Excerpt from "Trees & Toadstools" by M C Rayner 1)

The Honey Agaric (Armillaria mellea), is exceptional and shows peculiarities in its mode of life that challenge attention.

A deadly and widely distributed parasite of trees and sometimes of other plants, the Honey Agaric forms its sporophores only after the tissues in which it grows have been killed. The tawny, white-gilled toadstools are common on dead stumps in woodlands and hedgerows, thus betraying the presence of the vegetative mycelium of the parent fungus, at this stage growing as a saprophyte in the dead tissues of the tree and forming root-like strands, that extend into the tissues of the stump and far afield into the soil. These strands or rhizomorphs, looking like dark brown thongs or bootlaces, can grow in soil as well as in living or dead plant tissues, thus serving as a very efficient means of extending the attacks of the parasite to new hosts, spreading from tree to tree through the soil with deadly efficiency. On occasion, the rhizomorphs have been observed to extend into cultivated ground adjoining woodlands, invading potato fields with disastrous consequences to the growing crop. In its mode of life the Honey Agaric is thus not a typical soil fungus. It can be and often is an insidious and dangerous parasite attacking and killing trees and on occasion other kinds of plants; it may grow also as a saprophyte on the dead stumps of its victims, and by means of the rhizomorphs travel long distances through the soil, living upon the organic residues in the humus and thus behaving temporarily like a true soil fungus (Pl. 6, 7, 8, 9).

This remarkable plant has a very wide geographical distribution. In Japan and elsewhere, it is known to form a surprising kind of association with certain orchids of peculiar habit, an association in which the orchid seems to have secured the best of the bargain in respect to food supplies. The first of these associations to be described in detail was that with a curious species of orchid called Gastrodia elata, native in Japan.
The Gastrodia plant when fully developed consists merely of an underground tuber like a large elongated potato or artichoke tapering to one end and covered with brownish cork. The tuber is rootless and without green leaves or shoots; like those of other tubers, the tissues contain reserve food materials, at the expense of which it produces periodically an immense flowering shoot, a yard or more in length, bearing small brownish scale leaves and brownish flowers of the characteristic orchid type (Pl. 9).

It was observed by botanists that the production of flowering shoots by this orchid was very erratic, representing only a small proportion of the mature tubers present in the soil of any given locality. After a time, a Japanese botanist named Kusano made the interesting discovery that the tubers were frequently attacked by rhizomorphs of Armillaria mellea continuous with those infesting cultivated soils or woodlands nearby, and that these rhizomorphs penetrated the tubers by means of sucker-like outgrowths. There followed further researches and experiments leading to the surprising discovery that only tubers parasitized in this way produced flowering shoots, whence it appeared that the mature Gastrodia tuber, cut off from direct contact with the outside world by its corky covering and the absence of roots, re-establishes such contact by suffering parasitic invasion of its tissues. Only thus apparently can it utilize its store of reserve materials to produce flowers and fruit and so complete the life cycle. The details of this curious liaison in the plant world are still obscure. That the fungus gains entry by virtue of its equipment as a parasite seems certain; to what extent it robs the invaded tuber of stored reserve food materials and what it brings in return that enables the latter to utilize those reserves in producing a massive inflorescence giving rise eventually to fruit and seed is still uncertain. It is quite clear, however, that active parasitism of the orchid tuber by the rhizomorphs, if it occurs, is of a very different kind from the ruthless assaults made by the Honey Agaric fungus on potato tubers or living trees. This is in itself a very interesting fact showing how difficult it is to make absolute statements about the food habits of fungi. The relationship of the mycelium with the tissues of the tuber is particularly difficult to explain satisfactorily. There is plenty of suitable food material stored within the tissues and all the mechanism for lethal attack is apparently present in the rhizomorphs. Yet the attack halts at the initial stages, the most obvious result being stimulation of the victim to form new organs and so utilize its own reserves of food!

The Honey Agaric is known to form similar partnerships with another species of Gastrodia and with several East Indian species of orchid having the same curious habit: absence of green leaves or chlorophyll, underground tubers, and the production at intervals of gigantic inflorescences of brownish flowers.

It is known also that another soil fungus, a species of Marasmius, belonging to the same family group as the Honey Agaric, forms a similar kind of relationship with another tropical species of orchid.

All these strange associations are of crucial interest to our present inquiry; first, because they indicate the very wide geographical distribution of a soil fungus such as the Honey Agaric; secondly, and more important, because they indicate what may be called the flexibility of this fungus in respect to its food habits; it can be and usually is an out-and-out parasite on trees or other plants, it can live as a saprophyte in situ upon the dead remains of its victims, or on these and other organic remains in the soil as they pass into the condition of humus. Thirdly, because the orchids involved in these queer relationships are all plants without green leaves or chlorophyll and therefore committed to a mode of life similar to that of their fungus associate. Unable, like green plants, to utilize the inexhaustible supply of carbon present in the air as carbon-dioxide gas, they must seek their essential supplies of this element in organic form as do their fungus competitors. They are indeed, from this point of view, not worth parasitizing!

In what manner the young Gastrodia tuber obtains from the soil the carbon necessary to allow it to reach maturity and convert its tissues into a storehouse of reserve food materials is quite unknown. The impermeable covering of cork acquired subsequently by the mature tuber certainly brings any such absorption to an end, severing completely any direct relations with the soil around it.