Saprotrophic fungi are the principle decomposers of nonliving plant and animal detritus in the natural environment, thus recycling chemical elements back to the environment in a form other organisms may utilize. Filamentous fungi usually dominate wood and litter decomposing communities, but under particular ecological circumstances, for e.g., for wood in tropical ecosystems termites may predominate, and under waterlogged conditions bacteria may prevail (Rayner and Boddy 1988). Other wood and litter residents may include yeasts, bacteria, Myxomycetes and invertebrates such as Insecta, Oligochaeta, Acaria, and Nematoda. These may influence fungal community dynamics and consequently affect overall decay rates, either via direct interaction, such as antibiosis or grazing of fungal mycelium or spores, or by indirect interaction through impact on the abiotic environment (Dighton 1997; Rayner and Boddy 1988). Thus, invertebrate activity can increase the exposed surface area for decay activity, may provide channels for mycelial invasion, and also improve aeration. Invertebrate waste and remains will also increase local available nitrogen supplies. Therefore, decay of litter and wood in forest systems are ecologically significant and complex processes, produced by intricate and dynamic communities.
5.3.1 Leaf-Litter Decomposition at the Substratum Community Scale
Estimates for litter production in temperate woodlands range from 3.8 ton/ha/yr for oak (Quercuspetraea) and 5.7 ton/ha/yr for Norway spruce (Picea abies), although tropical forest litter production may be twice this. Leaves form the bulk of litter material, representing 65-75% of the total nonwoody input to forest ecosystems. The overall process of leaf decomposition involves the activities of fungi, bacteria, and animals, to produce a humic product, which becomes incorporated into the mineral soil fraction. Litter decomposition may take months (e.g., for Ulmus and Fraxinus excelsior) or years (e.g., for Pinus sylvestris, Quercus, Fagus sylvatica), and may accumulate to form layers if litter production is high and decomposition rates are low. Fungal successions on leaves as they mature, senesce, die and fall, are well characterized and described in detail elsewhere (Andrews and Hirano 1991; Frankland 1984; 1998; Dix and Webster 1995; Kinkel 1991; Ponge 1991). Unfortunately, investigations tend to focus on the generation of lists of species rather than enquiry into the underlying processes involved. Exceptions that attempt to explore the fundamental processes driving population and community dynamics include application of "Life-history strategy" concepts (Andrews and Harris 1986), "Island theory" (Andrews et al. 1987; Wildman 1992) and a dynamic "Patch occupancy" model (Gourbiere et al. 1999). Populations of fungi colonizing needles and leaves are governed by both external climatic effects with implicit immigration rates, and by fungal interaction effects such as competition and successional associations (Gourbiere et al. 2001; Kinkel 1991). Colonization by phylloplane filamentous fungi and yeasts may commence immediately following emergence of a new leaf, and some species may already have a prior colonization history within the bud itself. Fungal spores deposited from the atmosphere must first survive stressful conditions, such as desiccation and rapid wetting, and intense UV and visible light as well as other environmental and climatic factors. Subsequently, primary colonizers overcome leaf inhibitory structures and compounds as well as microbial competition, whilst deriving nutrients via absorption of simple atmospheric nutrient supplies and leaf cell exudates.
Phylloplane and litter studies usually involve cultural methods: either plating of macerated portions or washings from leaf tissue, or of surface-sterilized portions (to distinguish between true colonists and nonviable propagules). However, Frankland (1998) cautioned that plate isolations might generate misinformation by merely selecting certain species from a complex of substratum successions. The isolation of certain species may better indicate the prevalence of dormant survival propagules, than their actual activity within the substratum. Direct observation following brief incubation in damp chambers is also useful, or following staining of leaf surface impressions produced in nail varnish or clear sticky tape, or even via electron microscopy. These different techniques have revealed that many incidental spores are in fact not viable, and that the pattern or succession of true colonizers is remarkably consistent for any particular leaf species, despite the diversity of propagules present. Early colonizers tend to be weak parasites or epiphytic saprophytes, e.g., certain yeasts and the cosmopolitan species Aureobasi-dium pullulans and Cladosporium herbarium, their activity often being restricted to the phylloplane until the onset of leaf senescence. The status of some species may indeed change from epiphyte to endophyte or even to weak parasite, depending on the interaction dynamic with the host plant defenses. Endophytes, pathogenic, parasitic or symptomless, may occupy up to 75% of leaves within a site. However, despite the diversity of endophytic genera involved, which may include Phomopsis, Cryptosporiopsis, and Phoma, the dominant mycoflora appear to be characteristic of the host species, regardless of host geographical distribution, thereby indicating a close evolutionary relationship between plant and fungus (Petrini 1991). Frankland (1998) also recognized the influence of host substrate on fungal species composition. Comparison of successions on different litter and nonwoody plant debris, revealed that the main differences in species composition were the early stage weak parasites, and that the duration of the decay succession, could be attributed to resource quality, particularly nitrogen content and also to levels of fungi-inhibitory tannins. So, Quercus litter with the highest C:N ratio and tannin content was the slowest litter to decay, whereas Fraxinius with the lowest, produced the shortest decomposition period. In fact, during the decomposition of litter collected from a single source, but allowed to decay in adjacent but environmentally dissimilar habitats, similar successions were observed but with different temporal scales (Frankland 1998).
Senescent leaves together with resident mycoflora will eventually fall to the litter or soil surface. Some phylloplane fungi (Aurobasidium spp. and Cladosporium spp.) may persist, and some may even complete their (sexual) life cycle during this phase. However their consequential net decomposition may be very low. Litter is rapidly colonized by certain soil-inhabiting fungi (e.g., Penicillium, Trichoderma, and Fusarium spp.), which appear to cause little direct litter decomposition, but may produce significant indirect effects, such as synergistically increasing decay rates with litter-agarics. The early ruderal strategists are progressively replaced by saprotrophic communities, which decay leaf surface waxes, pectins, and the lignocellulose complex itself. Later significant decay stages are associated with the litter-basidiomycetes, especially agarics such as Mycena, Marasmius, and Clitocybe, which form a significant portion of fungal biomass within litter. Such species are capable of cellulose and hemicellulose hydrolysis and often also ligninolysis, as well as the detoxification of litter phenolics. Mycena galopus is often prevalent in temperate litter, displaying little resource specificity and causing typical white-rot, but is never found in bulky woody debris. Evidently, factors other than lignocellulose decay potential are significant in determining the part an individual may play in litter decomposition. For example, explanation of an apparent paradox co-existence of two litter saprotrophs M. galopus and Marasmius androsaceus both utilizing the same resource but possessing different colonizing vigor, involved microclimatic factors and another trophic level, i.e., preferential grazing by a mycophagous collembolan (Frankland 1998). Certain basidiomycetes show preferences for particular litter types, possibly due in part to the stimulatory effect that certain litter flavenoids have on their growth. So, for example, the growth of certain Clavaria, Collybia, Marasmius, and Mycena species is stimulated by addition of minute quantities of taxifolin glycoside to growth media. However, differences between representative communities occurring on angiosperm and coniferous litter, were attributed more to pH than to leaf phenolic properties (see Carlile et al. 2001 for references). Agarics are also most significant within deeper litter layers, where the improved moisture regime is conducive to basidiomycete growth and they are sheltered from fluctuating climatic conditions. The significant involvement of small soil animals in nutrient cycling, promoting litter decomposition via leaf fragmentation, nitrogen input, and detoxification of phenolics is reviewed elsewhere (Dix and Webster 1995; Ingham 1992).
5.3.2 Attached and Fallen Wood Decay at the Substratum Community Scale
Wood degradation is a relatively slow process that may in temperate woodlands, take tens of years for the decomposition of small branches to several hundred years for large trunks. The heterogeneous and polymeric nature of wood together with low nitrogen and phosphorus content limits decay of woody resources to certain fungi and less significantly to a few bacteria.
The 1980s and early 90s saw major advances in our understanding of the ecology of wood-decay fungi. This is comprehensively reviewed in several extensive and excellent texts (Boddy 1992; Rayner and Boddy 1988; Renvall 1995). Here I will simply present a brief outline. Investigations of indeterminate fungal growth within most natural environments present the ecologist with numerous constraints and practical challenges. However, the colonization of wood by fungi, particularly the higher fungi, provides the ecologist with an unparalleled opportunity to map the spatial activity domain of individuals in situ. Such systems can therefore provide a superb experimental system and conceptual framework for mainstream ecology. Competitive interactions dominate fungal communities within wood (Boddy 2000). Consequently, distinct territories prevail and are delineated within the wood by the production of antagonistic reactions such as pigmented zone lines, and colored activity domains indicated by different types of decay. Moreover, careful examination of wood sections may also reveal relic zone lines indicating the former occupants of woody domain. The community structures of colonized wood at various stages of decay have been mapped and the features affecting community development have been studied, using an astute but simple method based on these principles (Boddy 1992; Rayner and Boddy 1988). Essentially the technique involved sectioning wood, and recording the delineated boundaries of spatial domains occupied by individuals, prior to their isolation onto agar media. Isolates were identified and somatic compatibility of Basidiomycota and Ascomycota assessed using pairing techniques to map the presence of individuals. Interspecific pairing studies were used to assess antagonism and to rank species within a hierarchy of combative ability, to aid inference regarding the order of colonization and replacement (succession) of individuals. Thus, a 3D map may be constructed by aggregating information from serial wood sections. This basic method has also been complemented with other studies involving manipulation of drying regime, temperature, water potential, and gaseous environment. The approach has been used to study the community structure of attached branches and twigs of oak (Quercus petraea and Q. robur), Ash (Fraxinus excelsior), beech (Fagus sylvatica), and birch (Betula pendula) (Boddy 1992; Griffith and Boddy 1991a; Rayner and Boddy 1988). The majority of wood-decay studies have been concerned with basidiomycetes from early stages of decomposition, and with ascomycetes, moulds, and zygo-mycetes particularly from later decomposition stages
(Chapela 1989; Crane et al. 1996; Crawford et al. 1990; Lumley et al. 2000; Rayner and Boddy 1988). Host-wood species, physico-chemical properties, and microclimate govern the basic fungal community dynamics, as does the prior history of the substratum (Barron 1992; Butin and Kowalski 1986; Chapela et al. 1988; Griffith and Boddy 1990; Keizer and Arnolds 1990). Water distribution and its reciprocal relationship with aeration, were identified as principal determinants of colonization patterns (Rayner and Boddy 1988; Griffith and Boddy 1991b). Thus, the moisture relations of living trees inhibit fungal growth and decay by the majority of fungi, except for certain pathogenic and endophytic species. However, to overcome this, some fungi apparently employ a strategy of active wood desiccation to achieve appropriate conditions for establishment and decay (Hendry et al. 1998).
The decay process often commences in the standing tree, in attached lower or stressed branches (Rayner and Boddy 1988). Fungi may gain access either through wounds, tissues following microbial or stress damage or via lenticels or leaf scars. Studies have indicated that pioneer species such as Stereum gausapatum, Phlebia rufa, Phellinus ferreus, Exidia glandulosa, and Vuilleminia comedens in oak or Daldinia concentrica, Hypoxylon rubiginosum, and Peniophora limitata in ash, can colonize living or recently dead wood. The host tree may instigate a response to this invasion, by accelerating localized premature heartwood tissue formation, which contributes to restriction of the invading front. The identification of massive decay columns comprising a single individual extending for several meters along branches known to have been dead for a single growing season only, indicated the involvement of latent invaders (see "Endophytes") initially distributed within functional sapwood as "dormant" hyphal fragments or propagules. Mycelial growth and colonization would then activate from multiple inoculum sites, following stress alleviation for the fungus (usually drying sapwood), imposed by stress aggravation for the host. Ramets of an individual genet could then grow and unite by anastomoses thereby forming extensive decay columns apparently occupied by a single individual. Secondary invaders such as Coriolus versicolor, Phlebia radiata, Sterium hirsutum, and Peniophora lycii in oak, and Radulomyces confluens in ash, could invade and replace pioneers in already dead or decaying wood.
Decomposing dead wood gradually releases sources of nutrients (Harmon et al. 1994). Exposed stumps of felled trees, fallen branches and twigs, or cut timbers may become rapidly colonized by large numbers of individuals of fairly nonselective saprotrophs, thereby forming numerous smaller decay columns. Community structure and development is affected by the degree of exposure, contact with the ground or with other wood, and is influenced by microenvironmental conditions and the arrival mode of individuals. Exposed surfaces may be colonized by established air-borne spores of Coriolus versicolor, Bjerkandera adusta, Stereum hirsutum, Chondrostereum purpureum basidiomycetes or ascomycetes in the genus Hypoxylon or Xylaria commonly on hardwoods.
Such a mode of establishment often produces slower expansion of decay columns compared to that from ground contact, presumably due to the more stressful drying regimes. Buried or ground contact wood may be colonized by soil-derived spores, mycelia, or cords. Later decay stages may involve Mycena galericulata and Pluteus cervinus on hardwoods, or Tricholomopsis rutilans and Paxillus atrotomentosus on conifers. On very wet, well-decayed wood Dacrymycetales such as Dacrymyces stillatus, or discomycetes such as Mollisia cinerea may occur.
That different individuals produce different types and rates of decay is now evident (Worrall et al. 1997). Furthermore, the spatio-temporal combination of extracellular enzymes secreted by a fungus is dependent not only on its evolutionary heritage, but also on the local environmental and biotic conditions (Griffin 1994; White and Boddy 1992a,b). Few studies have related community structure and development with the decomposition process itself. This seems to be a little imprudent as both are obviously intricately linked. Notable exceptions (Coates and Rayner 1985a,b) have demonstrated that inoculation via large numbers of individuals produce slower net decay rates when compared with that for low spore loads, probably due to expression of alternative metabolic pathways related to antagonism between numerous small domains. However, several authors have observed enhanced decomposition rates by mixtures or sequences of fungi (Boddy et al. 1989; Deacon 1985).
5.3.3 Community Studies at the Forest Ecosystem Scale
Direct examination of twigs, branches, and logs for fruiting structures is a traditional method of surveying for basidiomycete and ascomycete activity. But the flora detected using this approach is often very different to that isolated by plating wood portions from interior wood regions. Inferences regarding community dynamics if based on sporophore surveys should be made with extreme caution as their appearance may bear little relationship to the arrival, activity or decline of the supporting mycelia and the relationship will vary for different individuals. Thus, the time taken for the mycelium to derive sufficient resource to devote to sporophore production may be one or more seasons but may be evident only temporarily and the active mycelium of some fungi may not produce sporophores until their final stages of colonization. Some, such as Ganoderma and Fomes produce perennial fruit bodies, which may survive for several years, whereas others may produce seasonal and/or ephemeral fruit bodies. For example, soft-rot fungi such as Chaetomium spp. are prevalent colonizers frequently only detected via plating techniques. Similarly, the dominant ectomycorrhizal species Tylospora fibrillosa in a Sikta spruce plantation was not detected in sporophore surveys, and species indicating most abundant fruiting represented only a very small abundance in association with sampled roots (Taylor and Alexander 1991). Therefore the phenology (climate and time of appearance) and abundance of fruit-bodies for different species must be considered when interpreting survey data. However, careful experimental design and statistical treatment of such data can provide the ecologist with a useful approach to investigating factors influencing fungal community dynamics and decay at the forest ecosystem scale.
Microclimate, substrate quality determined by host species and decay stage, and forest history are cited as being the most significant determinants of fungal community structure in decaying wood (Lindblad 1998; Lumley et al. 2001; Rayner and Boddy 1988; Sippola and Renvall 1999; Vogt et al. 1992; Zhou and Hyde 2001). Other factors affecting species compositions include soil chemical properties (Ruhling and Tyler 1990), and vegetation type (Wasterlund and Ingelog 1981). Furthermore, the initial heterotroph community (bark beetles, ambrosia beetles, moulds, or decay fungi) has been found to influence decomposition or carbon flux in freshly cut Douglas fir (Progar et al. 2000). Multivariate analysis of survey data, such as detrended correspondence analysis (DCA), can indicate the relative importance of these variables for community structure and development within forest ecosystems. In dead-wood, decay state and microclimatic stress have been identified as most influential with some impact of soil conditions (Heilmann-Clausen 2001). Cluster analysis and ordination of microfungus communities in white spruce (Picea glauca) and trembling aspen (Populus tremuloides) fallen logs in disturbed and undisturbed boreal woodland sites revealed tree species to be most influential, followed by stage of decomposition and moisture content (Lumley et al. 2001). From the foregoing, the importance of appropriate moisture regime for decay community development is evident, indeed particularly wet forests have revealed relatively depressed respiration and decomposition rates (Progar et al. 2000). Community analysis can also suggest general trends relating to species diversity and community development. Communities develop relatively quickly and predictably at early decay stages, but become slower and more diversified at later stages as the impact of fluctuating microclimatic stress become more significant due to increasing wood porosity (Heilmann-Clausen 2001). Biodiversity is greatest in undisturbed deadwood, and tends to increase as decay proceeds (Lumley et al. 2001; Norden and Paltto 2001; Renvall 1995). Moreover, some late-stage decay species may be prone to local extinction due to strict successional associations formed between certain species (Niemela et al. 1995).
The DCA of sporophore data from decomposing conifer trunks in northern Finland indicated the development of regular successions of wood-decay fungi. Differences observed among successions were due to associations with the prevailing microclimate and dependent on the resource capture strategies and combative ability of individuals (Renvall 1995). In short, environmental stress created succession pathways for specific saprotrophic groups. Such an inference is very much in accordance with the concept presented by Cooke and Rayner (1984), that community development pathways are initiated under varying degrees of high abiotic stress and/or low stress conditions following disturbance and is subsequently directed by four influences; disturbance, stress aggravation, stress alleviation, and intensification of combat (Boddy 1992).
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