Fungal Cultivation by Insects

Abstract

Fungi and insects are two hyperdiverse groups of organisms that have interacted for millennia. Over time, some insects have come to rely on fungi for a variety of resources, including room and board. Ants, wasps, beetles and a variety of other insects have adapted to using fungi primarily for reinforcing structures or as sources of food, with the most extreme examples resulting in cultivation of fungal crops. Chief among these examples are the mushroom‐farming ants and termites, and the wood‐boring beetles and wasps. These systems offer compelling insights into a miniature world that parallels our own human agricultural systems, providing new perspectives on sustainable practices that have endured millions of years of parasites, pests and environmental change. Yet our basic documentation of the natural history of fungal cultivation by insects is still very incomplete, with new discoveries regularly appearing that expand our knowledge of the true diversity of these interactions.

Key Concepts

  • Fungiculture evolved independently at least six times in three orders of insects.
  • Fungus‐farming ants, termites, beetles and wasps are prime examples of obligate fungiculture.
  • Insects cultivate fungi for food or structure.
  • Diverse lineages of fungi belonging to Ascomycota and Basidiomycota are cultivated.
  • Fungal crops are typically transmitted vertically, but may or may not engage in reproduction outside of gardens.
  • Fungi are capable of transforming plant materials into consumable forms for the insects, expanding ecological opportunities for both partners.
  • Insect fungicultural systems have been stable symbioses for millions of years, yet fungal gardens are complex communities of interacting microorganisms.

Keywords: symbiosis; coevolution; fungiculture; attine ant; leafcutter; ambrosia beetle; fungus‐growing termite; wood wasps; siricid

Figure 1. Cophylogenetic comparison of insect orders (left) and fungal phyla (right). Black and grey lines connect insect and fungal taxa involved in primary and secondary fungiculture, respectively. Orders of fungi are indicated with black or grey triangles to indicate approximate phylogenetic position within the phyla. Insect tree is based on Chesters , and the fungal tree is based on Spatafora et al. .
Figure 2. Free‐living relatives of attine crop fungi, fungus‐farming ants and their gardens. (a) Leucocoprinus birnbaumii, Tijuca National Park, Rio de Janeiro, Brazil. (b) Pterula verticillata, Gunung Mulu National Park, Sarawak, Malaysia. (c) Nest of Apterostigma dentigerum on the underside of an understory palm, Osa Biodiversity Center, Costa Rica. (d) Close‐up of the nest in (c). (e) Apterostigma ants tending their fungal crop, Osa Biodiversity Center, Costa Rica. (f) Leaf‐cutter ants (Atta) excising fresh leaf material from cultivated bananas, Osa peninsula, Costa Rica. (g) Acromyrmex ants tending their fungal crop in an underground chamber, Tijuca National Park, Rio de Janeiro, Brazil. Photos: Bryn Dentinger.
Figure 3. Fungus‐farming termites and their mushroom crops in a lowland tropical forest in Cameroon. (a) Large soil mound formed by a Macrotermes termite colony with Termitomyces sp. mushrooms emerging at the top. (b) Excavated mound showing the elongated stipes of the Termitomyces sp. mushrooms that originate as a tangle of tough mycelial cords surrounding the garden comb deep within. (c) Mature mushrooms of Termitomyces sp. harvested for food by local inhabitants (ruler in photo = 10 cm). The mushrooms depicted are preserved as specimens stored in the fungarium at the Natural History Museum of Utah (Accession #UT‐M0000061). (d) Dorsal view of a Macrotermes sp. soldier (scale bar = 1 mm). (e) Head of a Macrotermes sp. soldier (scale bar = 1 mm). Photos (a–c): Bryn Dentinger. Photos (d) and (e): Courtesy of Breanne Van Den Broeke.
Figure 4. Side view of Dendroctonus simplex (specimen UMNH.ent.0060200). Courtesy of Breanne Van Den Broeke.
Figure 5. The woodwasp Tremex columba (a; specimen UMNH.ent.0032206) and mushrooms produced by its fungal symbiont Cerrena unicolor (b). Photo of wasp: Courtesy of Breanne Van Den Broeke. Photo of fungus: Courtesy of Joseph O'Brien, USDA Forest Service, Bugwood.org.
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Further Reading

Hölldobler B and Wilson EO (2011) The Leafcutter Ants: Civilization by Instinct. New York: W.W. Norton & Company, Inc.

Mueller UG and Gerardo NM (2002) Fungus‐farming insects: multiple origins and diverse evolutionary histories. Proceedings of the National Academy of Sciences 99: 15247–15249.

Mueller UG, Gerardo NM, Aanen DK, et al. (2005) The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics 36: 563–595.

Vega FE and Blackwell M (eds) (2005) Insect–Fungal Associations: Ecology and Evolution. Oxford, UK: Oxford University Press.

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Dentinger, Bryn TM, and Bills, Christy(Aug 2018) Fungal Cultivation by Insects. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027211]