Disentangling global soil fungal diversity David A. Wardle and Björn D. Lindahl Science 346, 1052 (2014); DOI: 10.1126/science.aaa1185

If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of November 27, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/346/6213/1052.full.html A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/346/6213/1052.full.html#related This article cites 10 articles, 4 of which can be accessed free: http://www.sciencemag.org/content/346/6213/1052.full.html#ref-list-1

Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.

Downloaded from www.sciencemag.org on November 27, 2014

This copy is for your personal, non-commercial use only.

INSIGHTS

Climate adaptation via female education p. 1061 Restoring trust in the financial services sector

p. 1065

PERSPECTIVES ECOLOGY

Disentangling global soil fungal diversity A worldwide sampling effort reveals the global drivers of soil fungal biodiversity By David A. Wardle1 and Björn D. Lindahl2

E

PHOTOS: K. E. CLEMMENSEN/SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCE

cologists have long sought to understand global patterns of biological diversity (1, 2). Most work on this topic has focused on visible aboveground organisms that can easily be counted, such as birds, butterflies, reptiles, and plants. In contrast, knowledge of the global ecology of most belowground organism groups is limited because of their microscopic size and hidden existence. Rapid advances in molecular techniques for analyzing soil communities are now offering unprecedented opportunities for understanding soil biodiversity (3, 4). On page 1078 of this issue, Tedersoo et al. (5) use pyrosequencing of soil samples to provide a comprehensive global study of a major group of soil organisms: soil fungi. Soil ecologists have long been aware of the need to test whether global diversity patterns established for aboveground biota also apply Fungal diversity. Tedersoo et al. (5) show that the ratio of fungal to plant diversity rises with increasing distance from the equator. Consistent with this finding, highlatitude boreal forests support few tree and understory plant species, yet fungal diversity is high, as shown in the diverse range of fruiting bodies (including those of ectomycorrhizal, saprotrophic, and pathogenic fungi) found within a ~150-m radius in Lunsen forest near Uppsala, central Sweden.

1052

sciencemag.org SCIENCE

28 NOVEMBER 2014 • VOL 346 ISSUE 6213

Published by AAAS

to soil biota (6, 7). However, attempts to understand the global ecology of soil biota have typically either synthesized data from different and often disparate studies, or included too few independent sites to usefully separate the effects of large-scale drivers such as geography, latitude, and macroclimate from local variation in soil properties. Tedersoo et al. overcome this problem by characterizing fungal communities in soil samples from 365 separate locations worldwide (including all continents except Antarctica), all of which were sampled, processed, and analyzed in exactly the same way.

nounced patterns in the natural world, at least above ground (9). In line with this, total fungal richness increases toward the equator, but major groups of fungi defy this pattern. For example, ectomycorrhizal fungal richness is greatest at mid- to high northern latitudes (coinciding with temperate and boreal forest), and richness within several ascomycete groups (notably the Leotiomycetes, which include fungi that form mycorrhizal associations with ericoid dwarf shrubs) increases toward the poles. Globally, fungal richness does not decline as sharply as plant species diversity with increasing latitude; the result

PHOTO: K. E. CLEMMENSEN/SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCE

Hidden diversity. The highly diverse fungal fruiting bodies shown in the previous figure were photographed during a brief walk through this Swedish forest, which supports low plant diversity.

The results indicate that at the global scale, mean annual precipitation is the strongest driver of the richness of fungal operational taxonomic units (“richness”). However, soil properties, notably soil pH and calcium concentration, also had important positive effects. Soil fungi are generally viewed as acidophiles (relative to bacteria), but the current results suggest that they have a wider range of tolerance, rather than a preference, for acidic conditions (8). Tedersoo et al. found that the relative richness of the main functional groups— ectomycorrhizal fungi, saprotrophs, and pathogens—varies widely among Earth’s major biomes, consistent with these groups each being driven by a separate set of factors. Ectomycorrhizal fungal richness is most strongly related to the richness of host plant species and high soil pH; saprotroph richness is positively related to mean annual precipitation; and pathogen richness is negatively related to latitude but positively related to nitrogen availability. The decline of species richness with increasing latitude is one of the most pro1

Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden. 2 Department of Soil and Environment, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden. E-mail: [email protected]

is that the ratio of fungal to plant richness rises exponentially toward the poles. Fungi are thus a key component of total terrestrial biodiversity at high latitudes, with important implications for conservation (see the figures). Reliable estimates of this ratio are important for deriving global fungal diversity from measures of plant diversity (10). Tedersoo et al.’s analysis also highlights the roles of biogeography and evolutionary history in driving fungal communities within regions. First, fungal taxa at higher latitudes on average had larger geographic ranges than did those nearer the equator, pointing to higher fungal endemism in tropical regions. This is supportive of Rapoport’s rule, which predicts more restricted geographic ranges for higher-latitude taxa and has often been demonstrated for aboveground biota. Second, through analyses aimed at assessing shared fungal diversity among different biomes or regions, the authors could identify similarities in communities between Southern Hemisphere land masses, between Northern and Southern Hemisphere temperate regions, and between paleo- and neotropical regions. These biogeographic patterns can be explained in part through comigration with hosts over Pleistocene land bridges and in part through long-distance dispersal by spores.

SCIENCE sciencemag.org

The main functional groups of fungi drive many ecological processes, and questions therefore remain as to how the global variation in fungal communities characterized by Tedersoo et al. interacts with other ecosystem components. For example, saprotrophs and mycorrhizal fungi play opposite roles in soil organic matter formation (11, 12). Shifts in their relative dominance may therefore have major implications for net ecosystem carbon exchange and sequestration. Furthermore, vegetation and soil fungi are tightly linked via mycorrhizal symbiosis, pathogenic interactions, and nutrient release during decomposition. Shifts in the relative diversity of major fungal groups could thus potentially affect plant productivity and diversity (13). Moreover, soil fungi serve as food for many soil invertebrates. It remains to be shown whether the variation in fungal communities characterized by Tedersoo et al. is reflected in corresponding global patterns in soil nematodes, mites, and springtails. Global studies of the type performed by Tedersoo et al. are also helpful for better understanding how the belowground subsystem may respond to global environmental change. Improved knowledge about links between macroclimate and fungal communities will help to predict how global climate change is likely to affect the relative abundances of key fungal groups and thereby alter fungal-driven ecological processes. Further, because most of the soil fungal community remains undescribed, we are currently unable to assess with any reliability the extent to which subsets of this community are likely to be threatened or to be spread (and potentially become invasive) through human activity. Studies such as that by Tedersoo et al. that enable better characterization of the soil mycobiome may serve as benchmarks against which we can assess rearrangement of species assemblages caused by human activity. ■ REFERENCES

1. M. Huston, Biological Diversity: The Coexistence of Species on Changing Landscapes (Cambridge Univ. Press, Cambridge, 1994). 2. K. J. Gaston, T. M. Blackburn, Pattern and Process in Macroecology (Blackwell Science, Oxford, 2000). 3. N. Fierer et al., Science 342, 621 (2013). 4. J. M. Talbot et al., Proc. Natl. Acad. Sci. U.S.A. 111, 6341 (2014). 5. L. Tedersoo et al., Science 346, 1256688 (2014). 6. D. A. Wardle, Communities and Ecosystems: Linking the Aboveground and Belowground Components (Princeton Univ. Press, Princeton, NJ, 2002). 7. T. Decaëns, Glob. Ecol. Biogeogr. 19, 287 (2010). 8. J. Rousk et al., Soil Biol. Biochem. 42, 926 (2010). 9. P. H. Taylor, S. D. Gaines, Ecology 80, 2474 (1999). 10. D. L. Taylor et al., Ecol. Monogr. 84, 3 (2014). 11. K. E. Clemmensen et al., Science 339, 1615 (2013). 12. C. Averill, B. L. Turner, A. C. Finzi, Nature 505, 543 (2014). 13. W. H. Van der Putten et al., J. Ecol. 101, 265 (2013). 10.1126/science.aaa1185 28 NOVEMBER 2014 • VOL 346 ISSUE 6213

Published by AAAS

1053

Ecology. Disentangling global soil fungal diversity.

Ecology. Disentangling global soil fungal diversity. - PDF Download Free
1MB Sizes 6 Downloads 5 Views