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Fig. 5.9. Example of patterns in fungal species succession and enzyme activity trends over time. (A) Variations in the frequency of single species abundance over time. (B) Enzyme activity patterns over time on a substrate (adapted from Rosenbrock et al., 1995).

Another important study described the spatial segregation of Basidiomycota species on decomposing Picea abies and Pinus sylvestris naturally fallen tree trunks, in a northeast Finland boreal forest (Renvall, 1995). During decomposition, the wood undergoes chemical modifications, which in turn cause structural changes in the matrix. The bark decays or falls more rapidly. The wood increases in water content with capillary water infiltration in the increasingly porous matrix. Waterlogged wood becomes anaerobic and inhibits much of the eukaryote activity. Overall, 120 species of Basidiomycota were found growing in Picea and 104 in Pinus. When considering the number of species found, one wonders whether there can be the same number of niches on a single tree trunk. The description suggested that indeed there are sufficient microhabitats to accommodate at least a majority of the species. In part, seasonal preferences in activity period can account for some of the species diversity. Succession over the period of tree decomposition and microhabitat differentiation within the tree can account for some of the remaining diversity. Several of the conclusions are outlined here. Species were restricted in substrate-volume colonized along the length of the tree. There were species that clearly preferred the base of the tree, and others that preferred the crown, or areas in between. This reflects the changing composition of the tree cell walls and tissues along the length, from old to young. Early saprotrophs give way to later colonists which tend to be more specialized and k-selected species. The growth of certain species was profuse and colonized large volumes, whereas other species were restricted to small volumes. These may reflect competition and inhibition between species. However, one also needs to consider the palatabil-ity of various hyphae to grazers inside the wood. The white rot species were more restricted in time and successional sequence than brown rot species. The brown rot fungi were active for longer durations but decreased in abundance from 25 to 7% of total species with progressing decomposition. The lignolytic Basidiomycota differed greatly in their physical matrix (substratum) requirements. The presence of lignin in itself was insufficient to describe their species composition. They also vary in their competitive ability with each other, as well as preference for the extent of decomposition prior to colonization. Co-occurring species may be competing for space on resources, or they may be utilizing different molecular components of the trunk, or different depths within the tree. Certain species tend to be followed by others. There was some sequence to species succession, but a stochastic element remains depending on which of several possible successional species arrives first. This observation was particularly striking when trees that had fallen for different reasons were compared. The author distinguishes between downed trees caused by fire, sickness, drying or live fall. In each case, the initial colonizing community was different. This affected the subsequent succession of species. There were species that were characteristic of a particular tree species, of a particular stage of decomposition, or of a particular sequence in succession. However, most species were rare, and not many were very common. These observations should be expanded in the future by determining the enzymatic functions of species in the sequence. Species composition may reflect some stochastic element in colonizing ability and competitive ability with existing colonists; however, at the functional level, the enzymatic sequence may be more similar. The author (Renvall, 1995) further points out that as we continue to destroy old growth forests, fungi that are specific saprotrophs of old mature trees with thick trunks no longer have adequate substrate in our young managed forests. The longer the spores remain inactive, they are buried in the litter and in turn decomposed. These species are probably increasingly rare as inactive spores, or are extinct.

The combative interactions of wood-decaying Basidiomycota on wood over succession on the substrate were reviewed recently (Boddy, 2000). The conclusions of the review in large part confirm what we have described here previously, regarding abiotic tolerance and preferences of fungi, and the interactions between coexisting individuals and species. New colonization of substrate by a species is followed by attempts at colonization by new arrivals. This leads to either inter-specific contact between mycelia, or antagonisms at a distance between adjacent mycelia, or consumption of one mycelium by the other (the author uses the misleading term 'mycoparasitism'). The end results of these interactions are most simply categorized as deadlock or replacement of one species by another over time. In particular, growth of one fungus around the periphery of another mycelium may completely prevent its expansion and limit its activity. Mutually tolerated growth is possible when species benefit from the functional role of enzymes and growth properties of coexisting species. As one substrate is exhausted and the matrix structure changes, species that were competitive give way to other species which are more competent on the remaining substrates. The review points out that different strains of the same species often vary in their ability to compete with other species. (There is probably an allelic polymorphism between populations.) Furthermore, the outcome between species is significantly affected by water potential, temperature, and soil or substrate air composition. For example, Basidiomycota require more water (less than -4.4 MPa) than xylariaceous Ascomycota, which can function at lower water potential. In some cases where contact between mycelia is not tolerated or inhibited, one species can destroy the other's mycelium. In most cases, the inhibition or cell lysis that ensues is caused by secondary metabolites, not by digestive enzymes. When it is caused by digestive enzymes, it is best described as predatory consumption of the mycelium. This is in contrast to decomposition of dead hyphae by primary saprotrophs. In general, the outcome of species interactions is not always predictable. Sometime, one species may have grown 'sufficiently' in a given volume to make it difficult for a competitor to establish a colony. The exact nature of these interactions is not always obvious, and requires experimental validation.

In the field, these direct interactions between mycelia are affected by the composition of the rest of the decomposer food web. In a review of fungal succession (Frankland, 1998), the case is made with Mycene galopus in northern temperate forests. It is a major decomposer of plant litter, which digests in vitro all major components of the plant cell wall. This species is not very effective on wood as it is susceptible to wood-inhibitory chemicals, and it requires more oxygen than is available inside the wood matrix. The fungus is seasonally active on new litter in autumn, where it effectively keeps out competing colonizers. One of its competitors is in fact more effective when it arrives first. However, its growth is limited by Collembola grazing because it has a preferred tasty hypha. That grazing preference is sufficient to cause the difference in species abundance, with Mycene galopus dominating.

These descriptive observations of species succession can be extended in the laboratory with functional assays. Moreover, many edaphic species do not form easily visible reproductive structures, and are more difficult to identify from field samples. They require molecular identification, especially if isolates are not easily cultured. Species baited on particular substrates can be obtained naturally and kept on agar plates in the laboratory. These can be assayed for enzymatic activity, for molecular identification, or forced to compete with other isolates on agar plates. For example, a study with sterile animal hair (wool) followed decomposition by fungi on Saboureau-dextrose agar (Ghawana et al., 1997). The authors observed that initial colonists did not digest keratin, but were gradually replaced by keratin-digesting species such as Acremonium species, Chrysosporium species and Trichophyton simii. These were more specialized and became dominant as other substrates (with more easily digested bonds) became exhausted. Similarly, Holmer and Stenlid (1997) tested the competitive ability of Basidiomycota on wood discs placed on water-agar. These types of studies, although they are simple and descriptive, open the way for extended and more detailed experimentation of parameters that control species activity periods and digestive enzyme secretion.

One example of a more elaborate description of fungal primary decomposition and succession is provided by Osono and Takeda (2001). The study was conducted along a hill slope, in a cool temperate deciduous forest in Japan. Beech leaves were selected because they harboured numerous fungal species in succession and because they decompose relatively slowly. Two sites along the hill slope were used to set leaf litter bags in 2 mm mesh: an upper moder soil and a lower mull soil 200 m away. The rate of decomposition at the two sites was about the same, with about 55% mass remaining after 35 months. The litter bags were sampled by first removing the surface spores (surface sterilization or surface washing), then making observations on the hyphae within the tissue by culture on agar plates. The extent of hyphal mesh in the litter was estimated by a grid intersect method using calcofluor white stain for the cell wall and acridine orange for the nuclei in living hyphae. The litter samples were assayed for content in lignin, holocel-lulose, soluble carbohydrates, phenolics, and total N, P, K, Ca, Mg. Sequential loss of cell wall components indicates indirectly the enzymes that were active in the leaf litter. The rate of loss followed the sequence: polyphenols>soluble carbohydrates>holocellulose>lignin. Both N and P increased at first, indicating colonization with living biomass and increase in living cytoplasm from saprotrophs. It is followed by a decline, as fewer living hyphae remain and nutrients are mobilized. The minerals K, Ca and Mg fluctuated up and down in abundance, but with an overall decrease over this time period. This reflects changes in the species composition in the litter as well as release of nutrients from the litter. Graphs of the frequency of occurrence of Ascomycota species over 35 months showed periods of activity that succeed each other. There was an increase in species with clamp connections near the end of the sampling period. The authors suggest that this reflects a functional shift that occurred at about 21 months. Interestingly, the percentage of living fungal biomass remained more or less steady as a fraction of the litter mass. It fluctuated between 6 and 2%. However, total hyphal biomass that includes the abandoned cell walls peaked between 7 and 12 months. Succession of species isolated from the litter bags established that there were particular fungal species associated with particular stages of primary decomposition.

Lastly, any section on fungi would be incomplete without some consideration of the yeast forms. These are rarely sampled by soil ecologists, but there is clearly some pattern that can be described (Spencer and Spencer, 1997). Many species are associated with surfaces of plants and insects where they grow by osmotrophy on the tissue secretions or leakage. Alternatively, some are intracellular symbionts of invertebrates. They find their way into the soil on death of the organisms, where they are picked up again or dispersed on to new hosts. These yeasts are transient species in the soil, not necessarily adapted for soil growth at all. Some species are true edaphic species particularly in the genera Candida, Cryptococcus, Hansenula, Lipomyces and Pichia. Most soil species are non-fermentative Basidiomycota. Abundances are often 1.4 X 104/g soil in surface layers, decreasing to 600-1800/g in subsurface layers. There is a seasonal increase in abundance during the summer months. Habitats with enriched yeast species are limited to fruit-fall periods and fruit wastes, where abundances increase to 104-105/g. However, after oil spills, some species increase in abundance as they can metabolize a wide range of aliphatic and aromatic organic molecules, in both soil and marine environments. Yeasts are sensitive to the presence of Actinobacteria, which inhibit their growth by antibiotic secretion. They are preyed on by grazing invertebrate larvae and some adult forms, especially of certain microarthropods. Ingestion of yeast cells by protozoa and nematodes is also common. Many bacterivorous species can be cultured on yeasts. The distribution of yeasts in the soil may not be limited by oxygen as some species are anaero-tolerant and capable of fermentation. It is probable that they are enriched in certain riparian or regularly flooded soil that is also rich in organic matter. Whether they contribute to soil food webs in any significant amount is unclear. They may be infrequently active opportunists.

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