Many plants interact with carnivores as an indirect defence against herbivores. The release of volatile organic compounds (VOCs) and the secretion of extrafloral nectar (EFN) are induced by insect feeding, a response that is mediated by the plant hormone, jasmonic acid. Although VOCs mainly attract predatory mites and parasitic wasps, while EFN mainly attracts ants, many more animal-plant interactions are influenced by these two traits. Other traits involved in defensive tritrophic interactions are cellular food bodies and domatia, which serve the nutrition and housing of predators. They are not known to respond to herbivory, while food body production can be induced by the presence of the mutualists. Interactions among the different defensive traits, and between them and other biotic and abiotic factors exist on the genetic, physiological, and ecological levels, but so far remain understudied. Indirect defences are increasingly being discussed as an environmentally-friendly crop protection strategy, but much more knowledge on their fitness effects under certain environmental conditions is required before we can understand their ecological and evolutionary relevance, and before tritrophic interactions can serve as a reliable tool in agronomy.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/j.1469-8137.2007.02330.x

Indirect defence via tritrophic interactions.

▪ Abstract Protective ant-plant interactions, important in both temperate and tropical communities, are increasingly used to study a wide range of phenomena of general interest. As antiherbivore defenses “worn on the outside,” they pose fewer barriers to experimentation than do direct (e.g., chemical) plant defenses. This makes them tractable models to study resource allocation to defense and mechanisms regulating it. As multi-trophic level interactions varying in species specificity and impact on fitness of participants, ant-plant-herbivore associations figure prominently in studies of food-web structure and functioning. As horizontally transmitted mutualisms that are vulnerable to parasites and “cheaters,” ant-plant symbioses are studied to probe the evolutionary dynamics of interspecies interactions. These symbioses, products of coevolution between plants and insect societies, offer rich material for studying ant social evolution in novel contexts, in settings where colony limits, resource supply, and ...

Protective ant-plant interactions as model systems in ecological and evolutionary research.

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (-23.7%), leaf production (-51.8%), and reproduction (-24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant-plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants.

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses

1. Shrubs of Caryocar brasiliense are intensively visited by many ant species in the cerrado vegetation of south-east Brazil. Ants collect nectar from the extrafloral nectaries (EFNs) located on the buds at the apex of the plant.



2. The proportion of C. brasiliense shrubs occupied by ants greatly surpassed that of neighbouring plants without EFNs and this resulted in many more termites being attacked and removed on this plant than on plants lacking EFNs. Ant attacks on Caryocar were more frequent near the EFNs.



3. Ant-exclusion experiments with Caryocar shrubs revealed that ants significantly reduce the infestation levels by the butterfly Eunica bechina, the sucking bud Edessa rufomarginata, the bud-destroying fly Prodiplosis floricola and by a stem-galling wasp. Ants had no effect on the infestation by a leaf-galling wasp.



4. Control (ants present) and treatment (ants excluded) plants produced equal numbers of buds but flower and initial fruit production was significantly greater for ant-visited plants. Higher abortion rates of initial fruits by control plants resulted in similar final fruit and seed sets for plants in either experimental category.



5. The extremely low fertility of cerrado soils is suggested as a possible factor constraining the ability of Caryocar shrubs to provide the resources necessary for growth and development of their heavy fleshy fruits. Higher production of initial fruits by ant-visited shrubs would be neutralized by competition among developing fruits and subsequent abortion.



6. Possible ant-derived benefits to C. brasiliense include: protection of vegetative tissues during plant growth, larger floral display and increased attractiveness to bat pollinators, increased male contribution to fitness through pollen donation and selective abortion of genetically inferior progeny as the maternal investment is adjusted to match available resources.

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The ecological function of extrafloral nectaries : herbivore deterrence by visiting ants and reproductive output in Caryocar brasiliense (Caryocaraceae)

1. This study examines the anti-herbivore effect of ants visiting the extrafloral nectaries (EFNs) of Opuntia stricta (Cactaceae) and its possible influence on the plant’s reproductive output in Mexican coastal sand dunes. Opuntia’s EFNs are located in the areoles of the developing tissue of emerging cladodes and flower buds.



2. Ants visited the EFNs of O. stricta on a round-the-clock basis. The associated ant assemblage was formed by nine species distributed in four subfamilies, and the species composition of the principal ant visitors changed markedly from day to night period.



3. Cladodes of control (ants present) and treatment (ants excluded) plants of Opuntia were equally infested by sucking bugs and mining dipterans. Damage to buds by a pyralid moth, however, was significantly higher on treatment than on control plants. Ant visitation to Opuntia’s EFNs translated into a 50% increase in the plant’s reproductive output, as expressed by the number of fruits produced by experimental control and treatment branches. Moreover, fruit production by ant-visited branches was positively and significantly associated with the mean monthly rate of ant visitation to EFNs.



4. This is the first demonstration of ant protection leading to increased fruit set in the Cactaceae under natural conditions. Although the consequences of damage by sucking and mining insects remain unclear for Opuntia, the results show how the association of EFNs with vulnerable reproductive plant organs can result in a direct ant-derived benefit to plant fitness.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-2435.1999.00360.x

Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae)

There are many definitions of extrafloral nectaries (EFNs), but those that define EFNs as nectaries that are not involved in pollination (e.g. Fiala & Maschwitz 1991) could be the most simple and correct- EFNs have been recorded from more than 93 angiosperm families (Elias 1983, Koptur 1992) in at least 2200 species (Keeler 1989). These glands secrete nectar that attracts many ant taxa, mainly Myrmicinae, Formicinae and Dolichoderinae (Oliveira & Brandao 1991). Many authors have demonstrated that the associations between ants and EFNs are beneficial to the plant. In these cases ants feed on nectar and protect the plants against several types of herbivores (Bentley 1977, Horvitz & Schemske 1984,. Koptur 1984). Nevertheless, Boecklen (1984), O'Dowd & Catchpole (1983) and Rashbrook

Vanderlei Berto

Papers

Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae)