Adding to ‘the enigma of soil animal diversity’: fungal feeders and saprophagous soil invertebrates prefer similar food substrates

Fungal feeding decomposer animals in soil appear to prefer dark pigmented microfungi (often termed Dematiacea) when given the choice. Both fruiting species (e.g. Cladosporium, Alternaria, Ulocladium) and species with sterile dark mycelia are preferred to hyaline species. In laboratory feeding choice experiments other fungi than dark pigmented forms were less preferred (e.g. Trichoderma, Fusarium, and Zygomycetes like Mucor and Mortierella) or rejected even when there was no other choice (e.g. Penicillium, Aspergillus). Interestingly, the soil mesofauna seems to be more selective than the soil macrofauna. These findings are in contrast to the assumption that decomposer animals and soil fungi co-evolved in a way similar to plants and pollinating animals above the ground. The lack of co-evolution between decomposer animals and soil fungi is surprising since below-ground systems are much older than above-ground systems, and therefore, there was more time for co-evolutionary processes. Furthermore, the findings contradict the explanation of the high diversity of fungal feeding decomposer animals by partitioning of food resources. In general, fungal feeding decomposer animals appear to be food generalists rather than specialists. Dark pigmented fungi often comprise 30-60% of fungal isolates from soils; virtually all of them appear to be of high food quality. Four reasons may explain the preference of fungal feeding decomposer animals for dark pigmented fungi. (1) Dark pigmented fungi contain more carbon or nutrients than other fungi. This, however, is unlikely because melanins, the characteristic components of dark pigmented fungi, are recalcitrant compounds, which are hard to digest. (2) Dark pigmented fungi may produce more efficient exo-enzymes than other fungi thereby effectively digesting organic compounds, which may serve as food for the decomposer animals. In this case, the attempt of decomposer animals to feed on dark pigmented fungi only reflects that the animals seek to exploit the superior enzymatic capabilities of dark pigmented fungi (‘external rumen hypothesis’). (3) Dark pigmented fungi may be used as indicators of organic material, which is at a specific stage of decomposition, and therefore, contains nutrients in high concentrations. (4) Dark pigmented fungi may be preferred because they are less toxic than other fungi, or decomposer animals avoid chitinolytic fungi like Trichoderma, Penicillium, Paecilomyces and Mortierella because the animals are in danger of being digested by these fungi. Each of the four hypotheses is little supported by experimental proof and this review, therefore, calls for a more detailed experimental analysis of decomposer animal-soil fungal relationships.