Farmer Ant and his Fungi

© Else Vellinga
Lab
Original publication: Mycena News, October 2010

A mere 10,000 years ago, Homo sapiens started planting and tending crops. This was at that time a stellar innovation, and a huge change from the gatherers’ way of life. It enabled the formation of permanent settlements, which ultimately developed into cities, and a division of labor was established. However, humans were preceded in these cultural developments by ants and termites.

Atta colombica

Attine ants occur in the (sub)tropical regions of America, and as far north as New Jersey on the east coast of North America. They cultivate fungi in the Leucoagaricus/Leucocoprinus clade of the mushroom family Agaricaceae. Pictured above: Atta colombica; photo courtesy of Wikimedia commons.

One group of ants, the new world ants in the tribe Attinae (attine ants for short), started farming at least 50 million years ago (that is, long before humans were around). The ants cultivate fungi for food in their nests, groom, manure, and weed their patches, and ultimately harvest the fungi. They also bring material to the nest to serve as substrate for their fungi. The plant material as such is unpalatable for the ants, and they depend on the fungi to turn it into something they are able to digest. The so-called lower attine fungi live in very small colonies, and bring mainly humus and plant debris to the nests; they cultivate a variety of parasol mushroom species (in the genera Leucoagaricus and Leucocoprinus in the family Agaricaceae). Other ants, in the pilosum-group of the genus Apterostigma, cultivate coral fungi of the genus Pterula, using dead branches and twigs as a substrate. The higher attine ants comprise two genera of leaf-cutting ants (Atta and Acromyrmex), which cut pieces of leaves from living plants and bring them to their nests, thereby causing considerable damage to human crop plants. These nests are huge underground caverns that can be as big as a mansion, and contain millions of ants in a strictly and highly organized society. They cultivate only one mushroom species, Leucoagaricus gongylophorus. The other two genera in the group of the higher attine ants, Trachymyrmex and Sericomyrmex, are also highly organized. Instead of cut leaves, they bring freshly shed flowers, insect frass and soft leaf fragments to the nests. Their fungal crop consists of a group of different Leucoagaricus species.

In short, there is a variety of substrates for the fungi to grow on in a range of ant settings. The question is, of course, how do the fungi handle this? Do they all have the same enzymes to break down the plant material, or does the species cultivated by the leaf-cutting ants have enzymes specifically tailored to the fresh leaves, and are these enzymes missing in the cultivars of the ants that bring dead plant material to the nest?

The main findings of enzyme assays conducted in the field, are that the leaf cutters’ cultivars are good at breaking down amylose, the higher ants (leaf cutters and flowerringing ants) have a lot of endoprotease that breaks down casein, and the fungi grown by the lower attine ants are much better at breaking down xylan while all are about equally good at breaking down cellulose (though there are differences among the cultivars). What we had expected was, of course, that the fungi of the leaf cutting ants would be good at breaking down the plant cell walls, and have cellulases in abundance. However, the ants themselves are very active in this task and this may explain why there is no need for the fungus to have its own enzymes that chemically break down the plant cell walls; the big worker ants cut the leaves and bring them to the nest, where an army of smaller and smaller ants chew the leaves into progressively smaller and smaller pieces,. The lower attine ants, on the other hand, do not have such organized labor forces, and for them the fungi themselves have to break down the (dead) plant material. The cultivated Pterula species differ considerably from the Leucoagaricus taxa, especially in the absence of a pectinolytic enzyme, and the low activity of the xylanases. Of course, only a small set of enzymes have been tested, and it may be possible that the fungi have different enzymes that do more or less the same job as those tested.

Leucoagaricus

This beautiful system of agriculture is open to influences from outside – some bad, some good to stem the bad. Every plant is host to many fungi – harmful pathogens, accidental commensals, and a host of fungi that just hang out inside the plant tissues, awaiting their turn. These endophytes do not do any harm to the plant, and may in fact play a role in defense mechanisms against pathogens, stress, and environmental damage. Yet inside the ants’ nest they could be competitors to the fungi already there, or a downright threat to their existence.

In some tightly controlled experiments, in which plants were either kept free of endophytes or inoculated with a fixed amount of fungi, Atta colombica ants were given a choice between these differently treated plants. It turned out that the ants spent more time cutting leaves from plants with endophytes than from endophyte-free plants. They also reduced the number of fungi during their manipulations of the leaves and the cultivar fungi themselves can fence off accidental newcomers. These ants can also discriminate between seedlings with a high load of endophytes (high both in numbers of taxa and in numbers of individuals) and plants with very few commensal fungi. The ants do more damage (by cutting more leaves) to plants with only a few endophytes, than to plants with a lot of fungi. This observation might be helpful in reducing the damage leaf cutting ants can do to human crops and cultivated plants. These results show once again how sophisticated this agricultural system of attine ants and their fungi is. Human farmers can still learn from the ants and the fungi!

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