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

Abstract

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.

A phylogenetic perspective on the association between ants (Hymenoptera: Formicidae) and black yeasts (Ascomycota: Chaetothyriales)

“…In addition, a recently described species, Arthrocladium tardum (Trichomeriaceae), has been isolated both from a domatium of Leonardoxa africana occupied by the ant Petalomyrmex phylax in Cameroon and from decaying coconut shells in Brazil [6]. Although some Chaetothyriales strains are clearly mutualistic symbionts of ants [28,33,34], our study indicates that ant nests can be colonized by opportunistic species and that Chaetothyriales taxa might display exceptional dispersal capacities and surprising ubiquity. In the future, it will be most useful to investigate the degree of specialization of the interactions between particular ant and fungal partners in order to interpret the phylogenetic pattern in evolutionary terms.…”

“…Fungal patches also contain nematodes, bacteria and spores of opportunistic fungi [30][31][32]. Detailed functional investigation of a few systems revealed that domatia patches are manured and used as a food source by the ants [33,34] in a way reminiscent of fungal culture by attine ants. Ants and plants living in symbiosis are scattered throughout their respective phylogenies and have evolved many times independently, at least 40 and 158 times in their respective lineages [24,35].…”

Community analysis of microbial sharing and specialization in a Costa Rican ant–plant–hemipteran symbiosis

“…Recent studies have found intimate cofeeding relationships between Chaetothyriales fungi and plant-ants, in which the ants fertilize the fungi and also consume it [11,44]. In other ant-plant symbioses, there has been some evidence for distinct fungal communities associated with different ant species (e.g.…”

“…Hemipterans were early and enduring models for studying how animals can obtain such key nutrients from microbes [9], but the broad relevance of bacteria and fungi as potential sources of nutrition for ants, which are typically omnivorous, was recognized only recently [10,11]. Most phloem-feeding hemipterans are associated with just one or a few highly specialized intracellular bacteria that are vertically transmitted, i.e.…”

The interactions of ants with their biotic environment

“…Ants also interact with Chaetothyriales fungi, either as part of the carton nest building process where arboreal ants use fungal hyphae to strengthen the nest or trap insects ([30,85], figure 1m) Chaetothyriales seem to be cultivated by ants and are involved in a complex trophic mutualism where the ants (especially larvae) feed on the fungi, which they actively fertilize by defecation [86], and the fungi play a role in nutrient recycling as well as facilitating nutrient uptake by breaking down materials [87]. In this special feature, Vasse et al [88] show that ant/Chaetothyriales interactions evolved multiple times and that carton nest fungi and domatium fungi form different lineages.…”