Fungal Parasites from the gardens of Leafcutter Ants.

Leafcutter Ants harvest vegetation from the tropical rainforests of South and Central America, which they then carry back to their nests and use as feed in fungal farms. Each species of Ant has its own unique species of food-fungus, and it is thought that the symbiotic relationship between the two has driven evolution within the group. The farms of the Ants are also infected by parasitic Fungi of the genus Escovopsis, which requires that the Ants constantly tend their farms, weeding out the parasitic Fungus before it overwhelms the colony. To date only two species have been described in the genus Escovopsis but it is thought that the group is more diverse, and it has been suggested that these parasites may be host specific, with each species of Ant having a species of parasitic Fungi that targets its nest.

In a paper published in the journal PLoS One on 20 December 2013, a team of scientists led by Juliana Augustin of the Departamento de Entomologia at the Universidade Federal de Viçosa, describe four new species of parasitic Fungi collected from the gardens and middens (external waste tips where unwanted material from the nests is dumped) of Leafcutter Ants from a tract of remnant subtropical Atlantic rainforest in Minas Gerais State, Brazil. Three of these parasites were placed in the genus Escovopsis, but one was considered sufficiently different to merit the erection of a new genus.

The first new species described is named Escovopsis moelleri, in honour of AFW Moeller, who first described and illustrated Fungi from the genus Escovopsis from Leafcutter Ants’ nests in 1893, although he did not formally name them. Escovopsis moelleri was originally isolated from the fungal gardens of the Leafcutter Ant Acromyrmex subterraneus molestans, and subsequently also found within colonies of Acromyrmex subterraneus subterraneus. Colonies of Escovopsis moelleri were fast-growing, reaching 5-6 cm in diameter on agar in 7 days at 25˚C. Spores developed on distinctive areal hyphae. 

Escovopsis moelleri, after 7 days on oatmeal agar, in 9 cm a diameter plate, at 25˚C. Augustin et al. (2013).

Escovopsis moelleri. (A–B) Growth habit, note stolons (long arrow) formed at the colony edge with rhizoids (short arrows) developing on the agar surface; (C–D) Details of conidiogenesis showing early development of the clavate vesicles (C, scale bar is 10 μm), and, a later stage covered with swollen, short-necked phialides (D, scale bar is 20 μm). Augustin et al. (2013).

Escovopsis moelleri. (A–D) Older stages of vesicle development showing darkening conidia with thickened rugose walls and apical caplike structures (arrows); note the short-lived or evanescent vesicle (D). All scale bars are 10 μm. Augustin et al. (2013).

 

Escovopsis moelleri: Details of conidiogenesis and spore morphology, as revealed by Critical-Point Drying SEM. (A) Branching and vesicle formation (scale bar is 10 μm); (B) detail of conidial morphology, with ornamentation and apical cap (arrows) (scale bar is 2 μm). Augustin et al. (2013).

The second new species described is named Escovopsis microspora, in reference to its small spores. It was originally isolated from nests of the Ant Acromyrmex subterraneus molestans, and subsequently also found in the nests of Acromyrmex subterraneus subterraneus and Acromyrmex niger. Colonies of Escovopsis microspora were fast-growing, reaching 4.5-5.5 cm in diameter on agar in 7 days at 25˚C. Spores developed on distinctive areal hyphae. 

Escovopsis microspora, after 7 days on oatmeal agar, in 9 cm a diameter plate, at 25˚C. Augustin et al. (2013).

Escovopsis microspora. (A–B) Details of conidiogenesis with clavate vesicles and swollen, short-necked phialides producing chains of conidia (scale bar is 20 μm); (C–D) Older evanescent vesicles with dark spores (scale bar is 10 μm); (E) Inset, showing conidial ornamentation (scale bar is 5 μm). Augustin et al. (2013).

The third new species described is named Escovopsis lentecrescens, in reference to its slow growth rate. Escovopsis lentecrescens was only isolated from the gardens of the Ant Acromyrmex subterraneus subterraneus. Colonies grew very slowly on agar, with no perceptible growth after 7 days at 25˚C, producing a 6-7mm diameter colony after 14 days and a 15-17 mm colony after 21 days.

 

Escovopsis lentecrescens, after 7 days on oatmeal agar, in 9 cm a diameter plate, at 25˚C. Augustin et al. (2013).

Escovopsis lentecrescens. (A–D) Stages of conidiogenesis, resulting in evanescent heads (D, arrow), all scale bars are 20 μm; (E–F) Paratype, faster-growing strain with more evanescent heads (scale bar is 10 μm), inset (G) showing detail of spore veil or coat (scale bar is 2 μm). Augustin et al. (2013).

The final new species is placed in a separate genus, Escovopsioides, meaning ‘similar to Escovopsis’, and given the specific name nivea, in reference to the snow white colouration of its colonies. Escovopsioides nivea was originally found growing on the middens and in the gardens of the Ant Acromyrmex subterraneus subterraneus, and subsequently also found in colonies of Acromyrmex subterraneus molestans and Acromyrmex niger. Colonies of Escovopsioides nivea were fast-growing, reaching 6-7 cm in diameter on agar in 7 days at 25˚C. 

Escovopsioides nivea, after 7 days on oatmeal agar, in 9 cm a diameter plate, at 25˚C. Augustin et al. (2013).

Escovopsioides nivea. (A–B) Conidiophores bearing both terminal and intercalary vesicles with few cylindrical, subulate phialides tapering gradually to a long neck region, and hyaline, thin-walled conidia (inset, C)—distinguished from the sphaerical darker aleurioconidia (B, left above inset); (D) Aleurioconidia emerging directly from hyphae; (E) Chlamydospores sensu lato formed in glistening white chains or ropes, densely guttulate. All scale bars are 10 μm. Augustin et al. (2013).

Details of conidiogenesis and spore morphology, as revealed by Critical-Point Drying SEM. (C) Escovopsioides nivea, chains of chlamydospores sensu lato revealing cryptic surface ornamentation or mucilaginous deposit (scale bar is 10 μm); (D–F) Escovopsioides nivea, (D) showing both terminal vesicle and phialides produced laterally on slight swelling (arrow) (scale bar is 10 μm). Augustin et al. (2013).

This study confirms the theory that parasitic weedy fungi in the gardens of Leafcutter Ants are more diverse than previously thought, but disproves the idea that the parasitic fungi are host specific, with each species of fungi apparently being able to infest the nests of any Ant.

The method of transmission of the parasitic Fungi has been a mystery for some time. When young Queen Ants leave their parent colony to start new colonies of their own they carry with them a supply of food fungus with which to start a new farm, but have never been found carrying the weedy fungi, suggesting that these are somehow transmitted from established colony to established colony rather than from parent colony to offspring colony. Augustin et al. suggest that this may be linked to the midden-building habit of the Ants; many related species of Ant build middens in underground chambers, which are then sealed off, isolating the waste. However Leafcutter Ants build midden heaps outside their nests, where waste, including material infected with weedy fungi, are placed. This enables the weedy fungi to produce spores outside the nest, with can then be more widely distributed, either by water or air, infecting workers of other Leafcutter Ant colonies or settling on leaves likely to be collected by such workers, and thereby reaching new Ant nests.

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