Fungus-growing ants

Attini
Atta mexicana workers carrying a leaf section
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hymenoptera
Family:	Formicidae
Subfamily:	Myrmicinae
Tribe:	Attini Smith, 1858
Type genus
Atta Fabricius, 1804
Genera
See text
Diversity
46 genera

Fungus-growing ants (subtribe Attina) comprise all the known fungus-growing ant species participating in ant-fungus mutualism. They are known for cutting grasses and leaves, carrying them to their colonies' nests, and growing fungi on them which they later feed on.

Their farming habits typically have large effects on their surrounding ecosystem. Many species farm large areas surrounding their colony and leave walking trails that compress the soil and no longer grow plants. Attine colonies commonly have millions of individuals, though some species only house a few hundred.

They are the sister group to the subtribe Dacetina. Leafcutter ants, including Atta and Acromyrmex, make up two of the genera. Their cultivars mostly come from the fungal tribe Leucocoprineae of family Agaricaceae.

Attine gut microbiota is often not diverse due to their primarily monotonous diets, leaving them at a higher risk than other beings at certain illnesses. They are especially at risk of death if their colony's fungus garden is affected by disease, as it is most often the only food source used for developing larvae. Many species of ants, including several Megalomyrmex, invade fungus-growing ant colonies and either steal from and destroy these fungus gardens, or they live in the nest and take food from the species.

Fungus-growing ants are only found in the Western Hemisphere. Some species stretch as far north as the pine barrens in New Jersey, USA (Trachymyrmex septentrionalis) and as far south as the cold-deserts in Argentina (several species of Acromyrmex). This New World ant clade is thought to have originated about 60 million years ago in the South American rainforest. This is disputed, though, as it appears that they likely evolved in a drier habitat while still learning to domesticate their crops.

Evolution

Early ancestors of Attine ants were probably insect predators. Eventually, they likely began foraging for leaf sections, but then converted their primary food source to the fungus these leaf cuts grew. Higher attines, like Acromyrmex and Atta evolved in Central and Northern America about 20 MYA, starting with Trachymyrmex cornetzi. While the fungal cultivars of the 'lower' attine ants can survive outside an ant colony, those of 'higher' attine ants are obligate mutualists. This obligate mutualism is thought to have evolved outside the rainforest, in areas where the fungi would not have been able to survive outside a colony anyway due to the dry environment.

Generalized fungus farming in ants appears to have evolved about 55-60 million years ago, but early 25 MYA ants seemed to have domesticated a single fungal lineage with gongylidia to feed colonies. This evolution of using gongylidia appears to have developed in the dry habitats of South America, away from the rainforests where fungus-farming evolved. About 10 million years later, leaf-cutting ants likely arose as active herbivores and began industrial-scaled farming. The fungus the ants grew, their cultivars, eventually became reproductively isolated, and co-evolved with the ants. These fungi gradually began decomposing more nutritious material - fresh plants.

Shortly after Attine ants began keeping their fungus gardens in dense aggregations, their farms began suffering from a specialized genus of Escovopsis mycopathogens. The ants evolved cuticular cultures of Actinobacteria that suppress Escovopsis and possibly other bacteria. These cuticular cultures are antibiotics and antifungals. The mature worker ants wear these cultures on their chest plates and sometimes on their surrounding thorax and legs as a biofilm.

Description

Different sizes of Atta insularis workers demonstrating the common polymorphism of higher attines

Lower attines have very minor polymorphism within the minor workers, though higher attines commonly have very different sizes of worker ants.

Queens have much larger ovaries than females in the working castes.

Workers

Between the different castes of workers, head width varies 8 fold and dry weight 200 fold. The size differences in workers is nearly nonexistent in newly-founded colonies.

Heads and mandibles

Due to the variety of tasks needed to be performed by a colony, the widths of workers heads are important and good measures of what jobs workers are likely to perform. Those with the heads, about .8–1 millimetre (0.031–0.039 in) wide tend to work as gardeners, although many with heads .8–1.6 millimetres (0.031–0.063 in) wide participate in brood care.

Workers need heads only about .8 millimetres (0.031 in) to do the work of caring for the very delicate hyphae of the fungus, which they care for by stroking with their antennae and moving with their mouths. These tiny workers are the smallest and most abundant and are called minim. 1.6 millimetres (0.063 in) appears to be the smallest workers that cut vegetation, but they cannot cut very hard or thick leaves. Most foragers have heads of about 2–2.2 millimetres (0.079–0.087 in) wide.

Attines, particularly the workers who cut leaves and grass, have large mandibles powered by strong muscles. On average, 50% of worker ants head mass and 25% of their full body mass is these mandibular muscles alone.

Behavior

Mating

A still-winged fungus-growing alate

Typically, there is one queen per colony. Every year after the colony is about three years old, the queen lays eggs of female and male alates, the reproductive ants who will pass on the genes of the queens. Before leaving the nest, queens stuff some of the fungus' mycelia in her Cibarium. These winged males and queens then take their nuptial flights to mate high in the air. In some areas, species flights are synchronized with all local colonies' virgin royalty flying at the same time on the same day, such as Atta sexdens and Atta texana.

Some species' queens mate with only one male, like species in Seriomyrmex and Trachymyrmex, while some are known to mate with as many as eight or ten, like Atta sexdens and many Acromyrmex. After mating, all males die, but their sperm stays alive and usable for a very long time in the spermatheca, or sperm bank, of their mate meaning that many ants technically father offspring years after their death.

Colony foundation

After their mating flights, queens cast off their wings and begin their descent into the ground. After creating a narrow entrance and digging 20–30 centimetres (7.9–11.8 in) straight down, she creates a small 6 centimetres (2.4 in) chamber. In here she spits on a small wad of fungus and starts her colony's garden. After about three days, fresh mycelia is growing out of the fungus wad and the queen has lain 3-6 eggs. In a month, the colony has eggs, larvae, and often pupae surrounding the ever-growing garden.

Until the first workers are grown, the queen is the sole worker. She grows the garden, fertilizing it with her fecal liquid, but does not eat from it. Instead, she gains energy from eating 90% of the eggs she lays, in addition to catabolizing her wing muscles and fat reserves.

Though the first larvae feed on the eggs of the queen, the first workers begin growing and eating from the garden. Workers feed malformed eggs to the hungry larvae while the garden is still fragile. After about a week of this underground growth, workers open the closed entrance and begin foraging, staying very close to the nest. The fungus begins growing at a much faster rate [13 micrometres (0.00051 in)] an hour. From this point on, the only work the queen does is egg-laying.

Colonies grow slowly for the first two years of existence, but then accelerate for the next three years. After winged males and queens begin being produced at around five years, the growth of the colony begins to level out.

The founding of a nest by these queens is highly difficult, and successful cases are not likely. After three months, newly founded colonies of Atta capiguara and Atta sexdens are 0.09% and 2.53% likely to still exist respectively. Some species have better odds, like Atta cephalotes which are 10% likely to survive a few months.

Caste system

Queens

An Atta Colombica queen surrounded by workers in a fungus garden

Since their needs are constantly taken care of, queens rarely move from a single location, which is typically in a centralized fungal garden. Workers take their eggs and move them to other fungal gardens.

Workers

Size

Differences in size between worker castes begin to develop after a colony is well established.

Though all castes defend their nests in the event of invasion, a true solider caste, with individuals called majors, exists. They use their large, sharp mandibles, powered by huge adductor muscles, to defend their colonies from large enemies, such as vertebrates. When a foraging area is threatened by conspecific or interspecific ant competitor, the majority of respondents are smaller workers from other castes since they are more numerous, and therefore better suited for territory combat.

Age

Tasks are divided not only by size, but by the age of individuals workers as well. Young workers of most sub-castes tend to work inside the nest, but many older workers take on tasks outside. Minims, who are too small to cut or carry leaf fragments, are commonly found at foraging sites. They often ride from the foraging site to the nest by climbing onto the fragments carried by other workers. Most likely, they are older workers who defend carriers from parasitic phorid flies that attempt to lay eggs on the backs of the foragers.

Smaller worker riding back to the nest on a leaf fragment carried by a forager

All size groups defend their colonies from invaders, but older workers have been found to attack and defend territories most often.

Habitat

Lower attines mostly live in inconspicuous nests with 100-100 individuals and relatively small fungus gardens in them. Higher attines, in contrast, live in colonies made of 5-10 million ants who live and work within hundreds of interconnected fungus chambers in huge subterranean nests. Some colonies are so large they can be seen from satellite photos, measuring up to 600 cubic metres (21,000 cu ft).

Farming

Workers carrying leaf fragments

The majority of fungi that is farmed by attine ants comes from the family Lepiotaceae, mostly from the genera Leucoagaricus and Leucocoprinus. Though, there is variance within the tribe. Some species in the genus Apterostigma have changed their food source to fungi in the family Tricholomatceae. Some species cultivate yeast, like Cyphomyrmex rimosus.

Some fungi that have supposedly been vertical transmitted are believed to be millions of years old, but it is unknown. It was previously assumed that the cultures are always transmitted vertically from colony to young queen, but some lower attines have been found to be growing recently-domesticated Lepiotaceae. Some species transfer cultures laterally, like Cyphomyrmex and occasionally some species of Acromyrmex, whether by joining a neighboring tribe, stealing or invading another colony's garden.

A leafcutter worker taking a leaf to its colony

Lower attines do not use leaves for the majority of the fertilizer for their gardens, and instead prefer dead vegetation, seeds fruits, insect feces, and corpses.

Recruitment

Early studies found the pheromones used to mark foraging trails comes from poison gland sacs. Studies suggest there are two purposes for marking the trails this way: worker recruitment and orientation cues. The trail recruitment pheromone in many Atta species, methyl-4-methylpyrrole-2-carboxylate (MMPC), was the first whose chemical structure was identified.

Harvesting vegetation

Most harvesting sites are in tree canopies or patches of savanna grass.

After following the pheromone trail to vegetation, ants climb onto leaves or grass and begin cutting off sections. To do this, they place one mandible, called the fixed mandible, onto a leaf and anchor it. Then they open the other, called the motile mandible, and place it on the leaf tissue. The ant keeps moves the motile jaw and pulls the fixed jaw behind it until the fragment detaches. Which jaw is fixed and which is motile varies depending on the direction the ant chooses to cut a fragment in.

An Atta Colombica worker using its mandibles to cut a leaf

The sizes of leaf fragments has been found in some studies to vary based on the size of ants due to the ants' anchoring of their hind legs while cutting, though other studies have not found correlations. This is likely because many factors affect how ants cut leaves, including neck flexibility, body axis location, and leg length.

Gardening process

First, foragers bring in to and drop leaf fragments on the nest's chamber floor. Workers that are usually slightly smaller clip these pieces into segments that are about 1–2 millimetres (0.039–0.079 in) across. Smaller ants then crush these fragments and mold them into damp pellets by adding fecal droplets and kneading them. They add the pellets into a larger pile of other prill.

Smaller workers then pluck loose strands of fungus from dense patches and plant them on the surface of the freshly made pile. Then the smallest workers, the minim, move around and upkeep the garden by delicately prodding the piles with their antennas, licking the surfaces, and plucking out the spores and hyphae of unwanted mold species.

Nutrition

Higher Attine fungi grows gongylidia which form clusters called staphylae. The staphylae are rich in carbohydrates and lipids. Though workers can also eat the hyphae of the fungi, which is richer in protein, they prefer staphylae and appear to live longer while eating.

Cellulose has been found to poorly degraded and assimilated by fungus, if at all, meaning that the ants who eat the fungus do not get much carbon from the cellulose in plants. It appears that xylan, starch, maltose, sucrose, laminarin, and glycoside play the important roles in ant nutrition. It is not known yet how ants can digest laminarin, but myrmecologists E.O. Wilson and Bert Hölldobler hypothesize that there may be fungal enzymes in the ants guts, as evidenced by the enzymes found in larval extract.

In a lab experiment, the needs of only 5% of workers' energy needs were met by fungal staphylae, and it appears that the ants also feed on tree sap as they collect greens. Larvae seem to grow on all or nearly all fungus, whereas queens get a lot of their energy from the eggs non-queen females lay and workers feed to them.

Bacterial symbionts

The actinomycete bacteria Pseudonocardia is acquired by pupae from the workers that care for them two days after pupae eclose for metamorphosis. Within 14 days, the ants are covered in the bacteria, where it is stored in crypts and cavities found in the exoskeletons. The bacteria produces small molecules that can prevent the growth of a specialized fungus garden pathogen.

Impact of farming

The scale of the farming done by fungus-farming ants can be compared to human's industrialized farming. A colony can "[defoliate] a mature eucalyptus tree overnight". The cutting of leaves to grow fungus to feed millions of ants per colony has a large ecological impact in the subtropical areas in which they reside.

Attine ants have very specialized diets, which seems to reduce their microbiotic diversity.

Leafcutters transporting yellow flowers

Genera

• Acanthognathus Mayr, 1887
• Acromyrmex Mayr, 1865
• Allomerus Mayr, 1878
• Apterostigma Mayr, 1865
• Atta Fabricius, 1804
• †Attaichnus Laza, 1982
• Basiceros Schulz, 1906
• Blepharidatta Wheeler, 1915
• Cephalotes Latreille, 1802
• Chimaeridris Wilson, 1989
• Colobostruma Wheeler, 1927
• Cyatta Sosa-Calvo et al., 2013
• Cyphomyrmex Mayr, 1862
• Daceton Perty, 1833
• Diaphoromyrma Fernández, Delabie & Nascimento, 2009
• Epopostruma Forel, 1895
• Eurhopalothrix Brown & Kempf, 1961
• Ishakidris Bolton, 1984
• Kalathomyrmex Klingenberg & Brandão, 2009
• Lachnomyrmex Wheeler, 1910
• Lenomyrmex Fernández & Palacio, 1999
• Mesostruma Brown, 1948
• Microdaceton Santschi, 1913
• Mycetagroicus Brandão & Mayhé-Nunes, 2001
• Mycetarotes Emery, 1913
• Mycetophylax Emery, 1913
• Mycetosoritis Wheeler, 1907
• Mycocepurus Forel, 1893
• Myrmicocrypta Smith, 1860
• Ochetomyrmex Mayr, 1878
• Octostruma Forel, 1912
• Orectognathus Smith, 1853
• Paramycetophylax Kusnezov, 1956
• Phalacromyrmex Kempf, 1960
• Pheidole Westwood, 1839
• Pilotrochus Brown, 1978
• Procryptocerus Emery, 1887
• Protalaridris Brown, 1980
• Pseudoatta Gallardo, 1916
• Rhopalothrix Mayr, 1870
• Sericomyrmex Mayr, 1865
• Strumigenys Smith, 1860
• Talaridris Weber, 1941
• Trachymyrmex Forel, 1893
• Tranopelta Mayr, 1866
• Wasmannia Forel, 1893

See also

• Ant–fungus mutualism
• List of leafcutter ants

External links

• Media related to Attini at Wikimedia Commons