Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees

Abstract

Photosynthesis by leaves and acquisition of water and minerals by roots are required for plant growth, which is a key component of many ecosystem functions. Although the role of leaf functional traits in photosynthesis is generally well understood, the relationship of root functional traits to nutrient uptake is not. In particular, predictions of nutrient acquisition strategies from specific root traits are often vague. Roots of nearly all plants cooperate with mycorrhizal fungi in nutrient acquisition. Most tree species form symbioses with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi. Nutrients are distributed heterogeneously in the soil, and nutrient-rich "hotspots" can be a key source for plants. Thus, predicting the foraging strategies that enable mycorrhizal root systems to exploit these hotspots can be critical to the understanding of plant nutrition and ecosystem carbon and nutrient cycling. Here, we show that in 13 sympatric temperate tree species, when nutrient availability is patchy, thinner root species alter their foraging to exploit patches, whereas thicker root species do not. Moreover, there appear to be two distinct pathways by which thinner root tree species enhance foraging in nutrient-rich patches: AM trees produce more roots, whereas EM trees produce more mycorrhizal fungal hyphae. Our results indicate that strategies of nutrient foraging are complementary among tree species with contrasting mycorrhiza types and root morphologies, and that predictable relationships between below-ground traits and nutrient acquisition emerge only when both roots and mycorrhizal fungi are considered together.

Keywords: mycorrhizal fungi; plant traits; root proliferation; soil heterogeneity; symbioses.

Fig. S1.

Micrographs of the first three absorptive root orders. Root diameter increased from left to right in six AM (Upper) and seven EM (Lower) tree species. Complete genus and species names of trees are provided in Table 1.

Fig. S2.

Photographs of study site. (Left) Aerial view of the common garden plantation (highlighted with a dotted-line “fence,” © 2016 Google, Map data © 2016 Google). (Right) Ground view of the common garden plantation, showing the plot design. Each plot included six trees with the plot edges trenched to about 1 m and lined with plastic film to minimize root encroachment between plots.

Fig. S3.

Microscopic view of root–fungi associations. Both AM [Upper: Juglans nigra (Left), Liriodendron tulipifera (Right)] and EM [Lower: Pinus virginiana (Left), Pinus strobus (Right)] species are shown.

Fig. 1.

Foraging precision of roots vs. extramatrical mycorrhizal fungal hyphae. Six AM (red color) and seven EM (green color) tree species are shown. The thickness of the symbol “x” is proportional to averaged root diameter of the first three root orders of the species. Species located above the 1:1 line suggest higher foraging precision in mycorrhizal hyphae than roots, whereas species located below the 1:1 line suggest higher foraging precision in roots than mycorrhizal hyphae. Precision of mycorrhizal hyphal foraging of EM fungi was positively correlated with EM root foraging precision (slope = 2.58, r² = 0.76, P < 0.01; n = 7), but AM hyphal foraging precision was similar among the tree species (slope = 0.14, P = 0.16; n = 6).

Fig. S4.

Foraging precision of roots vs. extramatrical mycorrhizal fungal hyphae adjusted for background bacterial and saprotrophic fungal PLFA. Six AM (red color) and seven EM (green color) tree species are shown. The thickness of the symbol “x” is proportional to the averaged root diameter of the first three root orders of the species. AM fungal biomass was estimated using 16:1ω5c in EM plots as background bacterial PLFA, and EM fungal biomass was estimated using (18:1ω6 + 18:2ω9) in AM plots as background saprotrophic fungal PLFA. The precision of mycorrhizal hyphal foraging of EM fungi was positively correlated with EM root foraging precision (slope = 3.13, r² = 0.76, P = 0.05; n = 7), but AM hyphal foraging precision was less varied among the tree species (slope = 0.70, P = 0.13; n = 6).

Fig. S5.

Relationship of root and mycorrhizal fungal foraging attributes with absorptive root diameter in AM and EM tree species. Root diameter was determined from means of the first three orders of roots in each tree species, including six AM (Left) and seven EM (Right) tree species under two nutrient treatments (●, unfertilized controls; ○, treatments with supplemented organic nutrients). The error bar denotes 1 SE (n = 8, except for data for extramatrical mycorrhizas; details are provided in legend for Fig. 2). Statistics are shown in Table S3.

Fig. 2.

Species root length density and extramatrical mycorrhizal hyphal biomass under two nutrient treatments. Six AM (A and C; red color) and seven EM (B and D; green color) tree species were studied using an ingrowth method for one growing season. Bars with light colors represent unfertilized treatment, denoted by “no amendment,” and dark colors represent supplemented organic nutrients, denoted by “+ organic nutrients.” Error bars represent SEM (n = 8 for A and B, n = 7 for C; in D, sample size is denoted on each bar). Complete scientific names of trees are provided in Table 1.

Fig. S6.

Volumetric water content measured within the ingrowth cores with (○) or without (●) supplementary dried and ground leaves. Eight measurements were conducted from July to October 2013. For each measurement, a random block (including 13 species) was chosen and all of the 132 ingrowth cores of the block were measured for soil moisture with a time-domain reflectometer. For the ingrowth cores in plots of EM species, soil moisture of additional cores within the PVC root-exclusion tube was also measured (details are provided in Materials and Methods). Soil moisture was slightly lower in ingrowth cores with amended litter than in ingrowth cores containing only soil (decreased by 7% on average; P = 0.046). The difference was larger in root-excluded cores (cores placed within PVC tubes, decreased by 18% on average; P = 0.005).

Fig. 3.

Diagram showing the relationship between the mycorrhiza type, root diameter, and foraging precision of roots and mycorrhizal fungal hyphae. Some tree species, such as maple (A) and tulip poplar (B), associate with AM fungi, whereas others, such as oak (C) and pine (D), associate with EM fungi. Triangles depict simplified variation in patterns of the foraging precision of roots and mycorrhizal fungal hyphae roots with increasing root diameter.