Distinctive fungal communities in an obligate African ant-plant mutualism

Abstract

Three ant species nest obligately in the swollen-thorn domatia of the African ant-plant Vachellia (Acacia) drepanolobium, a model system for the study of ant-defence mutualisms and species coexistence. Here we report on the characteristic fungal communities generated by these ant species in their domatia. First, we describe behavioural differences between the ant species when presented with a cultured fungal isolate in the laboratory. Second, we use DNA metabarcoding to show that each ant species has a distinctive fungal community in its domatia, and that these communities remain characteristic of the ant species over two Kenyan sampling locations separated by 190 km. Third, we find that DNA extracted from female alates of Tetraponera penzigi and Crematogaster nigriceps contained matches for most of the fungal metabarcodes from those ant species' domatia, respectively. Fungal hyphae and other debris are also visible in sections of these alates' infrabuccal pockets. Collectively, our results indicate that domatium fungal communities are associated with the ant species occupying the tree. To the best of our knowledge, this is the first record of such ant-specific fungal community-level differences on the same myrmecophytic host species. These differences may be shaped by ant behaviour in the domatia, and by ants vectoring fungi when they disperse to establish new colonies. The roles of the fungi with respect to the ants and their host plant remain to be determined.

Keywords: Tetraponera; Vachellia (Acacia) drepanolobium; fungi; insects; metabarcoding; species interactions.

Figure 1.

(a) T. penzigi workers on domatium. (b) V. drepanolobium sapling. (c) Resident ant colonies defend host plants against damage by large mammalian herbivores. (d) Kitengela and Mpala field sites are located approximately 190 km apart. (e,f) T. penzigi ants (TP) removed significantly more fungus than either C. mimosae ants (CM) or C. nigriceps ants (CN). Removal of agar growth medium for Phoma fungal isolates was negligible.

Figure 2.

(a) Kenyan domatium communities differ in taxonomic diversity compared with leaf sample communities and greenhouse domatium communities. Error bars show standard errors. (b) Non-metric multidimensional scaling (NMDS) based on Sørensen distances for rarefied dataset. Greenhouse domatia and leaf samples were distinct from Kenyan domatium samples. Kenyan domatium communities also differed among ant species. (c) Relative abundances of fungi aggregated to class differ between sample types and between ant occupants. Each column represents one sample. (d) Bipartite graph of ant species against most abundant fungal OTUs in rarefied dataset. Connections reflect sequence counts.

Figure 3.

(a) Proportion of each Kenyan domatium's sequences that were also recovered from the three pooled T. penzigi alate samples (i) and the 12 pooled C. nigriceps alate samples (ii). Sagittal view of (b,c) T. penzigi and (d,e) C. nigriceps alates showing debris in the infrabuccal pockets (arrowed). Higher magnification images in (c) and (e) show details of debris present in the pocket.