Global patterns in endemicity and vulnerability of soil fungi

Abstract

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.

Keywords: biodiversity; biogeography; climate change; conservation priorities; global change vulnerability; global maps; mycorrhizal fungi; pathogens; saprotrophs.

FIGURE 1

Distribution of samples and fungal species across data sets. (a) Global sampling map, with different colours representing different data sets; (b) species distribution of fungi among data sets, with the proportion of unique and shared species indicated; (c) Krona chart indicating the taxonomic distribution of fungal species (interactive chart can be browsed at https://plutof.ut.ee/#/doi/10.15156/BIO/2483900); and (d) species richness and total read abundance of the top 10 most diverse fungal genera.

FIGURE 2

Distribution of 174 ecoregions used in endemicity analyses. Ecoregions excluded from the analyses due to the lack of data are indicated in grey. Their definition and relationship with Olson's ecological regions are given in Table S1.

FIGURE 3

Average endemicity of soil fungi across ecoregions (defined in Figure 2). The inset graph indicates that endemicity has a positive and U‐shaped relationship with mean annual air temperature, the best predictor of endemicity. Grey ecoregions were excluded because of insufficient data.

FIGURE 4

Endemicity patterns of fungi compared with plants and various vertebrate groups: (a) insularity effect and (b) latitudinal distribution. The analyses are based on world's ecoregions that differ for fungi compared with plants and animals (Kier et al., 2009). For all data sets, the mean maximum distance of all species was available and therefore taken as a measure of relative endemicity. For comparative purposes, these values were logarithm‐transformed, corrected for sequencing and sampling depth (only fungi) and z‐transformed. In (a) lines, boxes and error bars represent mean, SE and SD, respectively. In (b) the endemicity values were regressed against latitude using second‐order polynomial function; colours represent different organism groups as indicated in (a). For fungi, n = 156 and n = 28 for continent and island ecoregions, respectively; for other groups, n = 76 and n = 14 for continent and island ecoregions, respectively.

FIGURE 5

Vulnerability of fungi to global change drivers: (a) average vulnerability of all fungi to drought, heat and land cover change. The inset shows the near‐linear relationship of vulnerability to the air temperature of the warmest quarter. (b) Relative importance of predicted vulnerability of all fungi to drought, heat and land cover change as indicated by colour mixes. For example, the purple colour indicates high vulnerability to both heat and drought but low vulnerability to land cover change. (c) Relative importance of global change drivers for the predicted vulnerability of soil fungi and functional groups. Different letters indicate statistically significant (p < .001) differences among functional groups (a–e) and among global change drivers within functional groups (x–z). Mapping error estimates for panel (a) are given in Figure S4.

FIGURE 6

Conservation priority areas for all fungi (a) and their relationships with mean annual temperature (b) and Copernicus land cover types (c). In (b), black and red lines indicate best‐fitting linear and lowess functions, respectively. In (c), central lines and whiskers indicate mean and standard errors, respectively; letters above whiskers indicate statistically significant differences among land cover types.