The trophic structure of tropical ant–plant–herbivore interactions: community consequences and coevolutionary dynamics

McKey, Doyle; Gaume, Laurence; Brouat, Carine; Giusto, Bruno Di; Pascal, Laurence; Debout, Gabriel; Dalecky, Ambroise; Heil, Martin

doi:10.1017/cbo9780511541971.017

Cited by 22 publications

(21 citation statements)

References 109 publications

(147 reference statements)

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“…Ants and plants are among the most dominant taxa in tropical ecosystems, and the ecological importance of their mutualistic interactions is brought to light by two considerations: these interactions structure food webs [1] and the mutualistic benefits exchanged can convey ecological advantages to the partners [2]. Yet the nutritional ecology of these interactions is still poorly understood [3].…”

Section: Introductionmentioning

confidence: 99%

Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions

et al. 2012

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Usually studied as pairwise interactions, mutualisms often involve networks of interacting species. Numerous tropical arboreal ants are specialist inhabitants of myrmecophytes (plants bearing domatia, i.e. hollow structures specialized to host ants) and are thought to rely almost exclusively on resources derived from the host plant. Recent studies, following up on century-old reports, have shown that fungi of the ascomycete order Chaetothyriales live in symbiosis with plant-ants within domatia. We tested the hypothesis that ants use domatia-inhabiting fungi as food in three ant -plant symbioses: Petalomyrmex phylax/Leonardoxa africana, Tetraponera aethiops/Barteria fistulosa and Pseudomyrmex penetrator/ Tachigali sp. Labelling domatia fungal patches in the field with either a fluorescent dye or 15 N showed that larvae ingested domatia fungi. Furthermore, when the natural fungal patch was replaced with a piece of a 15 N-labelled pure culture of either of two Chaetothyriales strains isolated from T. aethiops colonies, these fungi were also consumed. These two fungi often co-occur in the same ant colony. Interestingly, T. aethiops workers and larvae ingested preferentially one of the two strains. Our results add a new piece in the puzzle of the nutritional ecology of plant-ants.

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Section: Introductionmentioning

confidence: 99%

Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions

et al. 2012

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“…In non-symbiotic ant-plant interactions, in which ants visit plants but maintain colonies elsewhere, coccoids and other hemipterans can provide indirect benefits to plants by attracting defensive ants (see review in Styrsky and Eubanks [2007]). However, it has been argued that in symbiotic ant-plant associations, coccoids impose greater direct costs than indirect benefits to the host plant (e.g., Becerra and Venable 1989), partly because host plants could better control their level of investment in ants by producing food for ants directly (McKey et al 2005). …”

Section: Introductionmentioning

confidence: 99%

Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree

Pringle

Dirzo

Gordon

2011

Ecology

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Abstract. The net benefits of mutualism depend directly on the costs and effectiveness of mutualistic services and indirectly on the interactions that affect those services. We examined interactions among Cordia alliodora myrmecophytic trees, their symbiotic ants Azteca pittieri, coccoid hemipterans, and foliar herbivores in two Neotropical dry forests. The tree makes two investments in symbiotic ants: it supplies nesting space, as domatia, and it provides phloem to coccoids, which then produce honeydew that is consumed by ants. Although higher densities of coccoids should have higher direct costs for trees, we asked whether higher densities of coccoids can also have higher indirect benefits for trees by increasing the effectiveness of ant defense against foliar herbivores. We found that trees benefited from ant defense against herbivores. Ants defended trees effectively only when colonies reached high densities within trees, and ant and coccoid densities within trees were strongly positively correlated. The benefits of reduced foliar herbivory by larger ant colonies were therefore indirectly controlled by the number of coccoids. Coccoid honeydew supply also affected per capita ant aggression against tree herbivores. Ants experimentally fed a carbohydrate-rich diet, analogous to sugar obtained from coccoids, were more aggressive against caterpillars per capita than ants fed a carbohydrate-poor diet. Ant defense was more effective on more valuable and vulnerable young leaves than on older leaves. Young domatia, associated with young leaves, contained higher coccoid densities than older domatia, which suggests that coccoids may also drive spatially favorable ant defense of the tree. If higher investments by one mutualistic partner are tied to higher benefits received from the other, there may be positive feedback between partners that will stabilize the mutualism. These results suggest that higher investment by trees in coccoids leads to more effective defense by ants against the tree's foliar herbivores.

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“…Ant -plant interactions have a structuring role in tropical arboreal communities through their impact on populations of other arthropods and thereby on food webs [5 -7]. The diverse feeding behaviours of tropical arboreal ants predispose them to be protective mutualists of plants: they prey on many arthropod enemies of plants, they are attracted by energy-rich, solid or liquid food rewards offered by plants and they often live in symbiosis with other organisms, such as hemipteran trophobionts or bacteria that help them adapt to the nutritional imbalances that dependence on plant-produced rewards often entails [5,7,8]. In particular, diets of tropical arboreal ants are often characterized by high C : N ratios, reflecting caloric richness relative to paucity of nitrogen and mineral nutrients [5,6].…”

Section: Introductionmentioning

confidence: 99%

Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen

et al. 2010

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In ant -plant symbioses, plants provide symbiotic ants with food and specialized nesting cavities (called domatia). In many ant -plant symbioses, a fungal patch grows within each domatium. The symbiotic nature of the fungal association has been shown in the ant-plant Leonardoxa africana and its protective mutualist ant Petalomyrmex phylax. To decipher trophic fluxes among the three partners, food enriched in 13 C and 15 N was given to the ants and tracked in the different parts of the symbiosis up to 660 days later. The plant received a small, but significant, amount of nitrogen from the ants. However, the ants fed more intensively the fungus. The pattern of isotope enrichment in the system indicated an ant behaviour that functions specifically to feed the fungus. After 660 days, the introduced nitrogen was still present in the system and homogeneously distributed among ant, plant and fungal compartments, indicating efficient recycling within the symbiosis. Another experiment showed that the plant surface absorbed nutrients (in the form of simple molecules) whether or not it is coated by fungus. Our study provides arguments for a mutualistic status of the fungal associate and a framework for investigating the previously unsuspected complexity of food webs in ant -plant mutualisms.

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The trophic structure of tropical ant–plant–herbivore interactions: community consequences and coevolutionary dynamics

Cited by 22 publications

References 109 publications

Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions

Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant–plant interactions

Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree

Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen

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