The ties that bind

In most higher plants, symbiotic fungi are central to the process of nutrient capture from soil¹. Evidence from fossils of the earliest land plants², as well as molecular studies³, confirms that roots co-evolved with fungal partners to form structures known as mycorrhizas — literally, ‘fungus-roots’. These are almost universally distributed through present-day terrestrial plant communities, yet most researchers (deterred, one suspects, from experimental analysis of mycorrhizal function in natural communities by the complexity of these systems) have instead used excised roots or pot-grown plants to examine the relationships between partners in the symbiosis. Unfortunately, reductionist approaches cannot answer larger questions about the effect of symbiosis on interactions between the individual plants that form natural ecosystems.

The study of Simard et al.⁴ (page 579 of this issue) is important in this context. Not only does it address these complex questions in a field situation but, for the first time, it shows unequivocally that considerable amounts of carbon — the energy currency of all ecosystems — can flow through the hyphae of shared fungal symbionts from tree to tree, indeed, from species to species, in a temperate forest. Because forests cover much of the land surface in the Northern Hemisphere, where they provide the main sink for atmospheric CO₂, an understanding of these aspects of their carbon economy is essential.

Hyphae are the main structural elements of mycorrhizal fungi. They either penetrate the cells of the plant root to form an ‘endomycorrhiza’ or, as in most of the trees in the forest studied by Simard et al., they ensheath the root to produce an ‘ectomycorrhiza’. In the nutrient-impoverished conditions that prevail in forests, at least 90 per cent of the ‘feeding’ roots of the tree are colonized by ectomycorrhizal fungi. The result is that a layer of fungal tissue, the mantle, forms an interface between the root and the soil. From this mantle, individual hyphae (˜3 μm in diameter) or organized, root-like aggregates called rhizomorphs (˜20 μm diameter) grow outwards to intimately explore the soil (Fig. 1). Extension of this fungal mycelium into the soil depends on a supply of photosynthetically fixed carbon from the plant¹. Conversely, essential minerals (especially nitrogen and phosphorus) captured at some distance from the root by the foraging mycelium, are transferred in the reverse direction to the root¹.

Figure 1: The roots of up to 90 per cent of the trees in a forest can be colonized by many fungal species, the mycelia of which form ectomycorrhizal networks.

These networks, shown above linking two conifer species, provide channels for the transfer of nutrients. Simard et al.4 have now shown that considerable amounts of carbon can be transferred in either direction between trees through these networks.

Fundamentally important for the processes investigated by Simard et al. is the fact that most mycorrhizal fungi are catholic in their choice of host species⁵. As a result, the roots of trees such as the Douglas fir or birch can be colonized by many fungal species, the mycelia of which extend from tree to tree, providing linkages between them. The lack of specificity ensures that, in an undisturbed forest ecosystem, almost all of the trees — irrespective of their taxonomic affinities — are interconnected by a diverse population of mycelial systems. Groups of tree species joined together in this way have been recognized as functional guilds⁶.

Simard et al. provide a fascinating glimpse of one of the exchange processes facilitated by these underground connections. Using an ingenious approach in which young trees growing close to one another in the forest were simultaneously fed with either ¹⁴C- or ¹³C-labelled CO₂, they showed that net transfer of carbon occurred from birch to fir, both of which shared up to ten mutually compatible fungal symbionts. Moreover, no such transfer occurred between the species of the ectomycorrhizal guild and cedar, which was colonized by fungi of the endomycorrhizal type. Previous studies⁷ using ¹⁴CO₂ have shown that carbon transfer between plants occurs through the hyphae of compatible mycorrhizal fungi. But these studies could not confirm net flow, because transfer in the reverse direction was not quantified.

Perhaps of greatest ecological significance is the demonstration that when the fir was in the shade, there was a considerable increase in the amount of carbon that it received from the birch. Most forest trees spend the early part of their lives as seedlings in the gloom of the forest floor. If, as indicated by this work, the direction of flux is determined by the carbon status of the recipient, the carbon economy of this shaded understorey will be subsidized by fully illuminated overstorey plants, through pathways provided by their fungal symbionts. The extent to which this subsidy might contribute to the ability of young trees to survive in shaded environments should clearly now be examined, because persistence under, and recruitment into, the canopy determines the equilibrium of the forest community. Moreover, certain plants that live on the forest floor — notably in the family Monotropaceae — totally lack chlorophyll, so they receive all of their carbon from photosynthesizing trees through mycorrhizal connections¹. This illustrates the potential of these processes for sustaining receiver plants.

The observation that carbon is transferred between green plants will stimulate us to examine forest ecosystems from a fresh standpoint. It indicates that we should place less emphasis on competition between plants, and more on the distribution of resources within the community. If mycorrhizal colonization results in an equalization of resource availability, as suggested by this and a number of microcosm studies, it would be expected to reduce dominance of aggressive species, so promoting coexistence and greater biodiversity.

Since Clements⁸ introduced the concept of the community as a ‘superorganism’, ecologists have espoused the abstract idea that all components of stable ecosystems are interdependent. Simard et al.⁴ show the physical presence of interconnections between individuals in the forest ecosystem, and expose some of the likely consequences of their formation. The challenge now is to quantify further the contribution of these fungal linkages to the maintenance of biodiversity and stability in terrestrial ecosystems.