15.1 Fungal co-operative ventures
We have already discussed the circumstance in which fungi are used as food for grazing animals, from cattle weighing hundreds of kilograms to the microarthropods weighing hundredths of a gram (see the section entitled Fungi as food in Chapter 11; CLICK HERE to view the page). Fungus fruit bodies are used as a useful dietary supplement by large mammals like deer and primates (Hanson et al. 2003) although lichens (Cladonia spp.) form an essential part of the winter diet of reindeer (Rangifer tarandus) (Kumpula, 2001; Oksanen, 2006; Olofsson, 2006) and the reindeer, which are ruminants, have behavioural and anatomical adaptations enabling them to graze lichens under snow cover and digest the fragments.
Many invertebrates use fungal mycelium as a major part of their nutrition, approximately 80% of the tens of thousands of microarthropod species in forest soils being fungivores (or mycophagous) that depend on the fungal mycelium as their main or only food source. The many small animals involved are summarised in the Resources Box Life in the Soil (CLICK HERE to view the page now).
At the microscopic level, some of the smallest grazers on fungi are organisms known as collembola. These plentiful, soil-dwelling, wingless microarthropods derive from some of the most ancient lines of insects. Collembola are an integral part of the soil environment feeding upon many different organisms including bacteria, lichens, and decomposing material, but collembola show a preference to feed on fungal hyphae over all other food sources. Collembola such as Folsomia candida have been shown to reside in the upper (litter) layers of the soil, often choosing to feed on the hyphae of saprotrophic (conidial) fungi rather than the hyphae of mycorrhizal fungi. They also preferentially graze on the hyphal tips and fine mycelium and in woodlands this type of grazing may impede the growth of mycelial networks and their ability to decompose dead organic material (Tordoff, Boddy & Jones, 2006; Wood et al., 2006).
The well co-ordinated nature of mycelial networks ensures that a morphological reaction occurs in response to grazing damage in many species of fungi, which can be interpreted as a method of evading the grazing animal. This implies that even at this level there is an evolutionary link between the grazing animal and the fungus. Indeed, collembola may even be perceived as mutualistic under some circumstances as they sometimes promote extra growth of the fungus as the mycelium overcompensates for grazing damage, producing a net increase in biomass, though this happens only when sufficient nutrients are available to the fungus (Bretherton et al., 2006).
Another factor known to influence the presence of collembola in soil is the presence of endophytic fungi in the leaves of grass growing on the soil. Leaf litter infected with fungal endophytes appears to decompose faster than uninfected plant matter, possibly due to the presence of toxins changing the composition of soil communities to produce a higher proportion of detritivores (Lemons, Clay & Rudgers, 2005). Endophytes deter larger animals, such as cattle, from grazing, thereby performing a protective function for their host (see Introduction to endophytes in Chapter 13; CLICK HERE to view the page) but in so doing they are also interacting with the animals by determining the palatability, digestibility or nutritional value of their food source.
Our next topic is a classic mutualism, but this time with the fungus encouraging grazing rather than attempting to deter the fungivore. Attine ants are a group of more than 200 fungus-growing ant species living in the Neotropics (Central and South America) that have a rather unusual ability to cultivate fungi. Most use leaf-litter debris for fungal cultivation, but the leaf-cutter ants (Atta spp. and Acromyrex spp.) cut and collect fresh leaves to grow two genera of fungi, Leucocoprinus and Leucoagaricus in the family Lepiotaceae (Basidiomycota: Agaricales) (Mueller & Rabeling, 2008). This ant-fungus mutualism shows how successful a relationship like this can be (Mueller et al., 2001).
Fungus cultivation evolved apparently only once in the attines, about 45-65 million years ago. The ants actively inoculate their nest with the fungus and then cultivate it by providing it with pieces of leaves, pruning the hyphae and removing intruder fungi. As a reward, the fungus provides bundles of specialised hyphae that the ants use as a food source; these are the gardening ants (Vega & Blackwell, 2005). The ants are engaged in an agricultural activity; they collect fresh leaf biomass to convert it to compost in order to cultivate a particular fungus that then provides the main food source for the nest. Schultz & Brady (2008) point out that agriculture is a specialised symbiosis that is known to have evolved in only four animal groups: ants, termites, bark beetles, and humans.
Updated December 17, 2016