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Basidiomycete Mycelia in Forest Soils: Dimensions, Dynamics and Roles in Nutrient Distribution

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Basidiomycete Mycelia in Forest Soils: Dimensions, Dynamics and Roles in Nutrient Distribution Mycol. Res. 109 (1): 7–20 (January 2005). f The British Mycological Society 7 DOI: 10.1017/S0953756204001753 Printed in the United Kingdom. Review Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution John W. G. CAIRNEY Centre for Horticulture and Plant Sciences, University of Western Sydney, Parramatta Campus, Locked Bag 1797, Penrith South DC, NSW 1797, Australia. E-mail: [email protected] Received 15 July 2004; accepted 3 October 2004. Basidiomycete mycelia are ubiquitous in forest soils where they fulfil a range of key ecological functions. Population studies, based largely on basidiome collections, indicate that mycelia of many ectomycorrhizal and saprotrophic basidiomycetes can spread vegetatively for considerable distances through soil, but the extent to which these become physically or physiologically fragmented is unclear. This review considers aspects of the distribution, dynamics and translocatory activities of individual basidiomycete mycelia in forest soil, highlighting current gaps in our understanding and possible ways to address these. INTRODUCTION in soil have been constrained by a lack of suitable techniques for discrimination between them, but some On the basis of basidiome collections, it is evident that progress is now being made. A useful method for esti- forest soils in a broad range of habitats house diverse mating ECM mycelial biomass in forest soils has, for communities of basidiomycetes (e.g. Schmit, Murphy example, recently been developed (Wallander et al. & Mueller 1999, de la Luz Fierros, Navarrete-Heredia 2001). This involves burying mesh bags containing & Guzma´n-Davalos 2000, Ferris, Peace & Newton sand in forest plots and comparing mycelial biomass in 2000, Packham et al. 2002). These include sapro- bags from trenched plots (designed to sever ECM roots trophic, mycorrhizal and pathogenic taxa which, col- from their tree hosts, and so exclude ECM mycelia lectively, play important roles in nutrient and carbon from the plots) with those from untrenched plots. Such cycling processes (Dighton 2003). Studies of basidiome comparisons, along with supporting d13C values, diversity and distribution, however, provide only a suggest that in Swedish conifer forest soils, 85–90% of limited, and extremely selective, view of basidiomycete mycelium that colonises the sand-filled bags is ECM occurrence in forest soils. There is ample evidence, for (Wallander et al. 2001, Hagerberg & Wallander 2002). example, that basidiome collections are poor indicators The sand-filled mesh bag approach has thus been useful of below-ground ectomycorrhizal (ECM) fungal diver- in demonstrating that ECM mycelial biomass varies sity and that below-ground diversity is much greater seasonally (Wallander et al. 2001) and with soil depth than implied by basidiome studies (Erland & Taylor (Wallander, Go¨ransson & Rosengren 2004), along with 2002). Observations of this nature emphasise the need determining the effect of differing forest management for more direct analysis of basidiomycete mycelia in regimes on ECM mycelial biomass (Hagerberg & soil. Wallander 2002, Nilsson & Wallander 2003). A less While methods for estimating fungal biomass in soil, direct method that involved tree girdling, soil fumi- such as ergosterol or phospholipid fatty acid analysis gation and measurements of dissolved organic carbon, (Zelles 1999, Montgomery et al. 2000), have provided has also been used to estimate that ECM mycelium useful information regarding the importance of fungi may contribute >32% to the soil microbial biomass in in soil microbial communities, they tell us little about a Swedish conifer forest (Ho¨gberg & Ho¨gberg 2002). the different functional or taxonomic groups of fungi. Important as these data are, however, they provide no Investigations of mycelia of specific fungal groups information regarding mycelia of individual taxa. Basidiomycete mycelia in forest soils 8 Their indeterminate filamentous nature creates depend on the relative size and quality of the woody obvious problems for investigation of mycelia of indi- resources, mycelium that interconnects old and new vidual basidiomycete taxa in the heterogeneous soil woody resources, or in the case of ECM fungi individ- environment. When considering individual mycelia of a ual root tips, may regress and become more rhizo- single taxon, the task becomes considerably more morphic, while extensive outgrowth of exploratory complex. Knowledge of the distribution, dynamics and fan-shaped mycelium may follow (Dowson et al. 1986, activities of individual mycelia in soil is, however, cru- 1989b, Read 1992, Boddy 1993, Wells, Donnelly & cial to understanding how different taxa influence and Boddy 1997, Donnelly et al. 2004). Discrete patches of modify the soil environment, along with the spatial and organic matter or mineral nutrients in soil microcosms temporal scales over which they operate. In this review can also influence mycelial growth, with several ECM I summarise current understanding of the distribution and saprotrophic taxa having been shown to grow re- and activities of individual basidiomycete mycelia in actively to form dense mycelial growth in such patches forest soils, and highlight some fundamental gaps in (e.g. Finlay & Read 1986a, b, Bending & Read 1995, our knowledge. Donnelly & Boddy 1997b, Wells et al. 1997, Perez- Moreno & Read 2000, Mahmood et al. 2001, Tibbett & Sanders 2002, Lilleskov & Bruns 2003, Donnelly et al. 2004, Rosling, Lindahl & Finlay 2004). More general MYCELIAL GROWTH AND DYNAMICS soil characters, such as physical structure, carbon or IN MICROCOSMS mineral nutrient status, temperature, water potential, Because of the difficulties in identifying mycelia in the pH and litter type have also been shown to influence field, investigations of the development and dynamics mycelial growth and development in soil microcosms of mycelia of individual basidiomycetes have largely (Morrison 1982, Erland, So¨derstro¨m & Andersson been conducted in the laboratory. A variety of methods 1990, Arnebrant 1994, Abdalla & Boddy 1996, has been utilised (e.g. Jennings 1991), however those Donnelly & Boddy 1997a, b, 1998, Boddy 1999, Wells, based on a non-sterile soil (or similar) substrate provide Thomas & Boddy 2001, Zakaria & Boddy 2002, the most useful information regarding likely behaviour Aquino & Plassard 2004). The ability of soil-borne of mycelia in the field, thus only these are considered mycelia to grow reactively in the heterogeneous soil here. environment is regarded as important to their func- Development of mycelial systems of various sapro- tioning in soil and has been discussed in the context of trophic and ECM basidiomycetes has been investigated foraging strategies elsewhere (e.g. Rayner 1991, Read extensively in soil-based microcosms. This approach 1992, Boddy 1993, 1999, Olssen et al. 2002, Donnelly has been important in demonstrating patterns of de- et al. 2004). velopment and temporal change with respect to diffuse The presence of other soil organisms, such as fungi- versus rhizomorphic components of mycelia growing vores, can further influence the growth and develop- from colonised wood (e.g. Dowson, Rayner & Boddy ment of basidiomycete mycelia in soil. Growth of ECM 1986, 1988a) or ECM roots (e.g. Duddridge, Malabari mycelia can be reduced by the presence of grazing & Read 1980, Read 1984, Finlay & Read 1986a) along collembolans, although this may depend on the popu- with interspecific differences in mycelial growth forms lation density of the fungivore (Ek et al. 1994, Seta¨la¨ (e.g. Dowson, Rayner & Boddy 1986, 1988a, Dowson 1995). Extensive invertebrate grazing can eliminate et al. 1989b, Donnelly, Boddy & Leake 2004). Mycelia rhizomorphic mycelia of certain saprotrophs from soil, of many taxa typically grow as diffuse fans, with pro- while lower grazing intensity can significantly alter gressive aggregation behind this growing front into mycelial morphology (Boddy 1999). In the case of the aggregated rhizomorphic structures (Read 1992, Boddy wood decomposer Hypholoma fasciculare, certain col- 1993, 1999, Olssen, Jakobsen & Wallander 2002). It lembolan taxa were shown to reduce diffuse mycelial has also become evident that growth of basidiomycete growth, with the fungus adopting a more fast-growing mycelia is strongly influenced by soil heterogeneity, in rhizomorphic growth pattern (Kampichler et al. 2004). particular the patchy distribution of organic substrates and mineral nutrients. Thus, when a mycelium of a wood decomposer encounters and colonises a new INTERSPECIFIC MYCELIAL woody resource, the pattern of mycelial growth has INTERACTIONS IN MICROCOSMS been shown to change, with invasive mycelia growing in a diffuse fashion (e.g. Dowson et al. 1986, Donnelly Interactions between mycelia of different saprotrophic & Boddy 2001). Similarly, hitherto undetermined fungi have been observed in soil microcosms in a signals between fungus and plant trigger a series of number of investigations, and can significantly alter morphogenetic events following contact between an patterns of mycelial growth. These interspecific ECM mycelium and a host root that leads to formation encounters result either in a ‘deadlock’ situation where of the fungal sheath and Hartig net (Martin et al. 2001). there appears to be a mutual interference between the Soil microcosm studies have also shown that, different taxa, or a ‘replacement’, where mycelium although for saprotrophic basidiomycetes it appears to of one taxon will out-compete another in soil and/or
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