Forests trapped in nitrogen limitation – an ecological market perspective on ectomycorrhizal symbiosis

Abstract

Ectomycorrhizal symbiosis is omnipresent in boreal forests, where it is assumed to benefit plant growth. However, experiments show inconsistent benefits for plants and volatility of individual partnerships, which calls for a re-evaluation of the presumed role of this symbiosis.We reconcile these inconsistencies by developing a model that demonstrates how mycorrhizal networking and market mechanisms shape the strategies of individual plants and fungi to promote symbiotic stability at the ecosystem level.The model predicts that plants switch abruptly from a mixed strategy with both mycorrhizal and nonmycorrhizal roots to a purely mycorrhizal strategy as soil nitrogen availability declines, in agreement with the frequency distribution of ectomycorrhizal colonization intensity across a wide-ranging data set. In line with observations in field-scale isotope labeling experiments, the model explains why ectomycorrhizal symbiosis does not alleviate plant nitrogen limitation. Instead, market mechanisms may generate self-stabilization of the mycorrhizal strategy via nitrogen depletion feedback, even if plant growth is ultimately reduced.We suggest that this feedback mechanism maintains the strong nitrogen limitation ubiquitous in boreal forests. The mechanism may also have the capacity to eliminate or even reverse the expected positive effect of rising CO2 on tree growth in strongly nitrogen-limited boreal forests.

Ectomycorrhizal Fungal Protein Degradation Ability Predicted by Soil Organic Nitrogen Availability

“…While their secretion appears to be induced by the presence of protein (16), recent results for a model ECM species (Paxillus involutus; Boletales, Basidiomycota) also showed that uptake of N from organic matter is additionally dependent on the availability of a simple carbon (C) source (17). The latter result supports the hypothesis that mining for organic N by ECM species does not occur without an energy supply (18,19). However, since the last two studies compared only the presence and absence of glucose, it has yet to be determined how different levels of C affect organic N degradation.…”

Variability of projected terrestrial biosphere responses to elevated levels of atmospheric CO<sub>2</sub> due to uncertainty in biological nitrogen fixation

“…Asymbiotic forms of BNF include plant-associated BNF (N-fixing microbes inhabiting the plant rhizosphere but not entering direct plantmicrobe symbioses), as well as heterotrophic BNF carried out by free-living bacteria. Furthermore, BNF from mycorrhizal fungi (Franklin et al, 2014) and cryptogamic communities (Elbert et al, 2012) has been shown to be of significant magnitude. These groups of N fixing organisms are phylogenetically diverse and poorly understood (Vitousek et al, 2013), making the quantification of global BNF rates challenging.…”

Simulating ectomycorrhiza in boreal forests: implementing ectomycorrhizal fungi model MYCOFON in CoupModel (v5)

“…A previous CoupModel application by Wu et al (2012) demonstrated that the nonlim approach could possibly describe short-term C and water dynamics for a Finnish forest site. The same nonlim approach was also used in Franklin et al (2014) to simulate Swedish forest biomass growth and its competition with ECM. This seems to suggest that plant growth and the C cycle can be simulated reasonably with the nonlim approach, although a slight trend of overestimation is exhibited.…”

“…The ECM implicit approach has been used in a similar way by Kirschbaum and Paul (2002) and Svensson et al (2008a). The nonlim approach assumes an "open" N cycle and plant growth is limited by a constant N availability to a static fixed level (e.g., in Franklin et al, 2014). These three ECM modeling approaches constitute most of the current ECM representations in ecosystem models and are tested by four forest sites situated along a climate and N fertility gradient across Sweden (Fig.…”