Ant–Plant Mutualisms

Abstract

Ants and plants are engaged in thousands of mutualisms, which can be categorised in two major groups: dispersal and defence mutualisms. Myrmecochory, the dispersal of plant seeds by ants, is usually facilitated by the elaiosome, an appendix of the seed that is used as a reward. Because elaiosomes represent a nutritional supplement rather than a full diet, dispersal mutualisms are facultative ones. Only in ant‐gardens, the ants use the dispersed epiphytes as support to construct their carton nests, and these mutualisms tend to be obligate ones. In facultative defensive mutualisms, plants provide ant rewards, such as cellular food bodies (FBs) or extrafloral nectar (EFN), to foraging ants that serve as an indirect defence against herbivores. Obligate defensive mutualisms, by contrast, are based on the provisioning of nesting space. Ants dominate most terrestrial ecosystems. Owing to their mobility and social structure, they appear perfect partners for plant dispersal and defence.

Key Concepts:

  • Plants can benefit from indirect defence that is mediated through the third trophic level.

  • Ants are the dominant animal group in terrestrial ecosystem and – being common predators – have a high potential to defend plants against herbivores.

  • Plants can provide food resources or nesting space to ants in order to increase their presence and capacity to function as defenders.

  • Ants can also transport seeds and thereby function in dispersal.

  • Obligate ant–plant mutualisms reach high levels of reciprocal specialisations.

  • The evolutionary origins of most interactions remain to be investigated.

Keywords: ant‐garden; ant–plant; dispersal; domatium; elaiosome; extrafloral nectar; food body; indirect defence; myrmecophyte

Figure 1.

Obligate defensive ant–plant mutualisms. In the majority of obligate ant–plant mutualisms, specialised defensive ant species are housed and nourished by specialised myrmecophytes, which depend on the ant‐mediated defence for their survival. Ant‐exclusion experiments revealed similarly dramatic effects on leaf damage for Acacia hindsii in Mexico (a) with ants; (b) without ants; and for Macaranga bancana in Malaysia ((c), left plant with ants, right plant after six weeks of ant exclusion). Ants are nourished commonly by cellular food bodies (FBs) ((d), Pseudomyrmex gracilis worker harvesting an FB of Acacia cornigera) and extrafloral nectar (EFN) ((e), Pseudomyrmex peperi ants feeding on EFN of Acacia hindsii). FBs can be produced on different plant parts ((f), FBs on the pouches below leaf stalks of Cecropia mexicana; (g, i), FBs under recurved stipules of M. bancana and (h), FBs on upper surfaces of stipules of Macaranga hosei). In several systems where EFN is missing, scale insects are kept as a third partner ((g), Crematogaster sp. workers attending scale insects within the hollow twig of M. bancana, which serves as domatium in this species). Reproduced in part from Heil M , with permission from Wiley‐Blackwell.

close

References

Beattie AJ (1985) The Evolutionary Ecology of Ant–Plant Mutualisms. Cambridge, England: Cambridge University Press.

Blüthgen N, Schmit‐Neuerburg V, Engwald S and Barthlott W (2001) Ants as epiphyte gardeners: comparing the nutrient quality of ant and termite canopy substrates in a Venezuelan lowland rain forest. Journal of Tropical Ecology 17: 887–894.

Brew CR, O'Dowd DJ and Rae ID (1989) Seed dispersal by ants: behaviour‐releasing compounds in elaiosomes. Oecologia 80: 490–497.

Brouat C, Garcia N, Andary C and McKey D (2001) Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant‐plant mutualism. Proceedings of the Royal Society of London, Series B 268: 2131–2141.

Buono RA, de Oliveira AB and Paiva EA (2008) Anatomy, ultrastructure and chemical composition of food bodies of Hovenia dulcis (Rhamnaceae). Annals of Botany 101: 1341–1348.

Chamberlain SA and Holland JN (2009) Quantitative synthesis of context dependency in ant‐plant protection mutualisms. Ecology 90: 2384–2392.

Clement LW, Köppen S, Brand WA and Heil M (2008) Strategies of a parasite of the ant‐Acacia mutualisms. Behavioral Ecology and Sociobiology 26: 953–962.

Darwin C (1877) On the glandular bodies on Acacia sphaerocephala and Cecropia peltata serving as food for ants. Journal of the Linnean Society of London Botany 15: 398–409.

Davidson DW (1988) Ecological studies of neotropical ant gardens. Ecology 69: 1138–1152.

Edwards DP, Hassall M, Sutherland WJ and Yu DW (2006) Selection for protection in an ant‐plant mutualism: host sanctions, host modularity and the principal‐agent game. Proceedings of the Royal Society of London, Series B: Biological Sciences 273: 595–602.

Feldhaar H, Fiala B, bin Hashim R and Maschwitz U (2000) Maintaining an ant‐plant symbiosis: secondary polygyny in the Macaranga triloba‐Crematogaster sp association. Naturwissenschaften 87: 408–411.

Fischer RC, Richter A, Hadacek F and Mayer V (2008) Chemical differences between seeds and elaiosomes indicate an adaptation to nutritional needs of ants. Oecologia 155: 539–547.

González‐Teuber M and Heil M (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signaling & Behavior 4: 809–813.

González‐Teuber M, Pozo MJ, Muck A et al. (2010) Glucanases and chitinases as causal agents in the protection of Acacia extrafloral nectar from infestation by phytopathogens. Plant Physiology 152: 1705–1715.

Heil M (2008) Indirect defence via tritrophic interactions. New Phytologist 178: 41–61.

Heil M (2009) Damaged‐self recognition in plant herbivore defence. Trends in Plant Science 14: 356–363.

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

Heil M, Fiala B, Linsenmair KE et al. (1997) Food body production in Macaranga triloba (Euphorbiaceae): a plant investment in anti‐herbivore defence via mutualistic ant partners. Journal of Ecology 85: 847–861.

Heil M, González‐Teuber M, Clement LW et al. (2009) Divergent investment strategies of Acacia myrmecophytes and the coexistence of mutualists and exploiters. Proceedings of the National Academy of Sciences of the USA 106: 18091–18096.

Heil M, Koch T, Hilpert A et al. (2001) Extrafloral nectar production of the ant‐associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proceedings of the National Academy of Sciences of the USA 98: 1083–1088.

Heil M and McKey D (2003) Protective ant‐plant interactions as model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution, and Systematics 34: 425–453.

Heil M, Orona‐Tamayo D, Eilmus S et al. (2010) Chemical communication and coevolution in an ant‐plant mutualism. Chemoecology 20: 63–74.

Heil M, Rattke J and Boland W (2005) Post‐secretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308: 560–563.

Herms DA and Mattson WJ (1992) The dilemma of plants: to grow or to defend. Quarterly Review of Biology 67: 283–335.

Jackson DE (2009) Nutritional ecology: a first vegetarian spider. Current Biology 19: R894–R895.

Kaufmann E and Maschwitz U (2006) Ant‐gardens of tropical Asian rainforests. Naturwissenschaften 93: 216–227.

Kautz S, Lumbsch HT, Ward PS and Heil M (2009) How to prevent cheating: a digestive specialization ties mutualistic plant‐ants to their ant‐plant partners. Evolution 63: 839–853.

Lengyel S, Gove AD, Latimer AM et al. (2009) Ants sow the seeds of global diversification in flowering plants. PLoS ONE 4: e5480.

Marussich WA (2006) Testing myrmecochory from the ant's perspective: the effects of Datura wrightii and D. discolor on queen survival and brood production in Pogonomyrmex californicus. Insectes Sociaux 53: 403–411.

McKey D (1974) Adaptive patterns in alkaloid physiology. American Naturalist 108: 305–320.

O'Dowd DJ (1982) Pearl bodies as ant food: an ecological role for some leaf emergences of tropical plants. Biotropica 14: 40–49.

Orivel J and Leroy C (in press) The diversity and ecology of ant gardens. Myrmecological News.

Raine NE, Gammans N, Macfadyen IJ et al. (2004) Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant‐plant. Ecological Entomology 29: 345–352.

Rico‐Gray V and Oliveira PS (2007) The Ecology and Evolution of Ant‐Plant Interactions. Chicago and London: The University of Chicago Press.

Rosumek FB, Silveira FAO, Neves FD et al. (2009) Ants on plants: a meta‐analysis of the role of ants as plant biotic defenses. Oecologia 160: 537–549.

Schmit‐Neuerburg V and Blüthgen N (2007) Ant‐garden epiphytes are protected against drought in a Venezuelan lowland rain forest. Ecotropica 13: 93–100.

Treseder KK, Davidson DW and Ehleringer JR (1995) Absorption of ant‐provided carbon‐dioxide and nitrogen by a tropical epiphyte. Nature 375: 137–139.

Webber BL, Abaloz BA and Woodrow IE (2007) Myrmecophilic food body production in the understorey tree, Ryparosa kurrangii (Achariaceae), a rare Australian rainforest taxon. New Phytologist 173: 250–263.

Youngsteadt E, Nojima S, Haberlein C et al. (2008) Seed odor mediates an obligate ant‐plant mutualism in Amazonian rainforest. Proceedings of the National Academy of Sciences of the USA 105: 4571–4575.

Yu DW and Pierce NE (1998) A castration parasite of an ant‐plant mutualism. Proceedings of the Royal Society of London Series B: Biological Sciences 265: 375–382.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Heil, Martin(Sep 2010) Ant–Plant Mutualisms. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022558]