Small farmers

Natural History, July-August, 2003

Jessie Gunnard, Andrew Wier, and Lynn Margulis ["Mycological Maestros," 5/03], having discovered that some populations of the termite Heterotermes tenuis consume spores of the fungus Delortia palmicola, suggest the termite might be a "missing link" to the higher termites that farm Termitomyces as their sole food source.

But the behavior of H. tenuis is not unique: many nonfarming termite species feed on fungus-infested wood. Because H. tenuis (of the family Rhinotermitidae) is not a direct ancestor of the Macrotermitinae, the "incipient farming" in H. tenuis is analogous, rather than homologous, to the elaborate fungus farming in the Macrotermitinae (a possibility the authors themselves raise).

Moreover, a "missing link" position for the South American H. tenuis is at odds with the supposedly African origin of fungus farming in termites. Likewise, for the fungi a true "missing link" would have to be a fungus that is sometimes farmed by termites and is also closely related to Termitomyces. This is not the case: D. palmicola (of the phylum Ascomycota) is as distantly related to Termitomyces (of the phylum Basidiomycota) as human beings are to protozoa.

Duur K. Aanen

University of Copenhagen

Copenhagen, Denmark

By colonizing wood, fungi "precondition" it, making it palatable to lower termites. No surprise, then, if fungal parts can be found in the guts of those termites. But the Macrotermitinae--the Old World subfamily of higher termites that engage in rather advanced fungus growing--feed predominantly on dry or freshly dead organic materials, which contain few fungi. The Termitomyces fungus farmed and ingested by those termites is therefore the first microorganism to attack the forage. Many species of Macrotermitinae degrade cellulose internally, with assistance from the fungus; in other species the fungus breaks down the plants' xylan and lignin.

The overall picture is one of an evolving diversity of mutualisms. Fungal nodules pass rapidly through the gut and germinate. Not enough are consumed to fully support the colony nutritionally; most termites feed on the fungus's more general fungal threads, which are richer in nitrogen than primary forage is. Thus the fungus is a composter, making energetically expensive nitrogen fixation unnecessary.

In spite of the complexity of the Macrotermitinae's mound constructions, the latest phylogenetic evidence places that subfamily in a basal position within higher termites, where the broadly dominant habit is the use of soil as a building material and/or as a food. We think the fungus found the termite and not vice versa.

David Bignell

University of London

London, England

Paul Eggleton

The Natural History Museum

London, England

After reading "Mycological Maestros," I finally know why the huge mushrooms I once (and only once) collected from a big termite mound in Zimbabwe are so rare: mushrooms appear only after the termite colony has abandoned the mound and stopped farming the fungus's mycelium. Those mushrooms, avidly sought by local residents, have a delicious, meatlike taste and texture strongly resembling that of the best commercial portobello mushrooms.

My own Zimbabwe research focused on the foraging habits of African elephants. I found strong ecological linkages between elephants and termites in woodland and savanna habitats in Africa: termites are the principal recyclers of elephant dung during the dry season.

Because both elephants and termites rely on microbial gut symbionts for digestion and nutrition, and because termites in Africa and Asia are intimately associated with elephant dung, it would be exceedingly interesting to determine whether any species of cellulose-digesting protists live not only in termites but also in the guts of elephants.

Joseph P. Dudley

The Pentagon

Washington, D.C.

LYNN MARGULIS REPLIES: Duur Aanen is correct. The behavior of the South American H. tenuis stimulates us to imagine the lives of the 200-million-year-old African ancestors of today's fungal gardeners.

David Bignell and Paul Eggleton assert that "the fungus found the termite and not vice versa." But whether the fungus found the termite or the termite discovered the fungus is scientifically indistinguishable. Wind-blown spores became delicious, fattening pinheads because of hungry insects. That's coevolution.

Joseph Dudley astutely suggests that elephants be examined for cellulose-digesting protists living in their guts. In fact, the search for cellulose-degrading microorganisms in elephants, as well as in beavers, pandas, and other mammals that feed on woody materials, promises rich rewards, particularly when the studies incorporate observations of the fossil record. With the electron microscope, my colleagues and I have observed, in 20-million-year-old Miocene amber, fragments of clearly identifiable plant xylem harboring protists and their adhering bacteria. We find termite muscle tissue, the cell nuclei and cell walls of wood, and even molecules of intestinal gas, such as methane and carbon dioxide. Similar success can be predicted with African elephant material.