Protection Mutualisms and the Community: Geographic Variation in an Ant-Plant Symbiosis and the Consequences for Herbivores

Elizabeth G. Pringle, Deborah M Gordon


Protection mutualisms mediate trophic interactions in many systems, but their effects on the surrounding community are rarely studied. Ant-plant symbioses are classic examples of protection mutualisms: myrmecophytic plants provide nesting space and food for symbiotic ants in exchange for ant defense. Ant defense should thus reduce the abundance of herbivores, but studies of ant-plant symbioses usually measure damage to the plant without quantifying the herbivores themselves. In this study, we investigated whether geographic variation in the quality of ant defense in a symbiotic mutualism between Cordia alliodora trees and Azteca ants was associated with the abundance and species richness of plant herbivore communities. In three tropical-dry-forest sites in Middle America, we found that the density of Azteca ants within trees was negatively associated with the levels of leaf herbivory. At sites where ants were effective tree defenders, tree herbivores were less abundant and herbivore assemblages on trees exhibited lower species richness than at a site where ants were poor defenders. In addition, in a site where ants reduced herbivory, herbivore communities were less abundant and diverse in the presence of ants than in their absence, where as in a site where ants did not reduce herbivory, there were no differences in herbivore abundance or richness between trees with or without ants. We conclude that geographic variation in the quality of ant defense drives variation in myrmecophytic-plant herbivore communities. Moreover, ant-plant protection mutualisms should have important but rarely considered effects on herbivore population dynamics and food-plant specialization.


Ant-plant mutualism; Azteca; context dependence; Cordia alliodora; seasonally dry tropical forest; trophic cascades

Full Text:



Agosta, S.J. (2008) Fitness consequences of host use in the field: temporal variation in performance and a life history tradeoff in the moth Rothschildia lebeau (Saturniidae). Oecologia, 157: 69-82. doi: 10.1007/s00442-008-1059-1.

Belovsky, G.E. & Slade, J.B. (1995) Dynamics of two Montana grasshopper populations - relationships among weather, food abundance and intraspecific competition. Oecologia, 101: 383-396. doi: 10.1007/bf00328826.

Boggs, C.L. & Inouye, D.W. (2012) A single climate driver has direct and indirect effects on insect population dynamics. Ecol. Lett., 15: 502-508. doi: 10.1111/j.1461-0248.2012.01766.x.

Bronstein, J.L. (1994) Conditional outcomes in mutualistic interactions. Trends Ecol. Evol., 9: 214-217.

Bronstein, J.L. (1998) The contribution of ant plant protection studies to our understanding of mutualism. Biotropica, 30: 150-161. doi: 10.1111/j.1744-7429.1998.tb00050.x.

Bruno, J.F., Stachowicz, J.J. & Bertness, M.D. (2003) Inclusion of facilitation into ecological theory. Trends Ecol. Evol., 18: 119-125. doi: s0169-5347(02)00045-910.1016/s0169-5347(02)00045-9.

Bullock, S.H., Mooney, H.A. & Medina, E. (1995). Seasonally dry tropical forests New York: Cambridge University Press.

Chamberlain, S.A. & Holland, J.N. (2009) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology, 90: 2384-2392. doi: 10.1890/08-1490.1.

Chittka, L. & Schürkens, S. (2001) Successful invasion of a floral market - An exotic Asian plant has moved in on Europe's river-banks by bribing pollinators. Nature, 411: 653-653. doi: 10.1038/35079676.

Davidson, D.W. & McKey, D. (1993) The evolutionary ecology of symbiotic ant-plant relationships. J. Hymenopt. Res., 2: 13-83.

Dawson, W., Mndolwa, A.S., Burslem, D. & Hulme, P.E. (2008) Assessing the risks of plant invasions arising from collections in tropical botanical gardens. Biodiv. Conserv., 17: 1979-1995. doi: 10.1007/s10531-008-9345-0.

Del-Claro, K. & Oliveira, P.S. (2000) Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia, 124: 156-165. 10.1007/s004420050002.

Dirzo, R. & Domínguez, C.A. (1995). Plant-herbivore interactions in Mesoamerican tropical dry forests. In: S.H. Bullock, H.A. Mooney, E. Medina (Eds.), Seasonally dry tropical forests (pp. 304-325). Cambridge: Cambridge University Press.

Dyer, L.A., Singer, M.S., Lill, J.T., Stireman, J.O., Gentry, G.L., Marquis, R.J., Ricklefs, R.E., Greeney, H.F., Wagner, D.L., Morais, H.C., Diniz, I.R., Kursar, T.A. & Coley, P.D. (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature, 448: 696-699. doi: 10.1038/nature05884.

Fowler, S.V. & Macgarvin, M. (1985) The impact of hairy wood ants, Formica lugubris, on the guild structure of herbivorous insects on birch, Betula pubescens. J. An. Ecol., 54: 847-855. 10.2307/4382.

Frederickson, M.E. (2005) Ant species confer different partner benefits on two neotropical myrmecophytes. Oecologia, 143: 387-395. doi: 10.1007/s00442-004-1817-7.

Gange, A.C., Stagg, P.G. & Ward, L.K. (2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol. Lett., 5: 11-15. doi: 10.1046/j.1461-0248.2002.00299.x.

Gaume, L., McKey, D. & Anstett, M.C. (1997) Benefits conferred by ''timid'' ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax. Oecologia, 112: 209-216. doi: 10.1007/s004420050302.

Gentry, G.L. & Dyer, L.A. (2002) On the conditional, nature of neotropical caterpillar defenses against their natural enemies. Ecology, 83: 3108-3119. doi: 10.1890/0012-9658(2002)083[3108:otcnon];2.

Gotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett., 4: 379-391. doi: 10.1046/j.1461-0248.2001.00230.x.

Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control, and competition. Am. Nat., 94: 421-425. doi: 10.1086/282146.

Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. P. Natl. Acad. Sci. USA, 103: 968-971. 10.1073/pnas.0510466103.

Hay, M.E., Parker, J.D., Burkepile, D.E., Caudill, C.C., Wilson, A.E., Hallinan, Z.P. & Chequer, A.D. (2004) Mutualisms and aquatic community structure: The enemy of my enemy is my friend. Annu. Rev. Ecol. Evol. System., 35: 175-197. doi: 10.1146/annurev.ecolsys.34.011802.132357.

Heads, P.A. & Lawton, J.H. (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation. Ecol. Entomol., 10: 29-42. 10.1111/j.1365-2311.1985.tb00532.x.

Heil, M. & McKey, D. (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu. Rev. Ecol. Evol. System., 34: 425-453.

Hölldobler, B. & Wilson, E.O. (1990). The ants. Cambridge, MA: Bellknap Press.

Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders - heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73: 724-732.

Itino, T. & Itioka, T. (2001) Interspecific variation and ontogenetic change in antiherbivore defense in myrmecophytic Macaranga species. Ecol. Res., 16: 765-774. 10.1046/j.1440-1703.2001.00432.x.

Jani, A.J., Faeth, S.H. & Gardner, D. (2010) Asexual endophytes and associated alkaloids alter arthropod community structure and increase herbivore abundances on a native grass. Ecol. Lett., 13: 106-117. doi: 10.1111/j.1461-0248.2009.01401.x.

Janzen, D.H. (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution, 20: 249-275.

Janzen, D.H. (1967) Interaction of the bull's-horn acacia (Acacia cornigera L.) with an ant inhabitant (Pseudomyrmex ferruginea F. Smith) in Eastern Mexico. The University of Kansas Science Bulletin, 47, 315-558.

Janzen, D.H. (1988) Ecological characterization of a Costa Rican dry forest caterpillar fauna. Biotropica, 20: 120-135.

Janzen, D.H. & Hallwachs, W. (2009) Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservación Guanacaste (ACG), northwestern Costa Rica. In.

Janzen, D.H. & Schoener, T.W. (1968) Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology, 49: 96-110.

Kaplan, I. & Eubanks, M.D. (2005) Aphids alter the community-wide impact of fire ants. Ecology, 86: 1640-1649. doi: 10.1890/04-0016.

Longino, J.T. (1996) Taxonomic characterization of some live-stem inhabiting Azteca (Hymenoptera: Formicidae) in Costa Rica, with special reference to the ants of Cordia (Boraginaceae) and Triplaris (Polygonaceae). J. Hymenopt. Res., 5: 131-156.

Longino, J.T. (2007) A taxonomic review of the genus Azteca (Hymenoptera : Formicidae) in Costa Rica and a global revision of the aurita group. Zootaxa, 3-63.

Mooney, K.A. (2007) Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology, 88, 2005-2014. 10.1890/06-1095.1.

Oliveira, P.S. & Del-Claro, K. (2005). Multitrophic interactions in a neotropical savanna: ant-hemipteran systems, associated insect herbivores and a host plant. In: D.F.R.P. Burslem, M. Pinard, S.E. Hartley (Eds.), Biotic interactions in the tropics: their role in the maintenance of species diversity (pp. 414-438). Cambridge: Cambridge University Press.

Palmer, T.M. & Brody, A.K. (2013) Enough is enough: the effects of symbiotic ant abundance on herbivory, growth, and reproduction in an African acacia. Ecology, 94: 683-691.

Pringle, E.G., Dirzo, R. & Gordon, D.M. (2011) Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree. Ecology, 91: 37-46.

Pringle, E.G., Dirzo, R. & Gordon, D.M. (2012a) Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies. Oecologia, 170: 677-685. doi: 10.1007/s00442-012-2340-x.

Pringle, E.G., Ramírez, S.R., Bonebrake, T.C., Gordon, D.M. & Dirzo, R. (2012b) Diversification and phylogeographic structure in widespread Azteca plant-ants from the northern Neotropics. Mol. Ecol., 21: 3576-3592. doi: 10.1111/j.1365-294X.2012.05618.x.

Rosumek, F.B., Silveira, F.A.O., Neves, F.D., Barbosa, N.P.D., Diniz, L., Oki, Y., Pezzini, F., Fernandes, G.W. & Cornelissen, T. (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia, 160: 537-549. doi: 10.1007/s00442-009-1309-x.

Rudgers, J.A. & Clay, K. (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecol. Lett., 11: 831-840. doi: 10.1111/j.1461-0248.2008.01201.x.

Rudgers, J.A., Savage, A.M. & Rua, M.A. (2010) Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity. Oecologia, 163: 985-996. doi: 10.1007/s00442-010-1584-6.

Rudgers, J.A. & Strauss, S.Y. (2004) A selection mosaic in the facultative mutualism between ants and wild cotton. P. Roy. Soc. Lond. B-Bio., 271: 2481-2488. doi: 10.1098/rspb.2004.2900.

SAS Institute Inc. (2010) JMP® Pro Version 10.0. In, Cary, NC

Sendoya, S.F., Freitas, A.V.L. & Oliveira, P.S. (2009) Egg-laying butterflies distinguish predaceous ants by sight. Am. Nat., 174: 134-140. doi: 10.1086/599302.

Stachowicz, J.J. (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience, 51: 235-246. doi: 10.1641/0006-3568(2001)051[0235:mfatso];2.

Stevens, P.F. (2001) Angiospterm phylogeny website. Version 12, July 2012. In.

Styrsky, J.D. & Eubanks, M.D. (2007) Ecological consequences of interactions between ants and honeydew-producing insects. P. Roy. Soc. Lond. B-Bio., 274: 151-164. doi: 10.1098/rspb.2006.3701.

Terborgh, J. (1986). Keystone plant resources in the tropical forest. In: M.J. Soulé (Eds.), Conservation biology: the science of scarcity and diversity (pp. 330-344). Sunderland, MA: Sinauer Associates.

Terborgh, J., Nunez-Iturri, G., Pitman, N.C.A., Valverde, F.H.C., Alvarez, P., Swamy, V., Pringle, E.G. & Paine, C.E.T. (2008) Tree recruitment in an empty forest. Ecology, 89: 1757-1768. doi: 10.1890/07-0479.1.

Thompson, J.N. (2005). The geographic mosaic of coevolution Chicago: University of Chicago Press.

Tillberg, C.V. (2004) Friend or foe? A behavioral and stable isotopic investigation of an ant-plant symbiosis. Oecologia, 140: 506-515.

Trager, M.D., Bhotika, S., Hostetler, J.A., Andrade, G.V., Rodriguez-Cabal, M.A., McKeon, C.S., Osenberg, C.W. & Bolker, B.M. (2010) Benefits for plants in ant-plant protective mutualisms: a meta-analysis. PLoS ONE, 5, e1430810.1371/journal.pone.0014308.

Trager, M.D. & Bruna, E.M. (2006) Effects of plant age, experimental nutrient addition and ant occupancy on herbivory in a neotropical myrmecophyte. J. Ecol., 94: 1156-1163. doi: 10.1111/j.1365-2745.2006.01165.x.

Vencl, F.V. & Srygley, R.B. (2013) Enemy targeting, trade-offs, and the evolutionary assembly of a tortoise beetle defense arsenal. Evol. Ecol., 27: 237-252. doi: 10.1007/s10682-012-9603-1.

Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera. Annu. Rev. Entomol., 8: 307-344. doi: 10.1146/annurev.en.08.010163.001515.

Wimp, G.M. & Whitham, T.G. (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology, 82: 440-452. doi: 10.1890/0012-9658(2001)082[0440:bcopah];2.



  • There are currently no refbacks.

JCR Impact Factor 2018: 0.604