Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest

Abstract

The relationships between plant carbon resources, soil carbon and nitrogen content, and ectomycorrhizal fungal (EMF) diversity in a monospecific, old-growth beech (Fagus sylvatica) forest were investigated by manipulating carbon flux by girdling. We hypothesized that disruption of the carbon supply would not affect diversity and EMF species numbers if EM fungi can be supplied by plant internal carbohydrate resources or would result in selective disappearance of EMF taxa because of differences in carbon demand of different fungi. Tree carbohydrate status, root demography, EMF colonization, and EMF taxon abundance were measured repeatedly during 1 year after girdling. Girdling did not affect root colonization but decreased EMF species richness of an estimated 79 to 90 taxa to about 40 taxa. Cenococcum geophilum, Lactarius blennius, and Tomentella lapida were dominant, colonizing about 70% of the root tips, and remained unaffected by girdling. Mainly cryptic EMF species disappeared. Therefore, the Shannon-Wiener index (H') decreased but evenness was unaffected. H' was positively correlated with glucose, fructose, and starch concentrations of fine roots and also with the ratio of dissolved organic carbon to dissolved organic nitrogen (DOC/DON), suggesting that both H' and DOC/DON were governed by changes in belowground carbon allocation. Our results suggest that beech maintains numerous rare EMF species by recent photosynthate. These EM fungi may constitute biological insurance for adaptation to changing environmental conditions. The preservation of taxa previously not known to colonize beech may, thus, form an important reservoir for future forest development.

FIG. 1.

Seasonal fluctuations in demography of root tips of healthy beech trees and trees after girdling. Bars indicate means (±standard errors) of 15 measurements per treatment and time point for vital ectomycorrhizal root tips (A), vital nonmycorrhizal root tips (B), dead ectomycorrhizal root tips (C), and dead nonmycorrhizal root tips (D). F and P values obtained by repeated-measures analyses of variance are shown next to the figures. P values of <0.05 are shown by bold letters.

FIG. 2.

Starch (A) and soluble carbohydrate (B) concentrations in coarse and fine roots of healthy beech trees (C) or trees after girdling (G). Samples were collected in October 2006 (-06) and October 2007 (-07). Bars indicate means (±standard errors) of 15 measurements per treatment and time point. glc, glucose; frc, fructose; suc, sucrose. Different letters indicate significant differences at a P value of ≤0.05.

FIG. 3.

Relative abundances, sorted according to descending rank, of EMF species at roots of girdled trees and at roots of control beech trees. The relative abundance was calculated for all sampling dates together. y, number of ectomycorrhizal root tips. Dashed lines indicate the range of lost species with a detection probability of P ≤ 0.99. Details are given in the text.

FIG. 4.

Seasonal fluctuations of rarefied Shannon-Wiener index (H′), species richness (S), and evenness of ectomycorrhizal fungal species on roots of girdled and control beech trees. Results are means (±standard errors) of 15 measurements, except those for girdled trees at 2 and 10 months after girdling, which are means (±standard errors) of 3 and 7 measurements, respectively. For each sample, 100 (±10) root tips were registered. F and P values obtained by repeated-measures analyses of variance are shown next to the figures. P values of <0.05 are shown by bold letters.

FIG. 5.

DCA of EMF communities on roots of healthy (C) and girdled (G) trees. Numbers represent the sampling time points (1, October 2006; 2, May 2007; 3, August 2007; 4, October 2007).

FIG. 6.

Regression between the Shannon-Wiener index (H′) and the sum of glucose and fructose (A) and DOC/DON (B). Data for DOC and DON were taken from reference . H′ is given as the means of five soil cores collected per plot in October 2006 and October 2007, respectively. An exception was October 2006, when only one pooled data set across all three plots was available for girdled trees. Filled symbols, controls; open symbols, girdled trees.