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

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.     

The evolution of intermediate castration virulence and ant coexistence in a spatially structured environment

Theory suggests that spatial structuring should select for intermediate levels of virulence in parasites, but empirical tests are rare and have never been conducted with castration (sterilizing) parasites. To test this theory in a natural landscape, we construct a spatially explicit model of the symbiosis between the ant-plant Cordia nodosa and its two, protecting ant symbionts, Allomerus and Azteca . Allomerus is also a castration parasite, preventing fruiting to increase colony fecundity. Limiting the dispersal of Allomerus and host plant selects for intermediate castration virulence. Increasing the frequency of the mutualist, Azteca , selects for higher castration virulence in Allomerus , because seeds from Azteca -inhabited plants are a public good that Allomerus exploits. These results are consistent with field observations and, to our knowledge, provide the first empirical evidence supporting the hypothesis that spatial structure can reduce castration virulence and the first such evidence in a natural landscape for either mortality or castration virulence.     

Facultative polygyny in the plant-ant Petalomyrmex phylax (Hymenoptera: Formicinae): sociogenetic and ecological determinants of queen number

In polygynous ants it has been proposed that the coexistence of several queens in a colony evolved as a response to ecological, social and genetic parameters. We present demographic, histological and genetic data showing that the plant-ant Petalomyrmex phylax is facultatively and secondarily polygynous. Polygyny is functional, lowers the reproductive output per queen, and is a kin-selected trait as new queens accepted in polygynous colonies are highly related females that never left their natal colony. The degree of polygyny varies according to a geographical gradient. Northern colonies can be strongly polygynous, while at the southern edge of the species' distribution, colonies are almost exclusively monogynous. However, ecological studies of the host-plant populations revealed that this cline could not be explained by variations in the degree of nest site limitation. We discuss selective costs and benefits associated with these social structures, and propose that this cline may result from historical processes such as selection of a more dispersive strategy along a colonization front.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 133–151.     

Diversity, evolutionary specialization and geographic distribution of a mutualistic ant-plant complex: Macaranga and Crematogaster in South East Asia

The most conspicuous and species-rich ant-plant mutualism in the Malesian region is found in the important pioneer tree genus Macaranga , yet little is known about the identities or community ecology of the species involved. Our studies have revealed a far more complex system than previously thought. This paper presents the first extensive investigation in the whole distribution area of myrmecophytic Macaranga. All ant-inhabited species were restricted to the moister parts of SE Asia: Peninsular Malaysia, South and East Thailand, Sumatra and Borneo. We found a rather strict and similar altitudinal zonation of myrmecophytic Macaranga species in all regions. Here we focus on the majority of the 19 Macaranga species obligatorily associated with ants of the genus Crematogaster. We identified a total of 2163 ant queens which belonged to at least eight (morpho)species of the small subgenus Decacrema as well as to one non-Decacrema (probably from Atopogyne ). The ant species were not randomly distributed among the Macaranga species but distinct patterns of associations emerged. Despite common sympatric distribution of Macaranga species, in most cases a surprisingly high specificity of ant colonization was maintained which was, however, often not species-specific but groups of certain plant species with identical ant partners could be found. These colonization patterns usually but not always mirror existing taxonomic sections within the genus Macaranga. Possible mechanisms of specificity are discussed. The results are compared with other ant-plant mutualisms.     

Characterization of polymorphic microsatellite loci in the tropical ant‐plant Leonardoxa africana (Fabaceae: Caesalpinioideae)

Ten microsatellite loci were isolated from the African ant‐plant Leonardoxa africana (Fabaceae: Caesalpinioideae). They differentiate the two most divergent subspecies of this polytypic complex, L. a. africana and L. a. gracilicaulis, showing promise for the study of gene flow. In each of these two subspecies, high levels of within‐population variation were observed, with a number of alleles ranging from one to 10 in ssp. africana and from one to 7 in ssp. gracilicaulis, and heterozygosity from 0 to 0.933 in ssp. africana and to 0.867 in ssp. gracilicaulis. All loci amplified successfully in the two other subspecies of L. africana.     

Interspecific variation in the defensive responses of ant mutualists to plant volatiles

In ant–plant mutualist systems, ants patrol their host plants and search for herbivores. Such patrolling can be inefficient, however, because herbivore activity is spatio-temporally unpredictable. It has been proposed that rapid and efficient systems of communication between ants and plants, such as volatile compounds released following herbivory, both elicit defensive responses and direct workers to sites of herbivore activity. We performed bioassays in which we challenged colonies of two Amazonian plant-ants, Azteca sp. and Pheidole minutula , with extracts of leaf tissue from (1) their respective host-plant species ( Tococa bullifera and Maieta guianensis , both Melastomataceae), (2) sympatric ant-plants from the Melastomataceae, and (3) two sympatric but non-myrmecophytic Melastomataceae. We found that ants of both species responded dramatically to host-plant extracts, and that these responses are greater than those to sympatric myrmecophytes. Azteca sp. also responded to non-myrmecophytes with an intensity similar to that of sympatric ant-plants. By contrast, the response of P. minutula to any non-myrmecophytic extracts was limited. These differences may be driven in part by interspecific differences in nesting behaviour; although P. minutula only nests in host plants, Azteca sp. will establish carton satellite nests on nearby plants. We hypothesize that Azteca sp. must therefore recognize and defend a wider array of species than P. minutula .  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 241–249.     

Cospeciation of ants and plants

Cospeciation, in which both parties of an ecological interaction speciate in parallel with each other, has rarely been reported in biotic associations except the cases for host–parasite interaction. Many tropical plants house ants and thereby gain protection against herbivores. Although these ant–plant symbioses have been regarded as classical cases of coevolved mutualism, no evidence of cospeciation has been documented. The Asian ant–plant association between Crematogaster ants and Macaranga plants is highly species specific and the molecular phylogeny of the ants parallels the plant phylogeny, reflecting history of cospeciation. Evidence is presented that this association has been maintained over the past seven million years. Phylogeographic patterns of 27 ants from two Macaranga species suggest that allopatric cospeciations are still in progress in Asian wet tropics.     

A reassessment of the relations in Malaysia between ants (Crematogaster) on trees (Leptospermum and Dacrydium) and epiphytes of the genus Dischidia (Asclepiadaceae) including 'ant-plants'

Three species of epiphytic Dischidia have been investigated in terms of their relationship to ants on trees. Two species, D. parvifolia and D. astephana , are associated with ants and trees in montane areas. A clear association has been found between ants of the genus Crematogaster and the tree Leptospermum flavescens. This relationship is complex and probably both organisms benefit from the association. The ants live in tunnels in the wood of the major branches and the trunk, and the entire tree is occupied by one ant colony. Trees occupied by ants are maintained by the ants substantially clear of epiphytes other than the two species of Dischidia. The potential benefits to the tree and to the ants of this association are noted. The roots of D. astephana and D. parvifolia penetrate into the cavities of these ant nests and presumably gain nutrients from waste in the ant nests. Both Dischidia species are effectively scavenging upon the waste material from the ant-tree association. The leathery dome-shaped leaves of D. astephana are not vital to the development of the scavenging habit as D. parvifolia has lens-shaped leaves, but may offer some advantage to D. astephana by the uptake of nutrients from waste deposited by the ants under the dome-shaped leaves by interception of stem flow and by uptake of gaseous waste. Ants do not nest under these leaves. Seeds of these species of Dischidia are taken by ants into the central woody area of the ant nest where they germinate. Both Leptospermum and Dischidia can be visualized as showing adaptations to a nutient-deficient tropical montane environment. These adaptations are discussed as is the need for reassessment in this genus of the term 'ant-plant', and the need for wider recognition of the 1ant-tree' relationship between Crematogaster and Leptospermum.     

Production of food bodies on the reproductive organs of myrmecophytic Macaranga species (Euphorbiaceae): effects on interactions with herbivores and pollinators

In protective ant–plant mutualisms, plants offer ants food (such as extrafloral nectar and/or food bodies) and ants protect plants from herbivores. However, ants often negatively affect plant reproduction by deterring pollinators. The aggressive protection that mutualistic ants provide to some myrmecophytes may enhance this negative effect in comparison to plant species that are facultatively protected by ants. Because little is known about the processes by which myrmecophytes are pollinated in the presence of ant guards, we examined ant interactions with herbivores and pollinators on plant reproductive organs. We examined eight myrmecophytic and three nonmyrmecophytic Macaranga species in Borneo. Most of the species studied are pollinated by thrips breeding in the inflorescences. Seven of eight myrmecophytic species produced food bodies on young inflorescences and/or immature fruits. Food body production was associated with increased ant abundance on inflorescences of the three species observed. The exclusion of ants from inflorescences of one species without food rewards resulted in increased herbivory damage. In contrast, ant exclusion had no effect on the number of pollinator thrips. The absence of thrips pollinator deterrence by ants may be due to the presence of protective bracteoles that limit ants, but not pollinators, from accessing flowers. This unique mechanism may account for simultaneous thrips pollination and ant defense of inflorescences.