Of Mammals and Mutualists
When asked to discuss some of the important ecological roles of fungi, many of us with some biological background might think of the mutualistic relationships between plants and fungi that characterize various kinds of mycorrhizae, or perhaps the complex symbiosis between the algae and fungi that make up a lichen. We might also think of fungi, particularly hypogeous fungi, as an important food item for many kinds of mammals; however, this only just scratches the surface of what is often a much more complex and fascinating relationship.
If some mammalian/fungal relationships go beyond just a simple "predatorprey" model, we must look at whether this relationship is obligate for one or both partners, as well as examining what the fungi get out of this relationship.
It's clear that fungi are a dominant food item for many species of small mammals, particularly among squirrels, mice, and voles, and, in Australia, among several groups of small marsupials, such as bettongs, potoroos, and rat-kangaroos. Some of the more notable fungivorous mammals include the California red-backed vole (Clethrionomys californicus) and the northern flying squirrel (Glaucomys sabrinus), for whom over half their diet is from hypogeous fungi, and the long-footed potoroo (Potorous longipes), who's diet is over 90% fungi.
The paradox here is that fungi are generally presumed to be a low-nutrition food item for most mammals. Certainly, fungi are high in many vitamins and are particularly high in mineral nutrients, making them a valuable supplementary food source. However, many fungal carbohydrates and proteins cannot be assimilated by the mammalian digestive system, hence most mammals cannot use them as a primary food source unless they have some way of assimilating these nutrients.
In the case of potoroos, there is a clear adaptation for breaking down these compounds. Potoroos have an enlarged foregut, containing a population of symbiotic anaerobic bacteria that are capable of fermentative breakdown of fungal compounds into forms that are useable by the animal. The ability of the potoroo to utilize fungal nutrients was demonstrated in an experiment by Australian wildlife ecologists Andrew Claridge and SJ Cork, which involved feeding long-nosed potoroos on a diet consisting entirely of two hypogeous fungi, Mesophellia glauca and Rhizopogon luteolus. It was found that the animals were more or less able to maintain their body weight on this diet.
The adaptations found in North American fungivorous mammals are less clear. Claridge and others later carried out a dietary experiment on red-backed voles and northern flying squirrels, feeding them entirely on Rhizopogon vinicolor. In this case, the animals lost weight, demonstrating that their assimilation of fungal nutrients is more limited and that they clearly need other items in their diet. Nevertheless, fungi do make up a large portion of their diet and is unclear how they maximize the nutrition they get from this food source. Anatomically, many murids ("true" mice, rats, and voles) have a large number of mucosal folds in their hindgut. These mucosal folds retain bacteria which may be capable of additional breakdown of fungal compounds; also many of these species are coprophageous, and in this way can redigest foods that have undergone additional breakdown in the hindgut.
While mammals can, to varying degrees, use hypogeous fungi as a food source, what do the fungi get out of it? First, it should be noted that most fungal spores can pass through the gut of an animal undigested, hence, consumption of a fleshy fungus by an animal can serve as an additional vector for spore dispersal. In the case of hypogeous fungi, which have entirely lost their ability to forcibly discharge spores, fungivorous animals are, for the most part, the only effective method of long-distance spore dispersal.
This leads to the questions of whether many spores remain viable after passing through the gut of an animal and whether spore viability is in any way enhanced by digestion. A number of studies have addressed this question. These studies involved isolating spores of Rhizopogon or Mesophellia from various small mammal scats, as well as isolating spores from sporocarps of the same fungi; these spore isolates were then used to inoculate seedlings of ectomycorrhizal tree species, such as Douglas-fir or Eucalyptus. Most of these experiments demonstrated that both digested and non-digested spores were viable and established mycorrhizae on the target trees, with about the same degree of inoculum potential. In one experiment, however, non-digested Mesophellia spores failed to inoculate Eucalyptus trees, while digested ones did so successfully - perhaps the experiment was a fluke, since the results weren't replicated, or perhaps there are conditions under which digestion of spores does help activate them for inoculation.
Hypogeous sporocarps show often other adaptations that indicate a more specific degree of coadaption with mammals. Most small mammals have a very strong olfactory sense, with olfaction being the main way in which they find underground food items. Many hypogeous fungi are characterized by strong odors; this certainly could also serve to attract fungivorous insects, however, at least some hypogeous fungi have scents that mimic mammalian pheromones. More importantly, these scents develop as the spores mature, hence, the strongest smelling sporocarps (which are presumably the ones most attractive to fungivores) are those in which the spores are most ready for dispersal.
In Australia, there is an example of a particularly close degree of coadaptation between Mesophellia and the mammals that consume them, particularly the long-nosed potoroo. Mesophellia is a very common hypogeous fungus in the Eucalyptus forests of Australia (as common as Rhizopogon in North American coniferous forests). It possesses a central columella that is rich in lipids and is a choice food item for fungivorous mammals. This columella is surrounded by a spore mass that is powdery at maturity; an animal that is eating this fungus will have to tear through the outer spore mass to get to columella beneath. In the process, the animal will get spores all over its paws and fur, in addition to ingesting spores. This adaptation bears a very close resemblance to flowers with powdery pollen and a nectar reward.
In addition, there seems to be a third party to this potoroid/fungus mutualism (or really a fifth party, if you count the anaerobic bacteria in the potoroo's foregut, plus the ectomycorrhizal trees themselves). Potoroos and other ratkangaroos often have any of several species of Onthophagus, a type of dung beetle, living in an around their tail. When a potoroo defecates, the beetles immediately jump on the dung; the female beetles then build deep underground nests under the dung pile, while the males deliver dung to them, which they later roll into the dung balls, into which they lay their eggs. The next generation of beetles live off the dung balls, but leave behind quite a bit of the spore-rich dung, which remain buried and can serve as inoculum for mycotrophic roots into which they come into contact.
Mammalian spore dispersal may play a very important role in mycorrhizal recolonization following disturbances such as fire or logging. This is among the factors being looked at by Tom Bruns and others at UC Berkeley studying mycorrhizal recolonization following the Mt Vision Fire at Point Reyes.
The small mammal/hypogeous fungus relationship clearly is a kind of non-symbiotic mutualism with many analogies to a pollination mutualism, and likely plays a key role in ectomycorrhizal forest ecosystems. It might also be kept in mind that, like most mammals, we too are descended from small shrew-like creatures, and it is entirely possible that fungi may have been an important dietary item at some point in our evolutionary history. Hence, our own fungivory may be something deeply rooted in our past.
- Claridge AW, Trappe JM. 2005. Sporocarp mycophagy: nutritional, behavioral, evolutionary, and physiological aspects. In: Dighton J, White JF, Oudemans P, eds. The Fungal Community. 3rd ed. Boca Raton, FL: CRC Press.
- Johnson CN. 1996. Interactions between mammals and ectomycorrhizal fungi. Trends in Ecology and Evolution 11:503-507.
- Luoma DL, Trappe JM, Claridge AW, Jacobs KM, Cazares E. 2003. Relationships among fungi and small mammals in forested ecosystems. In: Zable CJ, Anthony R, eds. Mammal community dynamics in coniferous forests: management and conservation issues in western North America. New York: Cambridge University Press. pp 343-373.
- Trappe JM, Claridge AW. 2005. Hypogeous fungi: evolution of reproductive and dispersal strategies through interactions with animals and mycorrhizal plants. In: Dighton J, White JF, Oudemans P, eds. The Fungal Community. 3rd ed. Boca Raton, FL: CRC Press.
- Werner PG. 2005. Small mammals and hypogeous fungi [website]. Available from: userwww.sfsu.edu/~pgwerner/mycophagy/mycophagy.html