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    A predictive timeline of wildlife population collapse

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    Fine-resolution global maps of root biomass carbon colonized by arbuscular and ectomycorrhizal fungi

    To calculate total root biomass C colonized by AM and EcM fungi, we developed a workflow that combines multiple publicly available datasets to ultimately link fine root stocks to mycorrhizal colonization estimates (Fig. 1). These estimates were individually derived for 881 different spatial units that were constructed by combining 28 different ecoregions, 15 land cover types and six continents. In a given spatial unit, the relationship between the proportion of AM- and EcM-plants aboveground biomass and the proportion of AM- and EcM-associated root biomass depends on the prevalence of distinct growth forms. Therefore, to increase the accuracy of our estimates, calculations were made separately for woody and herbaceous vegetation and combined in the final step and subsequently mapped. Below we detail the specific methodologies we followed within the workflow and the main assumptions and uncertainties associated.Fig. 1Workflow used to create maps of mycorrhizal fine root biomass carbon. The workflow consists of two main steps: (1) Estimation of total fine root stock capable to form mycorrhizal associations with AM and EcM fungi and (2) estimation of the proportion of fine roots colonized by AM and EcM fungi.Full size imageDefinition of spatial unitsAs a basis for mapping mycorrhizal root abundances at a global scale, we defined spatial units based on a coarse division of Bailey’s ecoregions23 After removing regions of permanent ice and water bodies, we included 28 ecoregions defined according to differences in climatic regimes and elevation (deposited at Dryad-Table S1). A map of Bailey’s ecoregions was provided by the Oak Ridge National Laboratory Distributed Active Archive Center24 at 10 arcmin spatial resolution. Due to potential considerable differences in plant species identities, ecoregions that extended across multiple continents were split for each continent. The continent division was based upon the FAO Global Administrative Unit Layers (http://www.fao.org/geonetwork/srv/en/). Finally, each ecoregion-continent combination was further divided according to differences in land cover types using the 2015 Land Cover Initiative map developed by the European Space Agency at 300 m spatial resolution (https://www.esa-landcover-cci.org/). To ensure reliability, non-natural areas (croplands and urban areas), bare areas and water bodies were discarded (Table 1). In summary, a combination of 28 ecoregions, 15 land cover types and six continents were combined to define a total of 881 different spatial units (deposited at Dryad-Table S2). The use of ecoregion/land cover/continent combination provided a much greater resolution than using a traditional biome classification and allowed to account for human-driven transformations of vegetation, the latter based on the land cover data.Table 1 List of land cover categories within the ESA CCI Land Cover dataset, used to assemble maps of mycorrhizal root biomass.Full size tableMycorrhizal fine root stocksTotal root C stocksEstimation of the total root C stock in each of the spatial units was obtained from the harmonized belowground biomass C density maps of Spawn et al.20. These maps are based on continental-to-global scale remote sensing data of aboveground biomass C density and land cover-specific root-to-shoot relationships to generate matching belowground biomass C maps. This product is the best up-to-date estimation of live root stock available. For subsequent steps in our workflow, we distinguished woody and herbaceous belowground biomass C as provided by Spawn et al.20. As the tundra belowground biomass C map was provided without growth form distinction, it was assessed following a slightly different workflow (see Section 2.2.3 for more details). To match the resolution of other input maps in the workflow, all three belowground biomass C maps were scaled up from the original spatial resolution of 10-arc seconds (approximately 300 m at the equator) to 10 arc‐minutes resolution (approximately 18.5 km at the equator) using the mean location of the raster cells as aggregation criterion.As the root biomass C maps do not distinguish between fine and coarse roots and mycorrhizal fungi colonize only the fine fractions of the roots, we considered the fine root fraction to be 88,5% and 14,1% of the total root biomass for herbaceous and woody plants, respectively. These constants represent the mean value of coarse/fine root mass ratios of herbaceous and woody plants provided by the Fine-Root Ecology Database (FRED) (https://roots.ornl.gov/)25 (deposited at Dryad-Table S3). Due to the non-normality of coarse/fine root mass ratios, mean values were obtained from log-transformed data and then back-transformed for inclusion into the workflow.Finally, the belowground biomass C maps consider the whole root system, but mycorrhizal colonization occurs mainly in the upper 30 cm of the soil18. Therefore, we estimated the total fine root stocks in the upper 30 cm by applying the asymptotic equation of vertical root distribution developed by Gale & Grigal26:$$y=1-{beta }^{d}$$where y is the cumulative root fraction from the soil surface to depth d (cm), and β is the fitted coefficient of extension. β values of trees (β = 0.970), shrubs (β = 0.978) and herbs (β = 0.952) were obtained from Jackson et al.27. A mean value was then calculated for trees and shrubs to obtain a woody vegetation β value of 0.974. As a result, we estimated that 54.6% of the total live root of woody vegetation and 77.1% of herbaceous vegetation is stored in the upper 30 cm of the soil. In combination, this allowed deriving fine root C stocks in the upper 30 cm of woody and herbaceous vegetation.The proportion of root stocks colonized by AM and EcMThe proportion of root stock that forms associations with AM or EcM fungi was obtained from the global maps of aboveground biomass distribution of dominant mycorrhizal types published by Soudzilovskaia et al.14. These maps provide the relative abundance of EcM and AM plants based on information about the biomass of grass, shrub and tree vegetation at 10arcmin resolution. To match with belowground root woody plants biomass data, proportions of AM trees and shrubs underlying the maps of Soudzilovskaia et al.14 were summed up to obtain the proportion of AM woody vegetation. The same was done for EcM trees and shrubs.Our calculations are subjected to the main assumption that, within each growth form, the proportion of aboveground biomass associated with AM and EcM fungi reflects the proportional association of AM and EM fungi to belowground biomass. We tested whether root:shoot ratios were significantly different between AM and EcM woody plants (the number of EcM herbaceous plants is extremely small17). Genera were linked to growth form based on the TRY database (https://www.try-db.org/)19 and the mycorrhizal type association based on the FungalRoots database17. Subsequently, it was tested whether root:shoot ratios of genera from the TRY database (https://www.try-db.org/)19 were significantly different for AM vs EcM woody plants. No statistically significant differences (ANOVA-tests p-value = 0.595) were found (Fig. 2).Fig. 2Mean and standar error of root to shoot ratios of AM and EcM woody plant species.Full size imageEstimation of mycorrhizal fine root stocksWe calculated the total biomass C of fine roots that can potentially be colonized by AM or EcM fungi by multiplying the total woody and herbaceous fine root C biomass in the upper 30 cm of the soil by the proportion of AM and EcM of woody and herbaceous vegetation. In the case of tundra vegetation, fine root C stocks were multiplied by the relative abundance of AM and EcM vegetation without distinction of growth forms (for simplicity, this path was not included in Fig. 1, but can be seen in Fig. 3. As tundra vegetation consists mainly of herbs and small shrubs, the distinction between woody and herbaceous vegetation is not essential in this case.Fig. 3Workflow used to create mycorrhizal fine root biomass C maps specific for tundra areas.Full size imageFinally, we obtained the mean value of mycorrhiza growth form fine root C stocks in each of the defined spatial units. These resulted in six independent estimations: AM woody, AM herbaceous, EcM woody, EcM herbaceous, AM tundra and EcM tundra total fine root biomass C (Fig. 4).Fig. 4Fine root biomass stocks capable to form association with AM (a) and EcM (b) fungi for woody, herbaceous and tundra vegetation. Final AM and EcM stock result from the sum of the growth form individual maps. There were no records of fine root biomass of EcM herbaceous vegetation.Full size imageThe intensity of root colonization by mycorrhizal fungiColonization databaseThe FungalRoot database is the largest up-to-date compilation of intensity of root colonization data, providing 36303 species observations for 14870 plant species. Colonization data was filtered to remove occurrences from non-natural conditions (i.e., from plantations, nurseries, greenhouses, pots, etc.) and data collected outside growing seasons. Records without explicit information about habitat naturalness and growing season were maintained as colonization intensity is generally recorded in the growing season of natural habitats. When the intensity of colonization occurrences was expressed in categorical levels, they were converted to percentages following the transformation methods stated in the original publications. Finally, plant species were distinguished between woody and herbaceous species using the publicly available data from TRY (https://www.trydb.org/)19. As a result, 9905 AM colonization observations of 4494 species and 521 EcM colonization observations of 201 species were used for the final calculations (Fig. 5).Fig. 5Number of AM (a) and EcM (b) herbaceous and woody plant species and total observations obtained from FungalRoot database.Full size imageThe use of the mean of mycorrhizal colonization intensity per plant species is based on two main assumptions:

    1)

    The intensity of root colonization is a plant trait: It is known that the intensity of mycorrhizal infections of a given plant species varies under different climatic and soil conditions28,29, plant age30 and the identity of colonizing fungal species31. However, Soudzilovskaia et al.9 showed that under natural growth conditions the intraspecific variation of root mycorrhizal colonization is lower than interspecific variation, and is within the range of variations in other plant eco-physiological traits. Moreover, recent literature reported a positive correlation between root morphological traits and mycorrhizal colonization, with a strong phylogenetic signature of these correlations32,33. These findings provide support for the use of mycorrhizal root colonization of plants grown in natural conditions as a species-specific trait.

    2)

    The percentage of root length or root tips colonized can be translated to the percentage of biomass colonized: intensity of root colonization is generally expressed as the proportion of root length colonized by AM fungi or proportion of root tips colonized by EcM fungi (as EcM infection is restricted to fine root tips). Coupling this data with total root biomass C stocks requires assuming that the proportion of root length or proportion of root tips colonized is equivalent to the proportion of root biomass colonized. While for AM colonization this equivalence can be straightforward, EcM colonization can be more problematic as the number of root tips varies between tree species. However, given that root tips represent the terminal ends of a root network34, the proportion of root tips colonized by EcM fungi can be seen as a measurement of mycorrhizal infection of the root system and translated to biomass independently of the number of root tips of each individual. Yet, it is important to stress that estimations of fine root biomass colonized by AM and EcM as provided in this paper might not be directly comparable.

    sPlot databaseThe sPlotOpen database21 holds information about the relative abundance of vascular plant species in 95104 different vegetation plots spanning 114 countries. In addition, sPlotOpen provides three partially overlapping resampled subset of 50000 plots each that has been geographically and environmentally balanced to cover the highest plant species variability while avoiding rare communities. From these three available subsets, we selected the one that maximizes the number of spatial units that have at least one vegetation plot. We further checked if any empty spatial unit could be filled by including sPlot data from other resampling subsets.Plant species in the selected subset were classified as AM and EcM according to genus-based mycorrhizal types assignments, provided in the FungalRoot database17. Plant species that could not be assigned to any mycorrhizal type were excluded. Facultative AM species were not distinguished from obligated AM species, and all were considered AM species. The relative abundance of species with dual colonization was treated as 50% AM and 50% ECM. Plant species were further classified into woody and herbaceous species using the TRY database.Estimation of the intensity of mycorrhizal colonizationThe percentage of AM and EcM root biomass colonized per plant species was spatially upscaled by inferring the relative abundance of AM and EcM plant species in each plot. For each mycorrhizal-growth form and each vegetation plot, the relative abundance of plant species was determined to include only the plant species for which information on the intensity of root colonization was available. Then, a weighted mean intensity of colonization per mycorrhizal-growth form was calculated according to the relative abundance of the species featuring that mycorrhizal-growth form in the vegetation plot. Lastly, the final intensity of colonization per spatial unit was calculated by taking the mean value of colonization across all plots within that spatial unit. These calculations are based on 38127 vegetation plots that hold colonization information, spanning 384 spatial units.The use of vegetation plots as the main entity to estimate the relative abundance of AM and EcM plant species in each spatial unit assumes that the plant species occurrences and their relative abundances in the selected plots are representative of the total spatial unit. This is likely to be true for spatial units that are represented by a high number of plots. However, in those spatial units where the number of plots is low, certain vegetation types or plant species may be misrepresented. We addressed this issue in our uncertainty analysis. Details are provided in the Quality index maps section.Final calculation and maps assemblyThe fraction of total fine root C stocks that is colonized by AM and EcM fungi was estimated by multiplying fine root C stocks by the mean root colonization intensity in each spatial unit. This calculation was made separately for tundra, woody and herbaceous vegetation.To generate raster maps based on the resulting AM and EcM fine root biomass C data, we first created a 10 arcmin raster map of the spatial units. To do this, we overlaid the raster map of Bailey ecoregions (10 arcmin resolution)24, the raster of ESA CCI land cover data at 300 m resolution aggregated to 10 arcmin using a nearest neighbour approach (https://www.esa-landcover-cci.org/) and the FAO polygon map of continents (http://www.fao.org/geonetwork/srv/en/), rasterized at 10 arcmin. Finally, we assigned to each pixel the corresponding biomass of fine root colonized by mycorrhiza, considering the prevailing spatial unit. Those spatial units that remained empty due to lack of vegetation plots or colonization data were filled with the mean value of the ecoregion x continent combination.Quality index mapsAs our workflow comprises many different data sources and the extracted data acts in distinct hierarchical levels (i.e plant species, plots or spatial unit level), providing a unified uncertainty estimation for our maps is particularly challenging. Estimates of mycorrhizal fine root C stocks are related mainly to belowground biomass C density maps and mycorrhizal aboveground biomass maps, which have associated uncertainties maps provided by the original publications. In contrast, estimates of the intensity of root colonization in each spatial unit have been associated with three main sources of uncertainties:

    1)

    The number of observations in the FungalRoot database. The mean species-level intensity of mycorrhizal colonization in the vegetation plots has been associated with a number of independent observations of root colonization for each plant species. We calculated the mean number of observations of each plant species for each of the vegetation plots and, subsequently the mean number of observations (per plant species) from all vegetation plots in each spatial unit. These spatial unit averaged number of observations ranged from 1 to 14 in AM and from 1 to 26 in EcM. A higher number of observations would indicate that the intraspecific variation in the intensity of colonization is better captured and, therefore, the species-specific colonization estimates are more robust.

    2)

    The relative plant coverage that was associated with colonization data. From the selected vegetation plots, only a certain proportion of plant species could be associated with the intensity of colonization data in FungalRoot database. The relative abundance of the plant species with colonization data was summed up in each vegetation plot. Then, we calculated the average values for each spatial unit. Mean abundance values ranged from 0.3 to 100% in both AM and EcM spatial units. A high number indicates that the dominant plant species of the vegetation plots have colonization data associated and, consequently, the community-averaged intensity of colonization estimates are more robust.

    3)

    The number of vegetation plots in each spatial unit. Each of the spatial units differs in the number of plots used to calculate the mean intensity of colonization, ranging from 1 to 1583 and from 1 to 768 plots in AM and EcM estimations, respectively. A higher number of plots is associated with a better representation of the vegetation variability in the spatial units, although this will ultimately depend on plot size and intrinsic heterogeneity (i.e., a big but homogeneous spatial unit may need fewer vegetation plots for a good representation than a small but very heterogeneous spatial unit).

    We provide independent quality index maps of the spatial unit average of these three sources of uncertainty. These quality index maps can be used to locate areas where our estimates have higher or lower robustness. More