Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest

Abstract

The central role that ectomycorrhizal (EM) symbioses play in the structure and function of boreal forests pivots around the common assumption that carbon (C) and nitrogen (N) are exchanged at rates favorable for plant growth. However, this may not always be the case. It has been hypothesized that the benefits mycorrhizal fungi convey to their host plants strongly depends upon the availability of C and N, both of which are rapidly changing as a result of intensified human land use and climate change. Using large-scale shading and N addition treatments, we assessed the independent and interactive effects of changes in C and N supply on the transfer of N in intact EM associations with ~15 yr. old Scots pine trees. To assess the dynamics of N transfer in EM symbioses, we added trace amounts of highly enriched 15 NO 3 label to the EM-dominated mor-layer and followed the fate of the 15 N label in tree foliage, fungal chitin on EM root tips, and EM sporocarps. Despite no change in leaf biomass, shading resulted in reduced tree C uptake, ca. 40% lower fungal biomass on EM root tips, and greater 15 N label in tree foliage compared to unshaded control plots, where more 15 N label was found in fungal biomass on EM colonized root tips. Short-term addition of N shifted the incorporation of 15 N label from EM fungi to tree foliage, despite no significant changes in below-ground tree C allocation to EM fungi. Contrary to the common assumption that C and N are exchanged at rates favorable for plant growth, our results show for the first time that under N-limited conditions greater C allocation to EM fungi in the field results in reduced, not increased, N transfer to host trees. Moreover, given the ubiquitous nature of mycorrhizal symbioses, our results stress the need to incorporate mycorrhizal dynamics into process-based ecosystem models to better predict forest C and N cycles in light of global climate change.

Short-term carbon input increases microbial nitrogen demand, but not microbial nitrogen mining, in a set of boreal forest soils

“…Microbial N mining might thus depend not on plantsoil C allocation in general, but specifically on the allocation of C to certain mycorrhiza. However, recent studies in boreal forests suggest that a high transfer of C from plants to ectomycorrhiza can also reduce plant N uptake as ectomycorrhiza keep a larger proportion of the available N for themselves (Hasselquist et al 2016;Näsholm et al 2013). Our laboratory experiment showed a similar stimulation of N sequestration by C input in non-symbiotic soil microorganisms and suggests that increased C availability can at least in the short term also reduce N availability for plants.…”

Dual‐mycorrhizal plants: their ecology and relevance

“…Therefore, a difference in the propensity to produce exploratory hyphae may be an advantage of EM fungi, even though it comes with increased absolute C partitioning belowground (Jones et al ., ). By contrast, retention of nutrients by the fungus to meet its own needs has been demonstrated for both EM and AM symbioses; therefore, the larger proportion of fungal tissue in EM than AM roots may be detrimental to plants in low‐nutrient soils (Hasselquist et al ., ; Püschel et al ., ; Teste et al ., ).…”

Dynamics of soil CO2 efflux under varying atmospheric CO2 concentrations reveal dominance of slow processes

“…Shading experiments can reduce C allocation to belowground less destructively, allowing evaluation of the effect of reduced carbohydrate source on belowground processes. In combination with enhanced N supply, such experiments can also alter carbohydrate sinks both aboveground and belowground, allowing further definition of processes (Hasselquist et al., ). However, the approach has only been employed over short vegetation: crops/grasses (Manderscheid, Pacholski, & Weigel, ), seedlings (Mao et al., ), or young trees (Hasselquist et al., ; Walcroft, Whitehead, Kelliher, Arneth, & Silvester, ).…”

“…In combination with enhanced N supply, such experiments can also alter carbohydrate sinks both aboveground and belowground, allowing further definition of processes (Hasselquist et al., ). However, the approach has only been employed over short vegetation: crops/grasses (Manderscheid, Pacholski, & Weigel, ), seedlings (Mao et al., ), or young trees (Hasselquist et al., ; Walcroft, Whitehead, Kelliher, Arneth, & Silvester, ). Stem chilling (Johnsen et al., ) and the recently developed pressure girdling (Henriksson et al., ) are both nondestructive methods for reversibly reducing carbohydrate transport to belowground.…”

“…We thus hypothesized that ( H1 ) the effect of five‐day CO 2 manipulation during the end of the growing season would be reflected in changes of F CO2 proportional to the change of CO 2 concentration during the 5 days. The reduction of F CO2 has been explained not only by a decrease in sugar flow belowground, but also in terms of rapidly decreasing biomass of mycorrhizae and fine roots (Drake et al., ; Hasselquist et al., ; Högberg et al., ; Jing et al., ). Reductions of mycorrhizae may occur within a week (Högberg et al., ).…”