Shifts in Ectomycorrhizal Fungal Communities and Exploration Types Relate to the Environment and Fine-Root Traits Across Interior Douglas-Fir Forests of Western Canada

Abstract

Large-scale studies that examine the responses of ectomycorrhizal fungi across biogeographic gradients are necessary to assess their role in mediating current and predicted future alterations in forest ecosystem processes. We assessed the extent of environmental filtering on interior Douglas-fir (Pseudotsuga menziesii var. glauca (Beissn.) Franco) ectomycorrhizal fungal communities across regional gradients in precipitation, temperature, and soil fertility in interior Douglas-fir dominated forests of western Canada. We also examined relationships between fine-root traits and mycorrhizal fungal exploration types by combining root and fungal trait measurements with next-generation sequencing. Temperature, precipitation, and soil C:N ratio affected fungal community dissimilarity and exploration type abundance but had no effect on α-diversity. Fungi with rhizomorphs (e.g., Piloderma sp.) or proteolytic abilities (e.g., Cortinarius sp.) dominated communities in warmer and less fertile environments. Ascomycetes (e.g., Cenococcum geophilum) or shorter distance explorers, which potentially cost the plant less C, were favored in colder/drier climates where soils were richer in total nitrogen. Environmental filtering of ectomycorrhizal fungal communities is potentially related to co-evolutionary history between Douglas-fir populations and fungal symbionts, suggesting success of interior Douglas-fir as climate changes may be dependent on maintaining strong associations with local communities of mycorrhizal fungi. No evidence for a link between root and fungal resource foraging strategies was found at the regional scale. This lack of evidence further supports the need for a mycorrhizal symbiosis framework that is independent of root trait frameworks, to aid in understanding belowground plant uptake strategies across environments.

Keywords: Pseudostuga menziesii var. glauca; biogeographic gradient; ectomycorrhizal fungi; exploration type; fine-root traits; forest ecosystems; functional ecology; mycorrhizas.

FIGURE 1

Geographical distribution of study regions (rectangles) and forest stands (3 triangles per study region) across the current natural range of interior Douglas-fir (Pseudotsuga menziesii var. glauca; green shading) in British Columbia, Canada.

FIGURE 2

Relative abundance (%) of ectomycorrhizal taxa on interior Douglas-fir among five regions in western Canada. Only the species/genera representing >2% of root tip abundance were included. For a given ectomycorrhizal species, numbers represent the percentage of root tips colonized by this species in each region.

FIGURE 3

Distance-based redundancy analysis (db-RDA) sample (A) and species (B) ordinations based on ectomycorrhizal fungal abundance on interior Douglas-fir roots across five regions in western Canada. Only the variation explained by environmental variables is visualized. The ectomycorrhizal species are color-coded by fungal exploration type and are sized according to their relative abundance. The species epithet (when known) was removed to improve readability. MAP, mean annual precipitation; MAT, mean annual temperature; CN, soil carbon-to-nitrogen ratio. To aid comparison, predictor variables were standardized (z-scores) prior to analysis and are therefore unitless. Contact-, short- and medium-distance smooth exploration types are hydrophylic while medium-distance fringe and long-distance exploration types are hydrophobic.

FIGURE 4

Ectomycorrhizal fungal species-specific response to environmental factors based on multivariate generalized linear models. Only species that were responsive were added to the model (coefficient > |5| ). Circles (•) represent species coefficients and lines, 95% confidence intervals. Species were grouped by exploration type indicated at the right-hand side of the plot, MAT, mean annual temperature; MAP, mean annual precipitation; CN, soil carbon-to-nitrogen ratio. To aid comparison, predictor variables were standardized (z-scores) prior to analysis and are therefore unitless. Hi, hydrophylic; Ho hydrophobic.

FIGURE 5

Distance-based redundancy analysis (db-RDA) sample (A) and exploration type (B) ordinations based on ectomycorrhizal fungal exploration type on interior Douglas-fir across five regions in western Canada. The ectomycorrhizal fungal exploration types are sized according to their relative abundance. MAP, mean annual precipitation; MAT, mean annual temperature; CN, soil carbon-to-nitrogen ratio. To aid comparison, predictor variables were standardized (z-scores) prior to analysis and are therefore unitless. Contact-, short- and medium-distance smooth exploration types are hydrophylic while medium-distance fringe and long-distance exploration types are hydrophobic.

FIGURE 6

Distance-based redundancy analysis (db-RDA) sample (A) and species (B) ordinations based on ectomycorrhizal fungal abundance on interior Douglas-fir across five regions. Only variation explained by Douglas-fir fine-root traits is visualized. The ectomycorrhizal species are color-coded by fungal exploration type and are sized according to their relative abundance. The species epithet (when known) was removed to improve readability. CN, fine-root carbon-to-nitrogen ratio; RTD, fine-root tissue density. To aid comparison, predictor variables were standardized (z-scores) prior to analysis and are therefore unitless. Contact-, short- and medium-distance smooth exploration types are hydrophylic while medium-distance fringe and long-distance exploration types are hydrophobic.