Invertebrate Effects On Fungal Community Structure

Invertebrates have differential effects on different species of fungi, resulting from different extents and sites of grazing, secretion of various chemicals including antibiotics, and from physical effects. Consequently, they can affect the species balance within fungal communities. For example, Collembola grazing alters the vertical distribution of Marasmius androsaceus and Mycena galopus in spruce (Picea sitchensis) needle litter (Newell, 1984a, 1984b): Onychiurus latus fed preferentially on M. androsaceus in laboratory and field tests caused the restriction of this species to the uppermost litter horizon. In inter-specific mycelial confrontations in agar culture and trays of soil in the laboratory, the balance was shifted in favour of one species over another when grazed by the Collembola F. candida; for example, in the absence of F. candida, R. bicolor overgrew P. velutina, whereas with Collembola grazing P. velutina was able to breach the R. bicolor advancing front (T.D. Rotheray et al., unpublished).

In small angiosperm branches decomposing on the forest floor there is a dramatic change in fungal communities following invasion by soil invertebrates: prior to invasion communities are dominated by Basidiomycota, but post-invasion by non-Basidiomycota, presumably resulting from destruction of resident fungi by feeding action, carriage and inoculation of spores of other fungi, and change in microenvironmental conditions (Swift and Boddy, 1984; see below).

The mutualism between Macrotermitinae and Termitomyces species, in which the former cultivate the latter within their nests, is even more dramatic. Termitomyces species are poor competitors and are rapidly over-run if the termites abandon the nest, but are maintained in the fungus comb in active nests in more or less pure culture, despite continual inoculation with other fungi on plant material collected by the termites (Wood and Thomas, 1989; Shinzato et al., 2005). Passage through worker guts reduces germination of non-mutualistic symbiont spores, oral secretions are fungistatic, and nest microclimate (30 °C and elevated CO2) is optimal for the fungal symbiont. There also seems to be genetic screening of Termitomyces strains, either directly via active selection by the termite or indirectly by intra-specific competition on the fungus comb, as evidenced by identical fungal molecular sequences in multiple samples from four different nests of species that have horizontal symbiont transmission (Aanen et al., 2002; see also below).

In the mutualism between attine ants and Leucoagaricus spp., Lepiota spp. and other Basidiomycota (Mueller, 2002), the fungi are more competitive than in the termite-fungus mutualism, being able to survive for approaching 12 days following abandonment (Bass and Cherrett, 1994). Nonetheless, contaminants are kept out by physical removal of spores by licking, chemical secretions from the ants (Hernandez et al., 1999; Ortius-Lechner et al., 2000), along with antibiotics secreted by actinomycetes (Streptomyces) targeted at a virulent Ascomycota mycoparasite (Escovopsis; Currie et al., 1999).

Studies in Mexican tropical cloud forest suggest that variability in fungivory (apparent biomass consumed) of understorey Basidiomycota by invertebrate taxa could be explained by apparency (sensu Feeny, 1976; ''ease of finding'')-related characteristics of the above ground structures (colour of pileus, stipe and hymenium; size and aggregation), as has been suggested for plant-herbivore relationships (Crawley, 1983). Considerable inter-specific and inter-taxa variation in fungivory was detected; colour attributes of fruit bodies were not strongly associated with the observed variation of consumption levels, whereas apparent biomass and aggregation size did correlate with the observed variation in fung-ivory. It was concluded that colouration patterns may not be important for fung-ivory, whereas genet size and species identity (probably via characteristics unrelated to apparency, such as mycotoxins and nutritional value) seemed to be critical factors (Guevara and Dirzo, 1999). In another example, screening forest soil nematodes for associated fungi showed that the pathogenic fungi Malassezia restricta and M. globosa were associated with the nematode genus Malenchus sp., whereas another nematode, Tylolaimophorus typicus, hosted only M. restricta (Renker et al., 2003). Preferences have also been shown by lumbricids: L. terrestris took far fewer wheat straws colonized by Agrocybe praecox than by non-Basidiomycota (Moody et al., 1995).

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