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Mycophagy

Introduction


Open woodland vegetation.

Australia is characterised by a dry climate and mineral poor soil. Vegetation found in this environment appears well adapted to cope with the stressful conditions. Examination of macrocarpic fungi has led to the view that the fungi also have adaptations that enable exploitation of the harsh environment.

Sequestrate Form

Most macrocarpic fungi belong to the Basidiomycota. The common form of Agarics in the northern hemisphere is a gilled or poroid “mushroom”. The cap is held on a stalk above ground. The elevated structure (epigeous) enables the dispersal of spores in moving air. LINK This form is also widely found in Australia. However, many taxa closely related to the epigeous form have rounded fruiting bodies that are found within or below the litter layer (hypogeous). Most of the fungi have retained active discharge of spores, but lack the elevation enabling release of the spores to the moving air. Hypogeous fungi are found around the world, and occur in the Basidiomycota, Ascomycota, Glomeromycota and Endogonales. Hypogeous fungi are particularly common in Australia.

The rounded forms are referred to as sequestrate. Sequestrate fungi have probably evolved from closely related epigeous species. The selection pressure for evolution of hypogeous forms appears to be related to the overall dry climate: the longer periods of moist conditions within the litter experienced during fruiting enable completion of fruiting.


Black truffles.

Hypogeous fruiting reduces the opportunity to disperse spores in air. Another mechanism is needed if the fungi are to be carried beyond their immediate vicinity. Dispersal is widely achieved by means of animal vectors. The Black truffle, Tuber melanosporum, has a well characterised chemical attractant that resembles a pig pheromone. Thus the animal (pig) is attracted to the fruiting body, eats it and then defecates the spores at a distant location, effectively dispersing the fungus. LINK

The same pattern of attraction, consumption and dispersal is believed to occur among the Australian hypogeous fungi. Fresh animal digs are seen where the fungi are fruiting. The scats of a range of mycophagous animals contain significant proportions of spores of a variety of fungi. LINK The potential nutritive value of fungi indicates a potential nutritional role of fungi to the mycophagous animal. LINK

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Mycophagous Animals

bettong
Photo of a bettong.

A broad range of smaller animals consume significant quantities of fungus at some time during the year. The animals are mostly small mammals, ranging in size from marsupial mice to small wallabies. They can be grouped into three feeding behaviours. One group, including the Long-footed Potoroo, use significant quantities of fungus throughout the year. Fungi constitute some 90% of their diet. Another group consume significant quantities of fungi for much but not all of the year. The Long-nosed Potoroo and the Tasmanian Bettong are believed to require fungi for most, though not all of the year and they consume other foods. A third group consume large quantities of fungi for short periods, seasonal or maybe opportunistic in their use of fungi. Their diet at other times lacks much fungal material. The third group includes rats and bandicoots.

A large range of other animals appears to consume fungi, almost incidentally. These include some birds, macropods and possums. It is unclear whether the fungi are consumed deliberately, or consumed while eating other materials. In some instances, consumption of above ground fruiting bodies has led to the assumption that the animals are attracted to the potential food source: this mechanism may also apply to hypogeous sporocarps.

In Australian woodlands and forests, hypogeous fungi are widely distributed and macromycetes sporulate predictably. However, with the continued clearing of forest and woodland, the fungi are becoming rare. Continued loss of habitat will see the complete disappearance of these fungi. Animals that rely on fungi for sustenance will become extinct because of insufficient food. LINKOnly if restoration deliberately includes these fungi will conservation efforts succeed in maintaining animal and fungus communities.

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Taxonomy of Hypogeous Fungi

Interestingly, most of the hypogeous fungi appear to form mycorrhiza, especially ectomycorrhiza. LINK The fungi are commonly found in close association with roots of ectomycorrhizal tree species, including Acacia, Eucalyptus and Casuarina, especially in undisturbed plant communities. The mycorrhizal status of the fungi has been confirmed by inoculation studies in only a few cases.

The fungi are found in a wide range of taxa. In the Basidiomycota, hypogeous fungi are documented in members of the Agaricales, Boletales, Lycoperdales, Ramariales, Russulales, Sclerodermatales, and Stephanosporales totalling more than 500 species. In the Ascomycota, members of the Elaphomycetales and Pezizales total at least 25 species. In the lower fungi, members of the Endogonales total around 8 species and in the Glomeromycota, Glomales total at least 20 species. With this wide diversity of taxa, it is difficult to make many generalisations about nutritional benefit or functional attributes. It is unlikely that similar nutritional benefit would arise from consumption of a sporocarp of Glomus and Elaphomyces. Indeed, the Glomalean fungi form arbuscular mycorrhiza, and most of the remainder form ectomycorrhiza. The fungi differ and their nutritive value to animals is unlikely to be the same.

Many fungi require specific environmental triggers to initiate fruit bodies, commonly changes in temperature. Most of the fungi fruit during autumn and winter in the south eastern and south western parts of Australia, and summer in the tropical north. However, some species fruit during autumn and the sporocarps are present for the entire year, and a few form fruiting bodies throughout the year or at times other than autumn. For others fire is a trigger that initiates fruiting. Few mycophagous animals are found in any one area. Thus, providing animals can detect the presence of sporocarps, some food is likely to be available in the woodlands at all times of the year.

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Fire

Only during and following fire is food likely to be scarce. Fire removes the protective litter layer and scalds the surface of the soil, albeit unevenly. A few fungi respond to fire by fruiting abundantly, either immediately or during the next wet autumn. However, many species of ectomycorrhizal basidiomycetes are removed with the litter, and the taxonomic diversity of fruiting bodies is probably also reduced.

The effect of fire on mycophagous animals remains unclear. The size of the population is likely to be reduced directly by fire. The overall nutritional effect is likely to be related to which fungi are present at the site. Adequate food would be available if species that are protected from and/or respond to fire are abundant. The food supply would be seriously reduced if most fungi are killed by fire. Abundant food supplies would enable a rapid return of the population of mycophagous animals.

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Dispersal

The current view is that the fungi benefit from mycophagy through improved dispersal of spores. LINK The basis for the argument is that spores pass through the GIT and are then deposited on the ground a long way from the source. Dung beetles would bury the dung, taking fungal spores into the soil profile. Should roots be actively growing adjacent to the spores, germination of ectomycorrhizal fungi would be stimulated and ectomycorrhiza initiated. LINK

If seed were also present in the dung, then on germination of seed, roots would be in immediate contact with inoculum of mycorrhizal fungi. These speculations require that roots are actively growing in the presence of the buried dung, that germination is possible and that the symbionts are in close proximity. However, some experimental evidence indicates that spores in dung may have a very low infectivity. This may be due to high levels of specificity between species of plant and fungus. In addition, most animals do not travel beyond the woodland. Roots of woodland plants are likely to be heavily colonised by mycorrhizal fungi. Hyphae from germinating spores will be at a competitive disadvantage with the existing mycorrhizal fungi. When considered with all the information, it could be argued that successful initiation of a mycorrhiza from inoculum in dung is an infrequent event, and that spore dispersal is likely to be a significant factor benefiting the mycorrhizal fungi only with establishing seedlings immediately following severe fire.

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Conclusion

Mycophagy provides an interesting example of animal fungus interaction. While the interaction appears extremely important for some animals and some fungi, the mechanisms underlying the interaction are still unclear. Speculation has been directed towards a simple dispersal/nutritional role for the symbionts. Only further evidence will allow this matter to be resolved.

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References

Bougher NL & Lebel T (2001) Sequestrate fungi of Australia and New Zealand. Australian Systematic Botany 14, 1 – 47.

Claridge AW & Trappe JM (2005) In The Fungal Community (3rd edit) eds Dighton J, White JF and Oudemans P. Taylor & Francis.

Trappe JM & Claridge AW (2005) In The Fungal Community (3rd edit) eds Dighton J, White JF and Oudemans P. Taylor & Francis.

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