Mutualistic interactions between ants and fungi: A review

Abstract

The large amount of dead plant biomass caused by the final extinction events triggered a fungi proliferation that mostly differentiated into saprophytes degrading organic matter; others became parasites, predators, likely commensals, and mutualists. Among the last, many have relationships with ants, the most emblematic seen in the Neotropical myrmicine Attina that cultivate Basidiomycota for food. Among them, leaf-cutting, fungus-growing species illustrate an ecological innovation because they grow fungal gardens from fresh plant material rather than arthropod frass and plant debris. Myrmecophytes shelter "plant-ants" in hollow structures, the domatia, whose inner walls are lined with thin-walled Ascomycota hyphae that, in certain cases, are eaten by the ants, showing a form of convergence. Typically, these Ascomycota have antibacterial properties illustrating cases of farming for protection. Ant gardens, or mutualistic associations between certain ant species and epiphytes, shelter endophytic fungi that promote the growth of the epiphytes. Because the cell walls of certain Ascomycota hyphae remain sturdy after the death of the mycelium, they form resistant fibers used by ants to reinforce their constructions (e.g., galleries, shelters for tended hemipterans, and carton nests). Thus, we saw cases of "true" fungal agriculture involving planting, cultivating, and harvesting Basidiomycota for food with Attina. A convergence with "plant-ants" feeding on Ascomycota whose antibacterial activity is generally exploited (i.e., farming for protection). The growth of epiphytes was promoted by endophytic fungi in ant gardens. Finally, farming for structural materials occurred with, in one case, a leaf-cutting, fungus-growing ant using Ascomycota fibers to reinforce its nests.

Keywords: ant constructions; ant fungiculture; composite materials; defoliation; fungi as food.

FIGURE 1

(a) Acromyrmex sp. worker positions its hind legs on the leaf edge and rotates around them while cutting an arc in a leaf blade, whereas it uses its mandibles asymmetrically, one leading the process, the other cutting a large piece of leaf. (b) By comparison, a Crematogaster clariventris worker cuts small pieces with a typical chewing motion of its mandibles moving symmetrically (photos Piotr Naskrecki).

FIGURE 2

Myrmecophytes shelter certain ant species in hollow structures where the ants grow Ascomycota fungi likely for their antibacterial role. (a–c) Maieta guianensis (Melastomataceae) bears pairs of leaf pouches sheltering Pheidole minutula ants that nest in one pouch, while they deposit wastes in the other where fungi develop. (d) Tachia guianensis (Gentianaceae), here in bloom, can shelter in its hollow twigs several ant species that raise their brood close to or on their fungi‐rich deposits. (e) Azteca sp. (f) Pseudomyrmex tenuis. (g) Crematogaster brasiliensis. (f) (Alain Dejean, personal observation). Nutrient provisioning to the plant, or myrmecotrophy, was shown for both the Maieta and Tachia (Dejean et al., ; Solano & Dejean, ; photos Alain Dejean).

FIGURE 3

Two examples of ant gardens. (a) Camponotus femoratus build large ant gardens generally in the canopy of Neotropical forests; here, we see the ant carton and epiphytes including Philodendron and Anthurium (Araceae) and tank bromeliads Aechmea mertensii. (b) Another Camponotus femoratus ant garden with Anthurium bearing fruits, the carton nest is clearly visible (photos Alain Dejean). (c) Foundation of Neoponera goeldii showing the rough carton nest made by several queens and their first workers; the epiphytes have begun to grow on this nitrogen‐rich carton. (d) A Neoponera goeldii ant garden with an Aechmea mertensii (Bromeliaceae) in bloom; the carton made by the ants is clearly visible (photos Bruno Corbara).

FIGURE 4

Gallery‐shaped traps built by Allomerus decemarticulatus on the myrmecophyte Hirtella physophora. The workers use intact host plant trichomes to form pillars onto which they build the vault of the galleries using cut trichomes reinforced by the hyphae of Chaetothyriales to form a composite material pierced by numerous holes. (a) The workers that ambush prey by placing themselves under the holes have captured a red reduviid bug and a grasshopper, whereas an Agelaia cajennensis wasp is robbing pieces of that prey (cleptobiosis). (b) Later, the Agelaia cajennensis was captured in turn, but an Agelaia pallipes successfully robbed several pieces of the grasshopper. (c) Small social wasps were easily captured. (d) Capture of a tabanid deer fly (photos Alain Dejean).

FIGURE 5

Brittle carton nest of dolichoderine ants reinforced by fungal mycelia of the Chaetothyriales. (a) Very large nest of the Azteca sp. chartifex group (b) The extremity of a similar nest with social wasps nesting side‐by‐side to be protected by the ants. (c) Azteca andreae build nests on the myrmecophyte Cecropia obtusa. (d) An Azteca chartifex nest. (e) Azteca andreae workers ambush side‐by‐side under Cecropia obtusa leaves permitting the capture of a large sphingid moth thanks to their hook‐like claws that catch on the fibrous loops on the undersides of the leaves recreating the Velcro® effect. (f) Nest of Dolichoderus bidens under a leaf (photos Alain Dejean).

FIGURE 6

Brittle carton nest of Crematogaster ants also reinforced by Chaetothyriales fungi. (a) Crematogaster stadelmanni nest with large protrusions that likely permits heavy rain to run off (see Moumite et al., 2022). (b) Carton nest of Crematogaster sp. showing its external structure. (c) Nest of Tetramorium aculeatum made of carton between the leaves of the supporting tree (photos Alain Dejean).

FIGURE 7

(a) Hard carton nest of Crematogaster clariventris reinforced by fungal mycelia of the Capnodiales. (b) Details of the hard carton inside the nest (photos Alain Dejean). (c, d) Workers cutting pieces of a young, nitrogen‐rich leaf (photos Piotr Naskrecki).