Not every fungus is everywhere: scaling to the biogeography of fungal–plant interactions across roots, shoots and ecosystems
Article first published online: 9 FEB 2010
© The Authors (2010). Journal compilation © New Phytologist (2010)
Volume 185, Issue 4, pages 878–882, March 2010
How to Cite
Peay, K. G., Bidartondo, M. I. and Elizabeth Arnold, A. (2010), Not every fungus is everywhere: scaling to the biogeography of fungal–plant interactions across roots, shoots and ecosystems. New Phytologist, 185: 878–882. doi: 10.1111/j.1469-8137.2009.03158.x
- Issue published online: 9 FEB 2010
- Article first published online: 9 FEB 2010
Early natural historians viewed the distributions of fungi as independent of ecology, and instead akin to spontaneous generation: if conditions are right, the appropriate fungi will appear (de Candolle, 1820). Accordingly, Miles Joseph Berkeley (1863), the founder of British mycology, writes to Darwin, ‘Indeed were not Fungi so much the creatures of peculiar atmospheric conditions, there would seem to be no limit to the diffusion of their species.’ Such a perspective captures a view that characterized the early literature in mycology: fungi may appear to have limited geographical distributions, but dispersal per se plays no role in determining such distributions. Nearly a century later, Bisby (1943) recognized endemism in fungi but remained convinced that, ‘distribution of hosts and substrata primarily controls distribution of fungi’. Whereas appreciation of spatial and historical patterns of biodiversity led Darwin and Wallace to the theory of evolution by natural selection, the perception that fungi are relatively free from dispersal barriers remained influential well into the 20th century (e.g. Bisby, 1943; Raper et al., 1958).
This assumption has been challenged by recent molecular studies of historical biogeography, ecology and population genetics of fungi (Taylor et al., 2006; Lumbsch et al., 2008). Such studies show that although some fungi are capable of long-distance dispersal (Moncalvo & Buchanan, 2008), the distributions of most reflect the same major dispersal barriers (e.g. oceans and mountains) that drive vicariance events in other organisms (James et al., 1999; Matheny et al., 2009). At first glance the dispersal and distribution of fungi may seem like a topic of interest only in an academic sense. However, broad-scale distributions of fungal pathogens, saprotrophs and mutualists influence key ecosystem properties (Fig. 1), which are currently under pressure from anthropogenic change.
The ecological and historical determinants of fungal distributions – particularly those of symbiotic fungi – were a topic of discussion at a special symposium on the phylogenetic and functional patterns of host plants and their associated fungi, as well as several other sessions, at the Botanical and Mycological Societies of America meeting at Snowbird, Utah, in July 2009. Speakers addressed patterns of fungal distributions at scales ranging from experimental gardens to continents, and at levels of biological organization from genotypes to phyla.
Two talks provided ecological evidence that dispersal limitation should be prevalent among fungi: T. E. Galante (SUNY College of Environmental Science and Forestry, USA) and J. L. Stolze-Rybczynski (Miami University, FL, USA) presented statistical and biomechanical models, respectively, based on direct measurements of basidiospore dispersal from fungal reproductive structures, highlighting how structural differences, such as mushroom height, spore shape and size of Buller’s drop, determine dispersal distances. These talks also showed that most spores travel only very short distances from their point of origin – for example, Galante found that 95% of the spores observed fell within 45 cm of the mushroom from which they originated – and suggest that dispersal limitation may occur even at small to moderate spatial scales. At the community level, differences between species in dispersal strategies can explain patterns of fungal community assembly at landscape scales (Nara, 2009), and isolation and dispersal limitation can lead to significant changes in the species richness and colonization intensity experienced by mycorrhizal host plants (Dickie & Reich, 2005).
At larger spatial and temporal scales, the interplay among dispersal limitation, biogeographical history and adaptive evolution have generated an array of unique fungal assemblages, many of which are just beginning to be characterized by morphological or molecular means. Talks by T. D. Fulgenizi (Humboldt State University, CA, USA) and K. G. Peay (University of California, Berkeley, USA) both described unique ectomycorrhizal communities from the major tropical rainforests of the Amazon and Borneo, respectively. Strong latitudinal changes in fungal community structure were demonstrated for foliar endophytes by A. E. Arnold (University of Arizona, USA), who highlighted the interplay of species diversity and phylogenetic diversity from tropical to arctic environments. A. S. Amend (University of California, Berkeley, USA), presenting a 454 pyrosequencing characterization of indoor environments from every continent, found greater phylogenetic similarity of fungal communities sampled from similar latitudes.
Such latitudinal and biome-level differences in the abundance of particular species, lineages and functional groups are probably linked with ecosystem processes and plant community structure at large spatial scales. For example, the increasing prevalence of ectomycorrhizal symbioses vs arbuscular mycorrhizal symbioses from low to high latitudes and (within tropical forests) from the Amazon to southeast Asia (Read, 1991), probably affects regional rates of carbon and nitrogen cycling. Still, relatively little is known about how mycorrhizal type and diversity interact with large-scale soil processes in most of the world.
Understanding determinants of fungal community structure across multiple spatial and temporal scales is particularly important given that fungal communities in a variety of ecosystems have been altered markedly by human activities (e.g. Arnolds, 1991; Lilleskov et al., 2002; Mummey & Rillig, 2006). Since the 1980s, compelling evidence has emerged of a decline in fruiting of forest fungi in northern and central European countries (Arnolds, 1991) and modelling of bioclimatic envelopes predicts changing distributions and possible extinction for some British lichen (Ellis et al., 2007). Some pathogenic and mutualistic fungi are expanding their geographical ranges (James et al., 2009; Pringle et al., 2009), and the phenology of fungi in some forests has changed markedly over the last 50 years, in many cases yielding not one annual fruiting season, but two (Gange et al., 2007; Kauserud et al., 2008). Despite the steady increase in mycological studies from tropical regions, many tropical fungal communities remain unstudied, and the continuing decline in forested areas may lead to a large loss of still uncharacterized biodiversity (Arnold & Lutzoni, 2007).
Moreover, evidence is accumulating that fungal responses to anthropogenic change may have far-reaching consequences. For example, complex changes in rates of fungal decomposition of organic matter have been observed in the context of climate alteration (Lensing & Wise, 2006; Allison & Treseder, 2008). A number of studies indicate that fungal species composition, root and/or shoot biomass, rates of herbivory and susceptibility to pathogens, and rates of nitrogen acquisition and cycling efficiency, respond to environmental changes such as elevated CO2 (Hunt et al., 2005; Chen et al., 2007; Cudlin et al., 2007; Clark et al., 2009). In turn, these processes will shape large-scale distributions of plants and animals. For example, high specificity has been demonstrated for a number of mycoheterotrophic plants (Bidartondo & Bruns, 2002; Bidartondo, 2005), and experimental tests have shown that the distributions of these plants (many of which are rare or endangered) are constrained by distributions of one or a few species of ectomycorrhizal fungi (Bidartondo & Bruns, 2005; Bidartondo & Read, 2008). Thus, the migration of these plants and others in response to climate change may be constrained by the distribution or co-migration of fungal symbionts. Given that many fungi, as well as plants, differ in their dispersal abilities, it is likely that individual species will differ in the rate of migration in response to global change, which will inevitably lead to the creation of novel communities and interactions (Davis, 1986; Keith et al., 2009). These may lead to temporary disequilibria (i.e. where species are not present in otherwise suitable environments) or to the formation of stable communities of plants and fungi much different from those we see today.
Despite compelling evidence that fungal communities are changing, and that these changes have potential ramifications for key ecosystem properties, we still have little ability to predict or generalize at the spatial and temporal scales necessary to inform sound experimental design for ecology and ecosystem science. This is primarily because we have accurate distributional data for only a small fraction of fungal species and lack the ability to extrapolate functional studies from the laboratory to the ecosystem and from single species to communities. Fortunately, our ability to map large-scale distributions is greater than ever before. From a methodological standpoint, fungal community ecologists have harnessed the power of molecular ecology to permit the following: more holistic and quantitative measures of community structure that take into account uncultured fungi and fungi that fruit infrequently; and rapid analyses at levels of biological organization ranging from genotype diversity to phylogenetic structure (Arnold et al., 2007; Peay et al., 2008). Concurrently, communities of researchers are rallying to enhance the quality and content of databases to accommodate and curate such data (Bruns et al., 2008), and ecologists are calling for use of the baseline distribution data for mycorrhizal fungi, ranging from regional to continental scales and encompassing entire ecosystems (Lilleskov & Parrent, 2007). These efforts will use increasingly powerful next-generation sequencing methods to open up the ‘black box’ of fungal ecology and to identify and focus on species, lineages or functional groups that are key to providing ecosystem services.
Such a change in perspective will also require scaling from the traits of individual fungi and their individual plant partners, across multiple scales, as well as a clear research framework that identifies links between research efforts and gaps in our knowledge (Fig. 1). With this framework in mind, we propose a series of fundamental questions that we hope will motivate and guide a global fungal biodiversity assessment.
- 1What are the large-scale spatial distributional ranges for fungal species and to what extent are these determined by abiotic and biotic environmental variables vs historical patterns of dispersal and migration?
- 2Can changes in fungal distributions driven by environmental change (i.e. climate shifts, habitat loss and changing host/substrate distribution) be predicted for groups with distinct geographical distributions, and how will this affect the future distribution of symbiotic plants or animals?
- 3Are there ecologically dominant fungi in particular ecosystems? What criteria should we use to identify them? How do they contribute directly to ecosystem processes (such as carbon sequestration) and how much do they indirectly affect ecosystem processes (such as net primary productivity)?
- 4If there are widespread, dominant fungal species or lineages across biomes and environmental gradients, to what extent are they functionally and genetically homogeneous?
- 5Can data from traditional, small-scale studies be extrapolated directly to entire ecosystems, or are large-scale pilot studies required to account for interactions and nonadditive effects in the scaling-up process?
- 6At what spatial scale can we detect key changes in fungal community structure that are related to essential ecosystem functions or responses to perturbations such as climate change? In other words – which scale is appropriate for detecting community responses to disturbance and at which scale do these changes in the fungal community structure translate to changes in ecosystem processes or services?
- 7Where are the geographical hot spots of fungal biodiversity and why?
The increasing interest by the broader ecological community in fungi, the existence of long-term plot networks and the increasing availability of next-generation sequencing technology make a global assessment of fungal diversity a realistically achievable goal now more than ever. We hope that these questions will help to motivate and guide such an effort and believe that the data generated will answer fundamental questions about the distribution and drivers of fungal diversity, provide baseline data for the incorporation of fungi into other ecological study programmes and help to meet the future challenges of global change.
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