Common mycelial networks: life-lines and radical addictions
Shared or common mycelial networks (CMNs; Fig. 1) linking the root systems of different plant individuals and species constitute a much studied and debated phenomenon. Although there seems little doubt that there is considerable potential for their existence, the general significance of these networks in plant and fungal ecology remains unknown. There is clear evidence that mycoheterotrophic plants and other plants that lack chlorophyll at early developmental stages (many orchids and Pteridophytes) depend on mycorrhizal fungi for carbon (C) and nutrients (Leake et al., 2004 and references therein). In autotrophic plants communities, the evidence is more equivocal. In a recent review on CMNs, Simard & Durall (2004) state that the strongest support for CMN effects is provided by the improved establishment, survival and growth of ectomycorrhizal (ECM) seedlings around existing ECM plants (Simard & Durall, 2004). However, the results from field studies on seedling establishment in such situations are often confounded by the de novo formation of mycorrhizas from spores. In this issue (pp. 169–178), Kazuhide Nara effectively circumvents this complication by capitalising on the harsh environment of the volcanic desert on the south-east slope of Mount Fuji, where spore inoculum is minimal (see Nara et al., 2003). In an elegant experiment, Nara transplanted laboratory generated nurse plant/seedling systems, inoculated with one of 11 ECM species, to the field site and examined colonisation, growth, and N and P uptake by the seedlings after 4 months. The study is notable because it demonstrates that, in general, colonisation by the fungi increased the size and N and P contents of the seedlings. In addition, Nara used ecologically relevant fungi, in other words the dominant local ECM species, many of which are considered intractable in such studies.
An extensive mycelial network formed by the ectomycorrhizal fungus Piloderma fallax on Scots pine (Pinus sylvestris).
‘One unanswered question, which has significant consequences for these research areas, is whether increasing diversity in fungal communities results in increased specialisation towards a single host’
Benefits of CMNs to establishing seedlings
Improved establishment of seedlings of ECM plants in close proximity to existing plants of the same (Matsuda & Hijii, 2004) and different (Horton et al., 1999) species is a commonly observed phenomenon. Studies that have compared the ECM communities on the root systems of seedlings and nearby plants have found a considerable overlap in species composition, particularly of ECM species that produce mycorrhizas of the long-distance exploration type (sensu Agerer, 2001). This group of fungi are considered to have high C maintenance costs that cannot be readily met by seedlings (Gibson & Deacon, 1990). The presence of these ‘high cost’ ECM fungi enhances the species richness of ECM communities on seedlings connected to CMNs compared with seedlings establishing in the same environment but without contact to neighbouring plants (Simard et al., 1997b). The increased abundance of these species on seedlings connected to CMNs has been interpreted as an indication that the costs to the seedling of supporting ECM fungi are offset by the larger nurse plant (Simard & Durall, 2004). This compensation could involve utilisation of nurse-plant-derived C by the mycorrhizal fungi during nutrient acquisition for the seedling or the transfer of C from the nurse plant to the seedling via the CMN (Simard et al., 1997a). The ecological significance of C transferred by the latter mechanism under field situations remains contentious (Fitter et al., 1999). In addition to the potential C benefits, the nutrient pool contained within and taken up by the existing ECM mycelia would also be available to the seedling, leading to improved growth.
However, establishing connections to a CMN is not always beneficial to seedlings, at least in the short term. Nara (this issue) and others (e.g. Kytoviita et al., 2003) have found that some fungi do not favour the growth of seedlings, but instead seem to supply the larger plant with nutrients preferentially. This has been interpreted as the fungus investing most resources in C acquisition from the largest C supplier. A parallel situation was observed in mature forests, where the ectomycorrhizal fungi gained most of their C from the largest overstorey trees (Högberg et al., 1999). However, it may be unnecessary to invoke preferential allocation of nutrients to the larger nurse plant in order to explain the negative impact of Laccaria amethystina on seedling growth observed by Nara. In both laboratory and field studies, where seedlings have been inoculated with Laccaria spp., positive, neutral and negative growth responses have been recorded (Kropp & Mueller, 1999). The outcome of any plant–fungus combination appears to be very context-dependent, particularly in relation to substrate nutrient content. The lack of a growth response by the seedlings inoculated with L. amethystina in the short term should not detract from the potential benefits of being colonised by ECM fungi in the long run.
… and the effects of mycorrhizal colonisation per se?
The study by Nara, like a number of other studies on the benefits to seedlings of CMNs, utilised nonmycorrhizal nurse plants and seedlings as control plants. It may therefore be difficult to differentiate between the influence of the network connection and that of ECM colonisation per se. This could be achieved by having seedlings colonised by the same ECM fungi as the nurse plant but having no mycelial connections with the nurse plant. Differences between seedlings connected to the CMN and those not connected would then indicate the influence of the network. Simard & Durall (2004) actually state that, despite numerous studies on seedling establishment, no transfer of nutrients or C from nurse plants to seedlings has been demonstrated and that ‘there is more evidence that the benefits arise simply from increased mycorrhization, which may or may not require CMN formation’. However, it is clear that, in the harsh conditions of the field site used by Nara, the establishment of mycorrhizal seedlings outside the influence of a CMN is an extremely rare occurrence.
Common mycelial networks and diversity and function relationships
The study of CMNs in species-rich plant and mycorrhizal fungal communities is very relevant to the examination of relationships between diversity and function in the same communities (van der Heijden et al., 1998; Jonsson et al., 2001). The formation of CMNs and the transfer of nutrients and C coupled with differential effects of plant–fungus combinations could provide a pathway and mechanisms by which increased fungal diversity supports greater plant diversity (Read, 1998). However, one unanswered question, which has significant consequences for both research areas, is whether increasing diversity in fungal communities results in increased specialisation towards a single host. This could, on the one hand, result in decreased potential for the formation of CMNs and, on the other, increase competition between hosts.
Stability, integrity and longevity of common mycelial networks
Fitter et al. (1999) noted that the great majority of the work on CMNs has focused on the benefits and consequences for the above-ground plant community. In the intervening period, the situation has not changed. Many aspects of the ecology of mycorrhizal fungal have largely been ignored when considering the significance of CMNs. Many studies refer to CMNs as though they are stable, long-term structures, yet we know that the extraradical mycelia of mycorrhizas are highly dynamic structures, which may turn over rapidly (Staddon et al., 2003; Leake et al., 2004). Considerable significance is also placed upon the size and continuity of ECM fungal genets in contributing to the potential for large CMNs. However, a comparison between saprotrophic forest floor fungi and ECM fungi may be illuminating in this respect. Many saprotrophic fungi form conspicuous fairy rings, in which fruit bodies are arranged in a circle often many metres in diameter. Where these rings are not related to zones of enhanced litter fall (Frankland, 1998), they represent the radial growth of a mycelium from a central point of origin. The fungi grow out as a mycelia front with the mycelium decaying behind the advancing front. The position of the front is indicated by the position of the fruit bodies. Similar structures are not uncommonly produced by ECM fungi and there is no a priori reason to assume that the integrity of the mycelium is any greater than that of the saprotrophic fungi. Genet size determined by fruit body appearance may therefore give a better indication of how much forest floor a mycelium has grown through, rather than the actual size of the genet. Finally, little attention has been given to the role of fungivory in disrupting the integrity of CMNs. Because fungi form the basis for many soil food webs, it is likely that grazing is a major factor determining the continuity of CMNs. Evidence for the effects of fungivory was recently found by Johnson et al. (2005), who demonstrated that the presence of Collembola disrupted the flow of C through the mycelia of arbuscular mycorrhizal fungi in unimproved grassland.
Life-lines and radical addictions
Seedlings establishing in the vicinity of plants supporting an appropriate mycorrhizal mycelium may become colonised and flourish as a consequence. One may ask the question: what benefits accrued to the fungi in colonising a small, struggling host? At least in the short term, benefits may be limited. However, a more relevant question might be: do mycorrhizal fungi have any option but to colonise susceptible roots?
