15.3 Termite gardeners of Africa
Leaf cutting ants cultivate their fungus in the Americas, but in the Old World, Africa and Asia, the insect partner which engages in a similar fungus-gardening relationship is a termite. Termites are responsible for the bulk of the wood degradation in the tropics. Indeed, insects accelerate deadwood decomposition in tropical forests and globally, insects may account for 29% of the carbon flux to the atmosphere from deadwood (a total of 10.9 billion metric tons per year), indicating a major role in the Earth’s carbon cycle (Seibold et al., 2021). Most of them carry populations of microbes in their guts to digest the plant material and release its nutrients, but termites in the insect subfamily Macrotermitinae have evolved a different strategy. They eat the plant material to get what nutrition they can from it, and then use their faeces as a compost on which they cultivate a fungus. The fungus belongs to the mushroom genus Termitomyces (Basidiomycota: family Lyophyllaceae) including Termitomyces titanicus of West Africa, which produces some of the largest mushrooms you can find, being up to about a metre across the cap. In the termite nest, fungal enzymes digest the more resistant woody plant materials and the fungus becomes a food for the termites.
Termitomyces typically forms mushrooms a few weeks after the termite colony has produced dispersing alates. It is thought that because workers consume the fungus, when the numbers of workers are reduced (because alate production reduces resources available for worker production) the fungus is released from the constant grazing and is able to form mushrooms that emerge from the host colony (Vreeburg et al., 2020).
Termites maintain their fungal cultivar on special structures in the nest, called fungus combs, within specially constructed chambers, either inside a nest mound or dispersed in the soil. Workers feeding on dry plant material produce faecal pellets (primary faeces) which are added continuously to the top of the comb, providing fresh substrata into which the fungal mycelium rapidly grows. In a few weeks, the fungus produces vegetative ‘nodule’ structures, which are aborted mushroom primordia. These are cropped and consumed by the termite workers who later consume the entire fungus comb, both mycelium and spent compost.
Nests of fungus-growing termites can have volumes of thousands of litres, may persist for decades, and contain millions of sterile workers, which are normally the offspring of a single queen. Different termites produce mounds of different size and shape. Chimney-like termite mounds up to 9 m tall (thirty feet) are common in several parts of the bush in Africa. Inside, the mounds have many chambers and air shafts that ventilate both nest and fungus culture; perhaps the most complex colony and mound structures of any invertebrate group. Thus: ‘…termite mounds are metre-sized structures built by millimetre-sized insects. These structures provide climate-controlled microhabitats that buffer the organisms from strong environmental fluctuations and allow them to exchange energy, information, and matter with the outside world...’ (King et al., 2015).
As we stated above, phylogenomics identifies independent origins of insect agriculture in the three clades of fungus-farming insects: the termites, ants or ambrosia beetles and dates all of them to the Paleogene Period in the Cenozoic Era (24 to 66 million years ago). Fossil fungus gardens, preserved within 25-million-year-old termite nests, have been found in the Rukwa Rift Basin of southwestern Tanzania, and confirm an African Paleogene origin for the termite-fungus symbiosis; perhaps coinciding with Rift initiation and consequential changes in the African landscape (Roberts et al., 2016).
All termite larval stages and most adults eat the fungus. The termite queen, ‘king’ and soldiers are exceptions, being fed on salivary secretions by the workers (Aanen et al., 2002, 2007). The two main symbioses of social insects with fungi, the agricultural symbioses of ants and termites are similar in many respects, but they differ in others. Mutualism with fungi has allowed both ants and termites to occupy otherwise inaccessible habitats that have abundant resources: the attine ants are dominant herbivores of the New World tropics; fungus growing termites are major decomposers of the Old-World tropics. However, the fungal cultivars of attine ants rarely fruit and are normally propagated clonally and vertically by being carried by dispersing queens (see above), whereas fungal symbionts of the Macrotermitinae often produce fruiting bodies. In the rainy season the termites may take portions of the culture out of the nest mound to fruit on the ground nearby and abandoned nest mounds also produce mushrooms after the termites have left.
These wild fruit bodies are inferred to be the source of fungal inoculum for new nests; that is, it is assumed that the fungal cultivar is generally a ‘horizontal acquisition’ because the termite fungal cultivars have a freely-recombining genetic population structure rather than being clonally-related. This implies that new termite colonies will usually start up without a fungus and then acquire the fungal symbiont through the occurrence of its basidiospores (produced by mushrooms growing from other nests) on the plant litter that the workers collect (Aanen et al., 2002). There are, however, two examples in which the fungal cultivar is transmitted clonally between nest generations. In the termite species Macrotermes bellicosus (via the male termite sexuals) and all species in the genus Microtermes (via the female sexuals) the reproductives of one or the other sex ingest asexual spores of the fungus before the nuptial flight and use these as inoculum for the new fungus comb after foundation of their new nest colony (Aanen et al., 2007).
Symbiotic relationships with a wide range of intestinal microorganisms, including protists, methanogenic archaea and bacteria, have played a major role in termite evolution. Plant biomass conversion is a multistage cooperation between Termitomyces and gut bacteria, with termite farmers mainly providing the gut compartments in which this fermentation can occur. Termitomyces has ability to digest lignocellulose and gut microbes of worker termites primarily contribute enzymes for final digestion of oligosaccharides. Termite gut microbes are most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and lignocellulose decomposition can proceed with high efficiency. All termites rely on gut symbionts to decompose organic matter but the single subfamily Macrotermitinae evolved a mutualistic ectosymbiosis with Termitomyces fungi to digest lignocellulose of woody substrates (Varma et al., 1994; Bignell, 2000; Poulsen et al., 2014).
The Macrotermitinae comprises 11 genera and 330 species; 10 of the 11 genera are found in Africa, 5 genera occur in Asia (one of these exclusively) and 2 genera occur in Madagascar. Approximately 40 species of the Termitomyces symbiont have been described. Molecular phylogenetic analyses of termites and their associated fungi show that the symbiosis had a single origin in Africa. These data are also consistent with horizontal transmission of fungal symbionts in both the ancestral state of the mutualism and most of the extant taxa. Clonal vertical transmission of fungi in Microtermes and Macrotermes bellicosus (mentioned above) had two independent origins. Despite these features there was a significant congruence between the termite and fungal phylogenies, probably because mutualistic interactions show high specificity; meaning that different genera of termites tend to rear different clades of Termitomyces (Aanen et al., 2002, 2007).
Fungus-growing termites are pests because they attack wooden structures; by eating through the wood they leave a maze of galleries that destroy the strength of the timber. Of the more than 2300 species of termite in the world, 183 species are known to damage buildings. Termite damage and control costs are estimated at US$5 billion annually in the United States alone (Varma et al., 1994; Su & Scheffrahn, 1998; and see https://www.americanpest.net/blog/post/the-real-facts-about-termite-damage).
Insecticides and fungicides can help to control this pest. The chitin synthesis inhibitor, hexaflumuron (1-[3,5-dichloro-4-(1,1,2,2-tetrafluoroethoxy) phenyl]-3-(2,6-difluorobenzoyl) urea), has proved particularly effective as a slow-acting bait. Termite colonies can be eliminated using less than 1 g of hexaflumuron, which is described in pesticide listings as a systemic (stomach-acting) insecticide, but it will also target chitin synthesis in the fungus and poison the nest that way as well (Su & Scheffrahn, 1998). Hexaflumuron is registered with the United States Environmental Protection Agency as a reduced-risk pesticide (one believed to pose less risk to human health and the environment than existing alternatives).
Updated September, 2021
