The role of parabiotic ants and environment on epiphyte composition and protection in ant gardens

Laura Carolina Leal, Catarina C Jacovak, Paulo Estefano D Bobrowiec, José Luiz C Camargo, Paulo Enrique C Peixoto

Abstract


Ant gardens (AGs) are a multi-partner specialized ant-plant interaction involving several ant and epiphyte species. Although studies on AGs have reported possible roles for some species in this system, there are unanswered questions regarding the process of epiphyte incorporation in the AGs and the role of less aggressive ant species in AG protection. In this study, we used AGs in the Brazilian Amazon forest formed by two parabiotic ant species to test a set of hypothesis regarding two main questions: 1) How is AG plant community composition affected by the surrounding environment? 2) Does Crematogaster levior play a role in the chemical detection of herbivory in the AGs? After identifying epiphytes occurring at AGs at the forest edge and in the interior, we found that ant gardens in each environment exhibited different compositions, and that plant species bearing oil or extrafloral nectar glands were more frequent in AGs located in the forest interior than in those at the forest edge. By performing experiments with volatile compounds emitted from injured epiphytes, we detected that only Camponotus femoratus was responsive, responding almost eight times faster in response to plant extracts than water treatments. Our results support the idea that environmental conditions affect ant preference for feeding resources provided by epiphytes and consequently shape the structure of the epiphyte community in AGs. On the other hand, the role of C. levior in AGs remains unknown, since it seems to play no direct or indirect role in AG protection.


Keywords


Camponotus femoratus; Crematogaster levior; epiphytes; partner selection; protective mutualism; Amazon

Full Text:

PDF

References


Agrawal, A. & Dubin-Thaler, B.J. (1999). Induced response to herbivory in the Neotropical ant-plant association between Azteca ants and Cecropia trees: response of ants to potential inducing cues. Behavioral Ecology and Sociobiology, 45: 47-54. doi: 10.1007/s002650050538

Archetti, M., Scheuring, I., Hoffman, M., Frederickson, M.E., Pierce, N.E. & Yu, D.W. (2011). Economic game theory for mutualism and cooperation. Ecology Letters, 14: 1300-1312. doi: 10.1111/j.1461-0248.2011.01697.x

Bates, D., Maechler, M., Bolker, B. & Walker, S. (2013). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-5. http://CRAN.R-project.org/package=lme4.

Bluthgen, N. & Reifenrath, K. (2003). Extrafloral nectaries in Australian rainforest: structure and distribution. Australian Journal of Botany, 51: 515-527. doi: 10.1071/BT02108

Bluthgen, N. & Fiedler, K. (2004). Competition for composition: lessons from nectar-feeding ant community. Ecology, 85: 1479-1485. doi: 10.1890/03-0430

Bronstein, J.L. (1994). Conditional outcomes in mutualistic interactions. Trends in Ecology and Evolution, 9: 214-217. doi: 10.1016/0169-5347(94)90246-1

Bronstein, J.L., Alarcón, R., Geber, M. (2006). The evolution of plant-insect mutualism. New Phytologist, 172: 412-428. doi: 10.1111/j.1469-8137.2006.01864.x

Brouat, C., McKey, D., Bessiere, J., Pascal, L. & Hossaert-Mckey, M. (2000). Leaf volatiles compounds and the distribution of ants patrolling in an ant-plant mutualism: preliminary results from Leonardoxa (Fabaceae: Caesalpinoidea) and Petalomyrmex (Hymenoptera: Formicinae). Acta Oecologica, 21: 349-357. doi: 10.1016/S1146-609X(00)01091-2

Buckley, R.C. (1982). Ant plant interaction: a world review. In: Buckley, R.C. (Ed.), Ant-plant interaction in Australia (p. 111-141). Netherlands: Springer.

Camargo, J.L.C. & Kapos, V. (1995). Complex edge effects on soil moisture and microclimate in Central Amazonian forest. Journal of Tropical Ecology, 11:205-221.

Christianini, A.V. & Machado. G. (2004). Induced biotic response to herbivory and associated cues in the Amazonian ant-plant Maietta poeppigii. Entomologia Experimentalis et Applicata, 12: 81-88.

Corbara, B. & Dejean, A. (1988). A stingless bee nesting inside ant-garden in French Guiana (Hymenoptera, Apiidae). Sociobiology, 32: 489-492.

Davidson, D.W. (1988). Ecological studies of neotropical ant gardens. Ecology, 69: 1138-1152.

Edwards, D.P., Ansell, F.A., Woodcock, P., Fayle, T.M., Chey, V.K. & Hamer, K.C. (2010). Can the failure to punish promote cheating in mutualism? Oikos, 119: 42-52. doi: 10.1111/j.1600-0706.2009.17591.x

Elias, T.S. & Gelband, H. (1976). Morphology and anatomy of floral and extrafloral nectaries in Campsis (Bignoniaceae). American Journal of Botany, 63: 1349-1353.

Forel, A. (1898). La parabiose chez les fourmis. Buletin de la Societé Vaudoise de Sciences Naturelles, 34: 380-384.

Holldobler, B. & Wilson, E.O. (1990). The ants. Cambridge: Harvard University Press, 732 p.

Janzen, D.H. (1985). The natural history of mutualisms. In: Boucher, D.H. (ed.) The biology of mutualisms: ecology and evolution (p. 41-85). Oxford: Oxford University Press.

Kauffman, E. & Machwitz, U. (2006). Ant gardens of tropical Asian forest. Naturwissenchaften, 93: 216-227. doi: 10.1007/s00114-005-0081-y

Kaspari, M. & Yanoviak, S.P. (2001). Bait use in tropical litter and canopy ants – evidence of diferences in nutrient limitation. Biotropica, 33: 207-211.

Kleinfeldt, S.E. (1978). Ant gardens: the interaction of Codonanthe crassifolia (Gesneriaceae) and Crematogaster longispina (Formicidae). Ecology, 59: 449-456.

Laurance, W.F., Camargo, J.L.C., Luizao, R.C.C., Laurance, S.G., Pimm, D.S.L., Bruna, E.M., Stouffer, P.C., Willianson, G., Benitez-Malvido, J.; Vasconcelos, H.L., Van Houtan, K.S., Zartman, C.E., Boyle, S.A., Didhamm, R.K., Andrade, A. & Lovejoy, T.E. (2011). The fate of Amazonian forest fragments: A 32-year investigation. Biological Conservation, 144: 56-67.

Menzel, F. & Kriesell, H. & Witte, V. (2014). Parabiotic ants: the costs and benefits of symbiosis. Ecological Entomology, 39: 436-444. doi: 10.1111/een.12116

Murcia, C. (1995). Edge effects in fragmented forests: implication for conservation. Trends in Ecology and Evolution, 10: 58-62. doi: 10.1016/S0169-5347(00)88977-6

Orivel, J. & Dejean, A. (1999) Selection of epiphyte seeds by ant gardens ants. Ecoscience, 6: 51-55.

Orivel, J., Errard, C. & Dejean, A. (1997). Ant gardens: interspecific recognition in parabiotic ant species. Behavioral Ecology and Sociobiology, 40: 87-93. doi: 10.1007/s00265 0050319

Orivel, J. & Leroy, C. (2011). The diversity and ecology of ant gardens (Hymenoptera: Formicidae; Spermatophyta: Angiospermae). Myrmecological News, 14: 75-85.

Rico-Gray, V. & Oliveira, P.S. (2007). The Ecology and Evolution of Ant-Plant Interaction. Chicago: Chicago University Press, 320 p.

Romero, G. & Izzo, T. (2004). Leaf damage induces ant recruitment in the Amazonian ant-plant Hirtella myrmecophila. Journal of Tropical Ecology, 20: 675-682. doi: 10.1017/S0266467404001749

Schupp, E.W. & Feener, D.H. (1991). Phylogeny, lifeform, and habitat dependence of ant-defended plants in Panamanian Forest. In: Huxley, C.R. & Cutler, D.F. (eds.). Ant-plant interactions (p.157-197).Oxford: Oxford University Press.

Stanton, M.L. (2003). Interacting guilds: moving beyond the pairwise perspective. The American Naturalist, 162: S10-23. doi: 10.1086/378646

Ule, E. (1901) Ameisengarten im Amazonasgebeit. Botanische Jahrbucher für Systematik, Pflanzengeschichte und Pflanzen-geographien, 30: 45-51.

Vantaux, A., Dejean, A., Dor, A. & Orivel, J. (2007). Parasitism versus mutualism in the ant-garden parabiosis between Camponotus femoratus and Crematogaster levior. Insectes Sociaux, 54: 95-99. doi: 10.1007/s00040-007-0914-0

Vicente, R.E., Dátilo, W. & Izzo, T.J. (2014). Differential recruitment of Camponotus femoratus (Fabricius) ants in response to ant garden herbivory. Neotropical Entomology, 43: 519-525. doi: 10.1007/s13744-014-0245-6

Youngstead, E., Nojima, S., Harbelein, C., Schultz, S. & Schal, C. (2008). Seed odor mediates an obligate ant-plant mutualism in Amazonian rainforest. Proceedings of National Academy of Sciences USA, 105: 4571-4575. doi: 10.1073/pnas.0708643105

Yu, D.W. (1994). The structural role of epiphytes in ant gardens. Biotropica, 26: 222-226.




DOI: http://dx.doi.org/10.13102/sociobiology.v64i3.1219

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2016: 0.699