Deep thoughts on ectomycorrhizal fungal communities
Three papers in this issue of New Phytologist deal with the vertical distribution of ectomycorrhizal fungi in soils. Anderson et al. (pp. 1423–1430) analyze an earlier dataset (Genney et al., 2006) to explore the fine-scale distribution and diversity of ectomycorrhizal fungi across vertical soil profiles, Hobbie et al. (pp. 1431–1439) present an application of isotope techniques to trace the uptake of nutrients at different depths by ectomycorrhizal hyphae, and Pickles & Pither (pp. 1101–1105) note the failure of most research to sample the vast majority of the soil profile. The topic of vertical distribution of fungi in soil profiles is now a familiar one in mycorrhizal ecology, with > 10 yr of studies showing vertical niche partitioning of ectomycorrhizal fungi on roots (Taylor & Bruns, 1999), as fungal hyphae (Dickie et al., 2002), or both (Genney et al., 2006). Other studies have integrated analyses of the vertical distributions of saprotrophic and ericoid mycorrhizal fungi in the same profiles (Lindahl et al., 2006). The brief history of ectomycorrhizal fungal vertical distribution studies is a product of the development of molecular techniques, particularly relatively high-replication methods.
‘… new, more ambitious, theoretical frameworks must be developed, to understand the physiological mechanisms driving vertical niche differentiation, to expand from studies of single sites to find regional and global patterns …’
The initial goal in studying vertical distributions of ectomycorrhizal fungi was to test the hypothesis that niche partitioning along vertical soil profiles is a mechanism that contributes to fungal diversity (Bruns, 1995). Anderson et al.'s contribution adds to the evidence that vertical partitioning occurs, with distinct fungal communities in litter and deeper horizons. Nonetheless, Anderson et al. also found 9–11 species of ectomycorrhizal fungi even within small (8 cm3) cubes, suggesting that mechanisms other than vertical niche partitioning must contribute to fungal diversity. The specific mechanisms responsible for such fine-scale diversity are not clear, but careful observations of this kind are essential to understanding controls on diversity. Nevertheless, studies that simply re-test the hypothesis that ectomycorrhizal fungi show vertical niche partitioning are unlikely to significantly advance the field at this point. Rather, we suggest that new, more ambitious, theoretical frameworks must be developed, to understand the physiological mechanisms driving vertical niche differentiation, to expand from studies of single sites to find regional and global patterns, and to understand the implications of vertical stratification of fungal communities for ecosystem function.
Virtually all studies of fungal communities across vertical profiles have focused on single research sites, often single host-species plantations at a single point in time. A critical question in any ecological study must be whether the results can be generalized to other situations, sites, and regions. Hobbie et al. make an attempt to summarize patterns in fungal genera vertical distributions across 10 studies. The results do not suggest clear patterns. At a broader scale, the high frequency of ectomycorrhizal taxa in surface horizons in Anderson et al. contradicts other reports (Lindahl et al., 2006). Despite these inconsistencies, further cross-study comparisons should be attempted, particularly if differences in soil horizon nomenclature across studies can be resolved. Studies that directly contrast different ecosystems are of particular value (McGuire et al., 2013), although achieving true statistical replication remains a challenge.
Another approach may be to seek functional traits as a mechanism for integration (Koide et al., 2013). Classifying fungal species into broad functional groups both reduces complexity of highly diverse fungal communities and allows comparison of communities that may not share any individual species. The results of Hobbie et al. suggest, for example, that hydrophobicity may be one trait that influences success in various soil horizons. The role of changing root density at varying depth in structuring fungal communities has not been examined, but is also likely linked to fungal functional traits (Peay et al., 2012).
Transitioning from phenomenological to mechanistic studies
The extent to which consistent patterns of community structure fail to emerge across habitats suggests that a taxon-based approach to community ecology is difficult at best. That is why, in fact, some ecologists have complained of ‘too much contingency’ among disparate communities (Lawton, 1999). Another approach appears to be warranted. Early studies of the distributions of plants documented, among other things, the stratification of plant communities along elevational gradients. Few general principles were gleaned from such studies until researchers related plant traits to the characteristics of the habitat. Studies of vertical niche differentiation of ectomycorrhizal fungi have so far been largely phenomenological. We suggest that progress in understanding the maintenance of ectomycorrhizal fungal diversity is likely to require more attention to the relationship between fungal traits and habitat. Vertical stratification of fungal communities across soil profiles has a high potential to greatly increase our understanding given that vertical soil profiles represent strong gradients in numerous physical and chemical properties. Many factors vary with soil depth including the age, chemical composition and physical properties of soil organic matter, nutrient availability, O2 and CO2 concentrations, temperature, and moisture. Diurnal and seasonal variability of microclimate are likely to be much higher in surface horizons compared with deeper soil layers. Finally, plant root identity and density may vary with depth.
Competition is an important factor structuring fungal communities (Koide et al., 2005) and may result in a species' fundamental niche (where they potentially can occur in time and space) differing from its realized niche (where they do occur). But competitive interactions are famously context-dependent due to different species reactions to the same set of conditions. Thus, as environmental conditions change, competitive superiority shifts from one species to the next and communities of distinct structure become established. Further, historically contingent events, such as the order of species arrival, can also be an important determinant of competitive outcomes (Dickie et al., 2012). These community interactions present a challenge in understanding vertical niche differentiation, as they suggest that patterns may be observable but not predictable. Rather than feeling that the study of community ecology is largely hopeless because of this context-dependence, context dependence is, itself, the key to the emergence of general principles. Instead of focusing on taxa, which vary from community to community, we advocate a focus on traits that influence species interactions and how these interactions are influenced by environmental heterogeneity. While this approach may not be recognizable as traditional community ecology, we suggest it is more likely to produce general principles of community structuring.
Traits also influence ecosystem functioning (Koide et al., 2013; Hobbie et al.). Relatively little has been known of how vertical stratification of ectomycorrhizal fungi might influence ecosystem function. The study of Hobbie et al. suggests important differences in nitrogen (N) acquisition, with different fungal genera specializing on different N sources and different soil layers. What role fungal communities deep in the soil profile might play in plant and ecosystem responses also remains unclear (Pickles & Pither).
One of the most important features of filamentous fungi in soils is that fungal hyphae and rhizomorphs can bridge across different soil substrates and vertical layers, potentially using resources from one location to drive decomposition processes in another. Translocation of soil nutrients into decomposing wood by fungi is known to be an important process in decay of high carbon substrates (Dickie et al., 2012). Mycorrhizal fungal hyphae can occur across multiple soil layers, in some cases occurring as hyphae in locations distinct from where they occur on roots (Genney et al., 2006). This suggests a strong potential for vertical translocation of resources, but implications for soil nutrient cycling remain unexplored. Indeed, most of the focus of vertical profile studies to date has been on finding fungal species that are restricted in vertical distribution. From the perspective of resource translocation, it would make sense to shift the focus to species found across multiple layers, particularly those with extensive rhizomorphs and hyphal development.
The rise of molecular techniques has led to a host of excellent phenomenological studies of fungal communities that have tested the hypothesis that the maintenance of diversity is partly due to vertical stratification of fungal species in the soil profile. We suggest, now, that attention to new theoretical frameworks will lead to the development of more general principles fundamental to the organization of communities. Prominent among these new frameworks should be trait-based approaches, including a better understanding of phylogenetic constraints of fungal traits. There should be an attempt to integrate these trait-based approaches with a better understanding of the interplay of ruderal, stress-tolerant, and competitive factors down vertical profiles. Vertical profiles also have great potential to understand historically contingent factors in fungal community assembly and how these are influenced by stress and resource gradients. It would also be fascinating to apply ecological network theory to vertical profiles (Chagnon et al., 2012), particularly in terms of how vertically stratified ecological networks with partially overlapping membership interact. Finally, vertical niche differentiation also implies niche complementarity, the effects of which on ecosystem nutrient cycles remain largely unexplored. These are only a few examples, but illustrate the potential to use fungal communities in vertical soil profiles not just to apply ecological theory, but also to lead the development and testing of new theoretical frameworks in ecology.