Mycelia Foraging Between Resources Distributed Heterogeneously In Space And Time

Fungi that utilize spatially discrete resources, with centimetre- or even metre-scale separations, have developed a variety of foraging strategies. They commonly form linear mycelial aggregates termed rhizomorphs, e.g. Marasmius androsaceus and Armillaria spp., or cords, e.g. Hypholoma fasciculare and Phanerochaete velutina (e.g. Boddy, 1984, 1993, 1999; Hedger, 1990; Cairney, 1992, 2005; Rayner et al., 1995; Boddy and Jones, 2006). Rhizomorphs are linear organs, with a thick melanized rind, the whole organ extending from the tip (Rayner et al., 1985). Mycelial cords are also insulated from the environment with a thick rind, but they develop from a mycelial margin of diffuse hyphae, each of which extends apically. They can all draw on water, nutrients and energy held within other parts of the mycelium to sustain growth outside the organic resource(s) to which they are connected. In addition, although mycelial cords are insulated from the environment, they are able to absorb water and soluble nutrients via individual hyphae at the mycelial margin or that sometimes develop elsewhere forming patches, and they may colonize small litter components en route to large organic resources (Boddy, 1999; Watkinson et al., 2006).

Fungi producing extra-resource mycelium risk loss of a large amount of biomass, as a result of invertebrate grazing, antagonistic microorganisms or death due to an unfavourable microenvironment. This can be minimized by a variety of different strategies. These include: (1) active growth and search for new resources; (2) a 'sit and wait' strategy, in which a mycelial network awaits arrival of resources, e.g. by branch fall, and then active colonization, often responding elsewhere in the system; and (3) most commonly, a combination of both. With all these strategies the mycelial networks are continuously remodelled in response to environmental cues, which can be abiotic (e.g. nutrient sources, microclimate or destructive events) and biotic (e.g. interaction with other fungi or grazing by invertebrates). Remodelling occurs through a complex combination of growth, branching, hyphal fusion and regression of different mycelial regions. Throughout the network, not only does morphology alter but also a complex set of physiological processes associated with uptake, storage and redistribution of nutrients change (Bebber et al., 2006; Watkinson et al., 2006). Both morphological and physiological changes are highly coordinated so that responses to local environmental changes can propagate through the mycelial network.

4.1 Search and Response Behaviour

Fungi have evolved a wide variety of patterns of mycelial outgrowth from resources into soil and litter (Figure 2; Boddy, 1999; Boddy and Jones, 2006). These have been quantified in terms of radial extension rate, hyphal coverage, and surface and mass fractal dimension (Ds and DM, respectively) (Boddy, 1999; Boddy et al., 1999; Boddy and Donnelly, 2007). These range between mycelia characterized by diffuse, slowly extending search fronts, with a high DM (close to the maximum of 2 in two dimensions), e.g. H. fasciculare (Figure 2b) and Stropharia

Figure 2 Patterns of mycelial outgrowth of four cord-forming basidiomycota across compacted soil in 24 x 24 cm trays from x cm (a-e) and y cm (f) Beech (Fagus sylvatica) wood inocula. (a) Coprinus picaceus, (b) Hypholoma fasciculare, (c) Phallus impudicus, (d) Resinicium bicolor and (e and f) Phanerochaete velutina. Digital images (a)-(d) courtesy Alaa Alawi, and digital images (e) and (f) from photographs taken by Rory Bolton.

Figure 2 Patterns of mycelial outgrowth of four cord-forming basidiomycota across compacted soil in 24 x 24 cm trays from x cm (a-e) and y cm (f) Beech (Fagus sylvatica) wood inocula. (a) Coprinus picaceus, (b) Hypholoma fasciculare, (c) Phallus impudicus, (d) Resinicium bicolor and (e and f) Phanerochaete velutina. Digital images (a)-(d) courtesy Alaa Alawi, and digital images (e) and (f) from photographs taken by Rory Bolton.

spp., and open systems characterized by well-defined, rapidly extending cords throughout the system, with a lower DM (between 1 and ~1.8), e.g. Agrocybe praecox, Coprinus picaceus, Phallus impudicus, P. velutina and Resinicium bicolor. The former can be considered to be short-range foragers that are likely to be successful in discovering and exploiting abundant, relatively homogeneously distributed resources as they search areas intensively (Figure 2b), and the latter longrange foragers that would be less successful at capitalizing on relatively homogeneously supplied nutrients, but would successfully discover large, more sparsely distributed resources. Mycelial systems tend to become more open with time as they become larger (DM decreases; Donnelly et al., 1995; Boddy et al., 1999; Figure 2a, c and d; patterns are modified by the quantity and quality of the resource from which the mycelium is extending (Bolton and Boddy, 1993; Donnelly and Boddy, 1997a; Boddy et al., 1999; Zakaria and Boddy, 2002; Figure 2e and f), soil structure and nutrient status (Donnelly and Boddy, 1998; Boddy et al., 1999; Zakaria and Boddy, 2002), microclimate (Donnelly and Boddy, 1997b; Owen, 1997; Wells et al., 2001), interaction with mycelia of other species (Donnelly and Boddy, 2001) and invertebrate grazing (Kampichler et al., 2004; Harold et al., 2005; Bretherton et al., 2006; Tordoff et al., 2006; Wood et al., 2006; Chapter 9).

When new resources are encountered the mycelium responds with dramatic changes in morphology (network architecture) and often with considerable reallocation of biomass. When the new resources are substantially larger than those from which the mycelium emanated, mycelium connecting the new resource with the original resource usually aggregates to form thick cords, while radial extension slows or ceases, and non-resource-connected mycelium regresses (Dowson et al., 1986, 1988; Bolton et al, 1991; Boddy, 1993, 1999; Bolton, 1993; Donnelly and Boddy, 1997a; Figure 3a-c). Subsequently mycelium grows out from the newly colonized resource, and foraging continues, though the amount of time before foraging continues depends on the sizes of the original and new resource (Bolton, 1993; Boddy and Jones, 2006). With short-range foragers (e.g. H. fasciculare), there are similar, although less dramatic, changes to system architecture even when newly encountered resources are similar in size to the original resource.

Not only does the mycelium respond by changes to network architecture but also with physiological responses: there is highly coordinated uptake, storage and redistribution of nutrients throughout the network (Watkinson et al., 2006; Chapter 3). Mineral nutrients (e.g. nitrogen and phosphorous) can be transported from wood resources to support growth at the mycelial margin, and nutrients scavenged as mycelia extend through soil can be translocated away from sites of uptake to sites of demand or storage, and commonly accumulate in wood resources connected within the mycelial system (Wells and Boddy, 1990; Wells et al., 1990,1998,1999; Cairney, 1992 Hughes and Boddy, 1994; Olsson and Gray, 1998). Rates of translocation can be rapid (sometimes >25cmh_1), the largest fluxes being through cords interconnecting resources (e.g. Wells and Boddy, 1990). Many factors, including the overall nutritional status of the mycelial network, and the distribution and quantity of colonized and newly encountered organic resources, affect the balance between, and the main sites of, uptake, storage and demand for carbon and mineral nutrients (Abdalla and Boddy, 1996; Hughes and Boddy, 1996; Wells et al, 1998, 1999; Boddy and Jones, 2006).

4.2 Persistent Mycelial Networks: 'Sit and Wait' Strategy

Saprotrophic cord- and rhizomorph-forming Basidiomycota produce extensive long-lived mycelial networks on the forest floor, eventually covering several square metres to many hectares (Thompson and Rayner, 1982; Thompson and Boddy, 1988; Smith et al, 1992; Ferguson et al., 2003; Cairney, 2005; Figure 1e). The largest recorded to date is a genet of Armillaria ostoyae spanning 965 ha, with a maximum separation of 3,810 m and estimated as 1,900-8,650 years old (Ferguson et al., 2003). The true extent and degree of connectivity within a genet is not known, however, since parts of mycelia can be separated from each other during development, and can also rejoin if parts of the same genet meet again. Similar systems are also found in the canopy of tropical forests where they effectively form a net (Hedger, 1990). Whether on the forest floor or in the canopy, these large, persistent networks allow capture of resources arriving by litter fall or root death at any time.

Although persistent, established systems are dynamic both as continued extension at growing fronts (Thompson and Rayner, 1983) and as renewed mycelial growth from mature cords. Arrival of new resources can result in reallocation of

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Figure 3 Reallocation of mycelial biomass of Phanerochaete velutina following colonization of new wood resources. (a-c) Extending from a 0.5 cm3 beech (Fagus sylvatica) wood inoculum to an 8 cm3 wood resource, in 24 x 24 cm trays of non-sterile soil, after, respectively, 11, 15 and 20 days. Note regression of much of the mycelium not connected to a new resource, and thickening of connected cords (c). (d-g) Growth in 57 x 57cm soil trays, with four new wood resources (located half way along each microcosm side) added after 36 days in (e)-(g). (d) Control with no additional wood resources. Images were captured 78-85 days after adding the central wood inoculum. Note thickening of cords connecting inoculum with new resources (f and g), and thinning of other areas compared with 78 days control having no additional resources (e). Outgrowth from the newly colonized lower resource is evident from 78 days (Perspex blocks in the corners of trays were for support of other replicates in stacks). Proliferation of mycelium occurred along cords linking the central wood inoculum with new resources between 78 days (f) and 85 days (g). Digital images (a)-(c) from photographs taken by rory bolton. Digital images (d)-(g) Courtesy of Jon Wood.

biomass, with thickening of cords connecting resources, and regression of non-connective fine mycelium (Wood et al., 2006; Figure 3d-g). Moreover, sometimes renewed growth occurs elsewhere as ephemeral patches of highly branched fine hyphae or along cords interconnecting new and original resources (Wells et al., 1997; Wood et al., 2006; Figure 3g). The patches have been shown, using 32P orthophosphate, to be sites of nutrient uptake (Wells et al., 1977), and presumably developed to satisfy the increased demand for nutrients to produce mycelial biomass and enzymes during early stages of colonization and decomposition. Carbon and mineral nutrients are continually rerouted to sites of need in mycelial systems interconnecting a variety of resources in different states of decay (Wells et al, 1998).

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