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.

Figure 1.

Microscopic observation of fluorescence under UV light after labelling of fungal patches with calcofluor. (a) Bluish hyphae from fungal patch in a domatium of Tachigali sp. occupied by the ant Pseudomyrmex penetrator. Note that the plant cells emit a faint yellowish fluorescence distinct from that emitted by the fungal patch. (b) Same as panel (a), for the ant–plant system Tetraponera aethiops/Barteria fistulosa. (c) Cluster of bluish hyphae from an infrabuccal pellet of a Tetraponera aethiops worker. (d) Part of the gut of a large Tetraponera aethiops larva emitting, under UV light (right panel), a bluish fluorescence similar to that of the fungal patch; left panel shows same under white light. (e) Same as panel (d), for a small Pseudomyrmex penetrator larva. Scale bars: (a–c) 50 µm, (d,e) 0.5 mm.

Figure 2.

Wavelength and intensity of the most intense fluorescence obtained by microspectrofluorometry under excitation at 365.5–368.5 nm for hyphae of the fungal patch labelled with calcofluor (red), hyphae of the fungal patch in control domatia (pink), plant cell from the inner wall of a domatium in which the fungal patch was labelled with calcofluor (light blue), part of larval gut showing bluish fluorescence (black), hyphae in infrabuccal pellet of workers (and one winged female; dark blue) and hyphae in larval trophothylax (brown), for the three study systems. Means ± s.e. The inserts within each graph show examples of fluorescence emission spectra for each of the above items.

Figure 3.

Difference of δ¹⁵N between colonies that had their fungal patch exposed to ¹⁵N-glycine and control colonies. Horizontal lines represent median, boxes represent first and third quartiles, and whiskers represent first and ninth deciles. *p < 0.05, **p < 0.01, n.s. not significant.