In some species, special squads leave the nest early each day, ascend the tree-trunks and then spend hours cutting out pieces of leaf that are dropped to other units on the ground.

The ants are celebrated for their diversity and success. Amongst the most remarkable evolutionary developments, however, is the independent emergence of agriculture, which has many striking similarities to that of humans (where indeed agriculture has developed independently a number of times). The agriculture developed by the attine ants involves the construction and maintenance of a fungal “farm”, and this too is convergent having developed independently also in the termites, certain beetles, and even snails.

To the first approximation human agriculture entails the cultivation of a monoculture, application of herbicides, use of manure and cropping. In addition, there is an associated cycle of transport of various commodities, which are essential for cultivation and ultimately a successful harvest. The arrangement in the attine ants (especially the leaf-cutters) is strikingly similar in practically all respects (and do not forget that whilst our agriculture is usually envisaged as fields of waving wheat, dense stands of corn or the limpidity of a rice paddy, cultivation of mushrooms and fungi is also very important).

Agriculture in leaf-cutter attine ants

Fungal agriculture has evolved at least twice amongst the ants, but the cultivation by the attines is by far the best known. It evidently had a single origin, about 50 million years ago, but since then there have been several events in the domestication of the fungi. In one case the fungus now cultivated is a yeast, and more dramatically another group has shifted to the so-called coral-mushrooms. In the more primitive attines the nests are generally rather small, with colony sizes of a few hundred (or less). However, a major innovation is represented by the leaf-cutter ants.

In contrast to the more primitive species that collect plant and other material, the leaf-cutters collect living vegetation, and this innovation along with more sophisticated controls against pathogens have allowed the development of enormous colonies, housing millions of individuals. In terms of consumption and metabolic output, such a colony is more or less equivalent to a large mammalian herbivore. These ants, like the termites, have a major ecological impact. 

As the name leaf-cutter ants suggests, the initial harvest is in the form of excised pieces of leaf that are then transported to the nest. This has its own complexities, including in some species special squads that leave the nest early each day, ascend the tree-trunks and then spend hours cutting out pieces of leaf that are dropped to other units on the ground.

So too transport to the nest may involve use of temporary caches, and in addition tiny ants (minims) may ride on the carried leaves to provide protection against attack, notably by parasitoid insects. Once in the nest the leaves are prepared as a mulch upon which the fungus is grown, and there is also evidence that this preparation may commence even before delivery. Of key importance are three factors. First, the crop must be manured and this is achieved by application of nitrogen-rich excreta produced by the ants. Second, the monoculture of fungi is in constant danger of pathogens, most notably a virulent fungal parasite known as Escovopsis.

To counter this, the ants apply antibiotics, which extraordinarily are secreted by bacterial filaments (actinomycetes) that live symbiotically on the bodies of the ants. This association is extremely intriguing because it may have an important bearing on the scourge of antibiotic resistance in human populations, as well as the prevalence of infections by parasitic fungi in immune-compromised patients, such as those suffering from AIDS. How have these ants, which adopted this type of agriculture millions of years ago, managed to ward off attack by pathogens? In addition to this defence system, like other ants these attines possess metapleural glands whose secretions also provide protection against pathogens. In addition to the application of manure and protection against pathogens, the ants also engage in weeding of the crop.

Finally, the fungus is cropped, and in particular sugar-rich tips (gongylidia) of the hyphae are harvested. The principal use of this food is to nourish the brood. Not surprisingly, in this environment with the constant war against invading pathogens, hygiene in the nest is of key importance. This includes not only the production of antibiotics and weeding of pathogens, but also removal of detritus and in some nests large dump-pits. In addition, in some species the workers “assigned” to these tasks are “quarantined” and do not mingle with other members of the colony. The dump-pits are only one manifestation of the complex structure of the nest, which not surprisingly needs adequate ventilation (including monitoring of carbon dioxide), and rather extraordinarily even wind-induced ventilation to ensure sufficient supplies of oxygen. Attine ants are extremely successful in the Neotropics, and from the human perspective they can be quite serious pests.

Although typically thought of in the context of forests farming, ants are ecologically widespread and extend into desert regions. The original association is evidently geologically ancient and may have a single origin. However, within the attine ants there is strong evidence that various types of fungi have been recruited, and this is clearly a polyphyletic phenomenon. Most typical are a group of basidiomycetes known as the lepiotaceans, but other fungi have been employed. Some ants in the genus Atta, for example, form an obligate symbiosis with the basidiomycete Attamyces, which is reminiscent of that between a termite family and the basidiomycete genus Termitomyces. In addition, there is evidence that just as in human agriculture there is extensive exchange of fungal cultivars between both colonies and also species of attine ants.

Not surprisingly the complex ecology of the ant fungal farm is not only attractive to the pathogenic fungus, but also species of marauding ants that act as so-called agro-predators. In addition, whilst most attention has been devoted to the most sophisticated attine ants, notably Atta and Acromyrmex, there are more primitive fungal-ant associations that help to shed light on how this association evolved.

Agriculture in non-attine ants

It is often claimed that fungal cultivation has only evolved once amongst the ants, specifically the attines. This is not correct. Excluding those ants that specifically harvest mushrooms, and intriguingly process the fragments in such a way that the collected food is preserved from rotting, employment of fungi has evolved at least twice independently of the attines.

(a) Whilst many ants have a symbiotic association with so-called ant-plants (myrmecophytes), in the case of an African example a fungus is involved as well in what appears to be a three-way symbiosis. The Fabacean plant Leonardoxa africana occurs in four (sub)species, three of which are true myrmecophytes with ants such as Aphomomyrmex afer and Petalomyrmex phylax as symbionts. The domatia, that is specialised nesting cavities, of these plants house patches of ascomycete fungi that are evidently deliberately planted and maintained by the mutualist ants. The ants show specific behaviours toward the fungus, “which are reminiscent of pruning activities known in fungus-farming ants” (Defossez et al. 2009, New Phytologist, vol. 182, pp. 942-949). Possibly the fungi provide food for the ants, and it seems more than likely that other such associations will be discovered.

(b) Many ants construct so-called cartons, which are nests composed of earth and/or vegetation. In the Old World Lasius group of ants (subgenera Dendrolasius and Chthonolasius) the carton has an associated ascomycete fungus that is evidently maintained and nurtured by the colony. Whilst the fungus appears to have a mainly structural function, forming a composite building material with shredded wood or soil, which allows for the construction of stable nests in tree or soil cavities, there is some evidence to suggest it might provide a source of nourishment.