJ, Vasconcelos HL (2002) Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia 133:200–205CrossRefGoogle Scholar
  20. Kalbfleish JD, Prentice RL (1980) The statistical analysis of failure time data. Wiley, New YorkGoogle Scholar
  21. Leroy C, Jauneau A, Quilichini A, Dejean A, Orivel J (2008) Comparison between the anatomical and morphological structure of leaf blades and foliar domatia in the ant-plant Hirtella physophora (Chrysobalanaceae). Ann Bot 101:501–507PubMedCrossRefGoogle Scholar
  22. Malé P-JG (2011) Stabilité évolutive des mutualismes et mécanismes de contrôle : le cas d’une relation plante-fourmis. PhD Thesis, Université de Toulouse, Toulouse, FranceGoogle Scholar
  23. Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514CrossRefGoogle Scholar
  24. Oliveira PS (1997) The ecological function of extrafloral nectaries: herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae). Funct Ecol 11:323–330CrossRefGoogle Scholar
  25. Orivel J, Lambs L, Malé P-JG, Leroy C, Grangier J, Otto T, Quilichini A, Dejean A (2011) Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants. Oecologia 165:369–376PubMedCrossRefGoogle Scholar
  26. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, ChicagoGoogle Scholar
  27. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592PubMedCrossRefGoogle Scholar
  28. Sage TL, Griffin SR, Pontieri V, Drobac P, Cole WW, Barrett SCH (2001) Stigmatic self-incompatibility and mating patterns in Trillium grandiflorum and Trillium erectum (Melanthiaceae). Ann Bot 88:829–841CrossRefGoogle Scholar
  29. Seavey SR, Bawa KS (1986) Late-acting self-incompatibility in angiosperms. Bot Rev 52:195–219CrossRefGoogle Scholar
  30. Solano P-J, Durou S, Corbara B, Quilichini A, Cerdan P, Belin-Dupoux M, Delabie JHC, Dejean A (2003) Myrmecophytes of the understory of French Guianian rainforests: their distribution and their associated ants. Sociobiology 41:605–614Google Scholar
  31. Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol S 12:253–279CrossRefGoogle Scholar
  32. R Development Core Team (2009) R: a language and environment for statistical computing. Available from http://www.R-projetc.org
  33. Therneau T, Lumley T (2009) survival: Survival analysis, including penalised likelihood. R package version 2.35-7. Available from http://CRAN.R-project.org/package=survival
  34. Wagner D (2000) Pollen viability reduction as a potential cost of ant association for Acacia constricta (Fabaceae). Am J Bot 87:711–715PubMedCrossRefGoogle Scholar
  35. Wyatt R (1980) The impact of nectar-robbing ants on the pollination system of Asclepias curassavica. Bull Torrey Bot Club 107:24–28CrossRefGoogle Scholar
  36. Young TP, Stubblefield CH, Isabell LA (1997) Ants on swollen-thorn acacias: species coexistence in a simple system. Oecologia 109:98–107CrossRefGoogle Scholar
  37. Yu DW (2001) Parasites of mutualisms. Biol J Linn Soc 72:529–546CrossRefGoogle Scholar
  38. Yu DW, Pierce NE (1998) A castration parasite of an ant-plant mutualism. Proc R Soc B 265:375–382CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Pierre-Jean G. Malé
    • 1
    • 2
  • Céline Leroy
    • 3
  • Alain Dejean
    • 3
  • Angélique Quilichini
    • 3
    • 4
  • Jérôme Orivel
    • 1
    • 2
    • 3
  1. 1.UPS, Laboratoire Evolution et Diversité Biologique (EDB)Université de ToulouseToulouse Cedex 9France
  2. 2.CNRS, EDB (Laboratoire Evolution et Diversité Biologique)UMR 5174, Université Paul SabatierToulouse Cedex 9France
  3. 3.CNRS, UMR Ecologie des Forêts de GuyaneKourou CedexFrance
  4. 4.Jardin Botanique Henri GaussenToulouseFrance

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