PLB143 - Lecture 13

Non-Human Farmers: Ants, Termites, and Beetles

© L. Saxe and P. Gepts 2008
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Readings

Pre-agriculture: Animals that alter their environment to enhance the growth of plants of interest

    Pre-agricultural societies altered their environment to promote the growth of desired plants:

  • See also: Lecture 3: California Indian tribes fiber production of deergrass (Muhlenbergia rigens ) (Anderson, 1996)


African Bush Elephants (Laws, 1970)

  • African Bush Elephants –  95% of diet is grass
  • Needs large areas of grassland, but optimum diet no more than 50% grass – takes out Acacias so that they can maintain grass 
  • In forests elephants found to destroy trees so that there is favorable growth of Cynometra alexandrii – the elephant induced “climax species” for their diet

Characteristics of an Organism Able to do Agriculture
-    non-specialized diet (ants, elephants)
-    social organisms
-    close relationship with organism that is used for food



Animal Agriculture or Ranching (animal tending by other animals) – analogous to milk cows

Ants herding aphids – for honeydew (Buckley, 1987) ( Stadler and Dixon, 1998 )

ant_aphid

  • Ants collect honeydew from the aphids.
  • Just as humans cannot get at the cellulose in plants directly, but use cows to digest the cellulose, ants collect plant carbohydrates and the ants are able to utilize it.
  • Ant herding scale insects
    Ants Herding

  • Ant herding an aphid
    ant/aphid1
  • Ant collecting honeydew

    ant/honeydew




Ants tending to caterpillars (Lycaenids) – for secretions (Pierce, 1987) ( Pierce, 1986 )

ant_cat

  • 50% of Lycaenid species are associated with ants
  • Lycaenid caterpillars are taken into ant colonies and raised for their excretions
  • Larvae of Lycaenids have glands that excrete substance that communicate with ants – pore cupolas
  • The pore cupolas exist all over the surface of the larvae – this substance communicates to the ants that they should not attack the larvae
  • A dorsal organ secretes a sweet substance – the ants harvest this sweet substance
  • Some species of Lycaenids are parasites of the ants, rather than providing the sweet excretions benefiting the ants



  • Ant tending to a caterpillar

    ant_butter


Crop Agriculture  (Plant or fungus cultivation by animals)

Leaf-Cutter Ants - (Mueller et al., 1998)

  • Evolved one time 50,000 million years ago in the American tropics with attines ants domesticating fungi in the family Lepiotacea
  • The ants travel from the nest to trees and plants and collect leaves and flowers
  • They go back to the nest and chew up vegetation and serve the partially chewed plant and saliva to the fungi in the fungus garden
  • They develop their fungus garden on a bed of chewed vegetation
  • Fungus can break down cellulose and thus provides the ants access to the fungus
  • The ants prune back the hyphae to prevent the fungi from producing reproductive structures and to stimulate swollen hyphal tips called gangylidia


Parallels to Human Agriculture
  • The ants cultivate the fungus and move – queens establish the fungus in new their new colonies
  • The ants fertilize the fungus – leaving excrement as a source of nitrogen
  • The ants weed the fungus – remove the unwanted fungi through volatile signals, mechanical removal, and fungicides
  • Biocontrol - Antibiotic producing bacteria ( Streptomycetes ) grow on the cuticle of the ant, producing anti-bacterial substance specific to the weed fungus, Escovopis
  • Pruning - promotion of gangylidia
  • Specialized labor force – certain ants gather leaves, other process leaves, others harvest fungi 
  • New fungal species are sometimes used – parallel to selection and crop improvement


    A queen and her fungi
    A Queen and Her Fungus


  • Ants transporting leaf cuttings
    • ant parade
  • Ants transporting petal cuttings
    ant flower
  • Fungus garden
    ant_fung
  • Swollen hyphal tips or gangylidia

  • Streptomyces on ant
    Streptomycete Biocontrol


Termites (Matsura et al, 2000)

  • Fungi cultivating termites found in tropical Africa and Asia
  • The fungus they cultivate is Termitomyces
    Termitomyces is grown in special chambers degrading lignin components of solid excrement of the termite
  • The termites water their fungal gardens with termite excretions and thus maintain the necessary humidity for fungal growth
  • The termites building ventilation ducts into their mound so that the fungi are properly aerated
  • Pruning – to form nodules on the fungus that are consumed by the fungus
  • When it rains the termites take a bit of the mycellium outside of the mound.  Upon the development of a mushroom, the termites take a bit mushroom tissue and culture it in their new mound (note the mushroom is probably cross fertilized and thus the termites are maintaining a level of genetic diversity of their mushroom crop).

  • Termite mound in Darwin, Northern Territory, Australia





Ambrosia Beetles  (Batra, 1966)

  • Ambrosia beetles carry fungus with them in a specialized structure called a mycangium
  • They plant the fungus in their galley by inoculating wood with the fungus
  • The Ambrosia Beetle is dependent on their cultivated fungi for food
  • The fungus is only found in active galleys
  • Like leaf-cutter ants, they weed and prune the fungus


    Mycangial fungus growing on wood
    wood inoculation

  • Ambrosia beetles

    ambrosia beetle

  • Mycangium

    mycangium




Ambrosia beetles vs. Bark beetles
Ambrosia beetles
 Bark beetles
Use numerous taxa Specialize on few taxa
Associated fungi: Ambrosiella and Raffaelea are not pathogens
 Associated fungi: quickly infect host plants
Larvae eat gregariously in the fungus garden – allows generalist use of several different host species.
 Larvae eat in isolation in the phloem – results in specialization to single host species.

A comparison between Non-Human versus Human Agriculture
  • Cultivate soil:
    • Ants: add chewed leaves to fungus garden
    • Termites: water and aerate fungus garden
  • Produce crop
    • Ants, termites, and beetles all produces a fungal crop
  • Raise livestock
    • Ants raise aphids and Lycaenid caterpillar

Domestication of Fungal Species (Mueller et al 1998)

  • Fungal Propagation
    • Some active maintenance of genetic diversity in the fungal crop
    • Clonal propagation
      • Fungi: Evidence for four separate domestications 
      • The queen carries a pellet of fungus from her natal nest to her new garden 
      • Many cultivars propagated

How did agriculture start? (see Lecture 4 )

  • Sauer (1952): Six suppositions of the conditions under which agriculture started
  • Anderson (1954): Weeds as potential domesticates – ‘dump heap theory’
  • Boserup (1965): Agriculture as a response to high population density
  • Flannery: Broad Spectrum Revolution
  • Harlan (1992): No Model Model

Hearths of domestication are to be sought in areas of marked diversity of plants and animals (Sauer, 1952)

  • Ants have developed at least 553 cultivars of farmable fungi coming from 7 genera  
  • 12 genera of New World ants belonging to the tribe Attine farm fungus
  • The New World is a center for the diversity of these fungal species

Inventors of agriculture already had acquired special skills in other directions predisposing them to agricultural experiments (Sauer, 1952)

  • Fungus farming ants developed from seed storing ants.
                AND/OR
  • Fungus farming ants developed from a group of predaceous ants (Garling, 1979)

Founders of agriculture: sedentary, fishing tribes near fresh water (Sauer, 1952)

  • Societal structure...the fact that ants, termites, and ambrosia beetles are social animals is important to their development of agriculture 

Weeds as Potential Domesticates (Anderson, 1954)

  • Garling (1979) Review of Ant-Fungus Relationship Hypotheses:
    • Attine ants derived from a group of predacious ants living in logs
    • First fungus-eaters ate fungus growing on their feces instead of going out and hunting
    • Like weeds that prefer disturbed, nutrient-rich environments, these fungi grow with the ants in a nutrient-rich environment

Agriculture as a resul of an Increase in Population (Boserup, 1965)

  • Ants live at high density whether they farm fungus or not, thus it may not be a response to population

Broad Spectrum Revolution (Flannery)

  • Ants’ omnivory allowed them to shift diet to fungal species pre-adapted for living in disturbed environments


Conclusions

  • Humans were not the first species to develop agriculture.
  • Some species are “ecosystem engineers” and alter their environment to facilitate the growth of plants and fungus that are particularly beneficial to them (Bush Elephants)
  • Ants, termites, and beetles have all developed food production systems analogous to agriculture and, as in humans, this has allowed specialization and high population density.

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