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.In temperate and boreal forest ecosystems, most tree species form ectomycorrhizal fungal (EMF) associations. EM fungi ensheathe the root tip, forming characteristic mantlelike structures (1). The presence and lengths of hyphae emanating from the mantle are characteristic of different EMF species and establish different soil exploration types (2). It has been assumed that EMF communities are adapted specifically to mobilize sparse soil nutrient resources in boreal and temperate forests (11, 50). Current estimates indicate that about 80% of all nitrogen and phosphorus present in plants has been taken up via mycorrhizas (30,41,63).Unlike free-living soil microbes, EM fungi have direct access to reduced carbon from their host plants. More than 50 years ago, Melin and Nilsson (46) showed that 14 C applied to leaves was recovered within one day in EM fungi, suggesting a strong dependence of fungal metabolism on host photosynthesis. Subsequent isotopic studies corroborated tight connections between current photosynthate and EM fungi (28,42). EMF hyphae constitute the main path of plant-derived carbon into the soil (24, 29). Furthermore, EMF hyphae contribute substantially to soil respiration (25% from hyphae and 15% from roots) (27). As hyphal respiration decreases strongly in response to girdling of trees, a tight metabolic link between extramatrical mycelia and host ...

Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress

“…Among the fungi in our study, C. geophilum is known as a drought-tolerant species (Coleman et al, 1989;Di Pietro et al, 2007). It is abundant on beech roots in dry habitats (Jany et al, 2003;Pena et al, 2010), but its function for forest tree N nutrition has been disputed (Herzog et al, 2012;Kipfer et al, 2012). The current results indicate a buffering function for C. geophilum against varying environmental conditions but also suggest that other EMF species provide greater host benefits under water-limiting conditions.…”

“…In our experiment, we used an NH 4 þ concentration similar to that found in the Tuttlingen forest (Dannenmann et al, 2009), where the soil for beech mycorrhizal inoculation was sampled. The beech trees in the Tuttlingen forest are colonized by a characteristic EMF flora, including all species present in this study (Buée et al, 2005;Pena et al, 2010;. Intact roots of these trees showed saturation of NH 4 þ uptake above a threshold of 50 mM NH 4 þ when exposed to feeding solutions with increasing NH 4 þ concentrations (Gessler et al, 2005).…”

“…Ectomycorrhizal communities are usually composed of a diverse flora consisting of several dominant and many infrequent EMF species (Buée et al, 2007;Courty et al, 2010;Pena et al, 2010;Tedersoo et al, 2012a;Danielsen et al, 2013). EMF community structures are strongly influenced by N deposition (Lilleskov et al, 2011;Kjøller et al, 2012).…”

Diversity of ectomycorrhizal fungus assemblages on nursery grown European beech seedlings

“…Detailed descriptions of the morphology and anatomy of 23 fungal taxa was revealed by Agerer (1987Agerer ( -2008. PCR-based molecular methods and DNA sequencing have been used to identify mycorrhizal fungi for the last 20 years as a matter of routine, and have led to a greater understanding of the composition and structure of the ECM fungal communities of beech in mature forests (Buée et al 2005;Grebenc and Kraigher 2007;Grebenc et al 2009;Pena et al 2010), or on young trees in natural conditions or in pot experiments (Železnik et al 2007;Druebert et al 2009;Pritsch et al 2009). These studies revealed remarkable below-ground ECM fungal taxa richness (16 to 89 taxa), depending on the beech age, and site or experimental conditions.…”

Comparison of root-associated communities of native and non-native ectomycorrhizal hosts in an urban landscape

“…EcM species differ in their functional attributes and physiological tolerances (Baxter and Dighton 2001;2005). Thus, greater diversity of root-associated symbionts should translate to more diverse benefits to the host, or alternatively, to greater flexibility under changing conditions (Druebert et al 2009;Pena et al 2010). However, the importance of mycorrhiza-mediated ecosystem services and/or host benefits in intensively managed, fertilized and watered urban systems remains unclear and requires further investigation.…”