Plant-fungal symbioses play critical roles in vegetation dynamics and nutrient cycling, modulating the impacts of global changes on ecosystem functioning. Here, we used forest inventory data consisting of more than 3 million trees to develop a spatially resolved “mycorrhizal tree map” of the contiguous United States. We show that abundances of the two dominant mycorrhizal tree groups—arbuscular mycorrhizal (AM) and ectomycorrhizal trees—are associated primarily with climate. Further, we show that anthropogenic influences, primarily nitrogen (N) deposition and fire suppression, in concert with climate change, have increased AM tree dominance during the past three decades in the eastern United States. Given that most AM-dominated forests in this region are underlain by soils with high N availability, our results suggest that the increasing abundance of AM trees has the potential to induce nutrient acceleration, with critical consequences for forest productivity, ecosystem carbon and nutrient retention, and feedbacks to climate change.

The two dominant types of fungi that associate with trees—arbuscular mycorrhizal (AM) and ectomycorrhizal (EM)—differ greatly in their forms and functions. Consequently, tree mycorrhizal associations have been hypothesized to represent trait-integrating phenotypes that give rise to “biogeochemical syndromes” in forests ( 13 ), although the relative contribution of the plants versus fungi to these syndromes is poorly quantified. EM-dominated forests often cycle carbon (C) and nutrients conservatively owing to the lower chemical quality of EM plant litter relative to that of AM-dominated forests, which have more “open” C and nutrient cycles ( 17 , 18 ). These effects not only alter the degree to which these ecosystems store C and nutrients ( 19 – 22 ) but also likely affect their sensitivity to human-induced global changes ( 23 – 26 ). Here, using forest inventory data collected by the U.S. Department of Agriculture (USDA) Forest Service, Forest Inventory and Analysis (FIA) program across the contiguous United States, we (i) map the tree mycorrhizal association patterns and identify underlying drivers of these observed associations; (ii) quantify the impacts of human-induced global changes, primarily climate change, N deposition, and disturbance regimes, on tree mycorrhizal associations; and (iii) assess the potential feedback of mycorrhizal association shifts on soil C and nutrient dynamics.

The forests of North America are experiencing unprecedented change owing to the combined effects of climate change, nitrogen (N) deposition, changes in disturbance regime, habitat fragmentation, and invasions of exotic species ( 1 – 5 ). While anthropogenic-induced shifts in the distribution and abundance of tree communities are well described ( 1 , 6 ), far less is known about the direct and indirect impacts of global anthropogenic changes on plant-fungal associations ( 7 , 8 ). More than 90% of vascular plants associate with mycorrhizal fungi ( 9 , 10 ), and there is an emerging consensus that these plant-fungal associations have profound impacts on nutrient cycling and vegetation dynamics in ecosystems, particularly temperate forests ( 11 – 15 ). However, critical gaps remain in our understanding of biogeographic patterns of mycorrhizal associations, and our limited knowledge of the anthropogenic factors responsible for shifting plant-mycorrhizal distributions has hindered efforts to predict ecosystem feedbacks to climate change ( 16 ).

RESULTS AND DISCUSSION

Distribution and drivers of tree mycorrhizal association patterns Using FIA vegetation data and tree mycorrhizal type information, we mapped the relative abundance of more than 3 million AM and EM trees across the conterminous United States (Fig. 1A). While patterns of mycorrhizal associations and associated drivers have been reported previously, these studies were based on species occurrence data (27–29), and they covered lesser spatial extent (30) and examined fewer vegetation survey plots than our study (31). Our results indicate that AM trees are more dominant in dry and warm ecoregions, while EM trees are more dominant in humid and cold ecoregions (Fig. 1, A and B). In the western United States, AM trees are dominant in the subtropical desert and steppe regions, while EM trees are dominant in the northwestern and intermountain west regions (Fig. 1A and fig. S1). AM and EM trees are well mixed in the eastern United States, with more AM trees in the hot continental region and more EM trees in the western portion of the warm continental region (Fig. 1 and fig. S1). Using a mixed-effects model that accounts for the spatial heterogeneity between plots in different subecoregions, we found that climate is an important driver of tree mycorrhizal association patterns at the continental scale (Fig. 1C). Overall, AM tree dominance was negatively associated with mean annual precipitation (MAP) and positively associated with mean annual temperature (MAT) (Fig. 1C), although the magnitude and direction of effect sizes differed in some ecoregions. Forest tree basal area, which was used as an indicator of forest successional stage, had smaller effects on AM tree dominance compared with climatic factors, implying that climate is a more important driver of the continental tree mycorrhizal association patterns than successional stage (Fig. 1C). Fig. 1 Distribution of forest tree mycorrhizal types and their associated factors in forests of the contiguous United States. (A) Geographical distribution of AM tree dominance. (B) Distribution of AM tree dominance in climatic space. MAP, mean annual precipitation; MAT, mean annual temperature. (C) Relative effects of MAP, MAT, and tree basal area on AM tree dominance. Each dot in (A) and (B) represents a plot and is colored on the basis of the associated AM-EM tree dominance. Boundaries of ecoregions (solid line) and nested subecoregions (dashed lines) in (A) are based on Cleland et al. (58). Circles in (B) indicate ecoregion-level mean MAT and MAP values with the associated SDs. The circle is colored on the basis of the mean AM tree dominance, and the size is proportional to the number of plots (log scale). Effects of MAP, MAT, and basal area on AM tree dominance across ecoregions in the contiguous United States (C) were tested using generalized mixed-effects models with subecoregions included as a random effect in each model. Significant coefficient estimates are plotted in (C) as solid circles, and nonsignificant ones are plotted as open circles. Circle size is proportional to the number of plots (log scale). The number beside each dot in (B) and (C) represents the associated ecoregion in (A). Error bars in (C) are SEs.

Shifts in tree mycorrhizal associations and associated drivers To understand the impacts of human-induced global changes on tree mycorrhizal associations, we used repeated measures of forest inventories from the FIA program during the past three decades in the eastern United States where rapid climate change has been observed (fig. S2) (1). AM tree dominance has significantly increased in all parts of the eastern United States during the past three decades (based on a paired Wilcoxon signed-rank test, P < 0.05; Fig. 2A), especially in the central regions (17% increase in prairie and 15% increase in hot continental regions), because of both an increase in AM tree abundance (i.e., basal area; fig. S3A) and a decrease in EM tree abundance (fig. S3B). AM tree dominance in southern and northern ecoregions also increased (5% increase in warm continental and 5% increase in subtropical; Fig. 2A), although these regions had statistically significant increases in both AM and EM tree abundance (fig. S3, A and B). In particular, the western portion of the warm continental region and northern portion of the subtropical region had similar increases in AM tree abundance, while the eastern portion of the warm continental region and southern portion of the subtropical region had the opposite trend (Fig. 2A). Fig. 2 Changes in forest AM tree dominance during the past three decades and the relative impacts of environmental changes on the mycorrhizal association changes in forests of the eastern United States. (A) Changes in AM tree dominance over the two inventories (T2-T1). All ecoregions had a significant increase in AM tree dominance during the period based on a paired Wilcoxon signed-rank test (P < 0.05; inset figures are boxplots of hexagon-level changes by ecoregions). (B) Relative effects of climate and basal area change, AM tree dominance at the first inventory (T1), N deposition, and fire frequency on AM tree dominance change. (C) Effects of tree abundance change of the top 10 most abundant tree genera (genera on the left without shaded background are AM trees, and genera on the right are EM trees) on AM tree dominance change. Mean coefficients in (B) and (C) were estimated at the ecoregion level based on generalized mixed-effects models with subecoregions included as a random effect. Significant coefficient estimates are plotted as solid circles, and nonsignificant ones are plotted as open circles with the size being proportional to the number of hexagons (log scale). Error bars in (B) and (C) are SEs. Our analysis indicates that three factors—N deposition, fire frequency, and climate change—likely contributed to the increases in AM tree dominance. First, we found a strong positive correlation between N deposition and shifts in AM tree dominance, consistent with earlier studies based on smaller spatial extent and shorter temporal scale (31). In temperate forests, most AM tree species have nutrient acquisitive traits (e.g., rapid root growth into nutrient hot spots and narrower C:N in leaf and root tissues) (17, 32–34) and often dominate stands characterized by open (i.e., fast) N cycles (13, 30). Thus, the positive relationship between N deposition and AM dominance may result from AM trees being competitively superior at acquiring excess N—the nutrient that generally limits plant growth in these forests. Second, we found strong negative associations between fire frequency and AM tree dominance (Fig. 2B). While it is well established that fire suppression following European settlement has led to oak (Quercus) regeneration failure and forest “mesophication” in the eastern United States (35), our results indicate that this trend is not merely a result of EM-associating oaks being replaced by AM-associating maples (Acer). The change in AM tree dominance was not driven by a specific phylogenetic group of tree species, as the most common AM and EM tree genera had relatively similar effect sizes on the change (Fig. 2C). Changes of abundance in all five most common AM genera, with a few statistically nonsignificant exceptions, were positively associated with AM tree dominance change, while the changes of abundance in EM genera were nearly all negatively associated with the AM tree dominance change (Fig. 2C). Possible explanations for the observed nonsignificant outliers (e.g., Prunus in prairie and Carya in warm continental region) could be due to small sample sizes or potential preferential harvesting in these regions. The third factor contributing to increases in AM tree dominance is climate change. In general, increases in MAP were negatively associated with increases in AM tree dominance, while the associations with MAT were weak and variable (Fig. 2B). The extent to which other factors may contribute to future shifts in tree mycorrhizal associations is unknown. AM tree dominance tended to increase with basal area, an indicator of forest succession, as shade-tolerant AM trees increase their abundance with the progression of forest succession. However, the effects of basal area were relatively small compared with the other drivers, suggesting that anthropogenic drivers (i.e., climate change, N deposition, and fire suppression) had far greater impact on recent demographic shifts. Other factors such as land use change and forest management, which directly affect tree species dominance, could also affect shifts in tree mycorrhizal associations. In addition, to the extent that pollution control and reduction reduce N loading to U.S. forests, future shifts in mycorrhizal associations may be lessened in the coming decades. A continuing shift to AM tree dominance is also predicted by our finding that saplings were more AM-dominated compared with adult trees in 7 of 11 ecoregions (Fig. 3). In the eastern United States, all ecoregions other than the warm continental region had greater AM tree dominance in saplings compared with adult trees (Fig. 3). The prairie, hot continental, and subtropical regions had more than 54% greater sapling AM tree dominance compared with adult trees. The differences in AM tree dominance between saplings and adult trees were mixed in the western United States (Fig. 3). Compared with adult trees, more AM saplings were observed in the marine, Mediterranean, and temperate steppe regions, but less AM saplings were observed in the temperate desert, tropical/subtropical desert, and tropical/subtropical steppe regions. In addition, the overall differences between adult and sapling AM tree dominance were smaller than those observed in the ecoregions in the eastern United States (Fig. 3). Fig. 3 AM tree dominance differences between adult trees and saplings in forests across 11 ecoregions of the United States. The difference in AM tree dominance between adults and saplings for each ecological region were tested on the basis of a paired Wilcoxon signed-rank test (*P < 0.05; **P < 0.01; ***P < 0.001). Error bars are SEs. The bar thickness is proportional to the number of plots (log scale). Only plots where both adult trees and saplings are present are used for the analysis (98,638 plots).