Mona N. Högberg

Isotopic pulse-labelling of photosynthate allows tracing of carbon (C) from tree canopies to below-ground biota and calculations of its turnover in roots and recipient soil microorganisms. A high concentration of label is desirable but is difficult to achieve in field studies of intact ecosystem patches with trees. Moreover, root systems of trees overlap considerably in most forests, which requires a large labelled area to minimize the impact of C allocated below-ground by un-labelled trees. We describe a method which combines a high level of labelling at ambient concentrations of CO2, [CO2], with undisturbed root systems and a model to account for root C and root-derived C from un-labelled trees. We raised 5-m-tall chambers, each covering 50 m2 of ground (volume 250 m3) in a young boreal Pinus sylvestris L. forest with up to 5 m tall trees. Rather than a conventional single release of 13CO2, we used five consecutive releases, each followed by a draw-down period, thus avoiding high [CO2]. Hence, we elevated successively the 13CO2 from 1.1 to 23 atom% after the first release to 61 atom% after the fifth, while maintaining [CO2] below 500 p.p.m. during 4–4.5 h of labelling. The average abundance of 13CO2 was as high as 42 atom%. We used the central 10 m2 of the 50 m2 area for sampling of roots and other soil biota. We modelled the dilution of labelled C across the plots by un-labelled C from roots of trees outside the area. In the central 10 m2 area, ~85% of roots and root-associated biota received C from labelled trees. In summary, we elevated the labelling of roots and associated soil biota four-fold compared with previous studies and described the commonly overlooked impact of roots from un-labelled trees outside the labelled area.

Summary: Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or ‘mother trees’, support the growth of seedlings in this way. This narrative has far‐reaching implications for our understanding of forest ecology and has been controversial in the scientific community. We review the current understanding of ectomycorrhizal C metabolism and observations on forest regeneration that make the mother tree narrative debatable. We then re‐examine data and conclusions from publications that underlie the mother tree hypothesis. Isotopic labeling methods are uniquely suited for studying element fluxes through ecosystems, but the complexity of mycorrhizal symbiosis, low detection limits, and small carbon discrimination in biological processes can cause researchers to make important inferences based on miniscule shifts in isotopic abundance, which can be misleading. We conclude that evidence of a significant net C transfer via common mycorrhizal networks that benefits the recipients is still lacking. Furthermore, a role for fungi as a C pipeline between trees is difficult to reconcile with any adaptive advantages for the fungi. Finally, the hypothesis is neither supported by boreal forest regeneration patterns nor consistent with the understanding of physiological mechanisms controlling mycorrhizal symbiosis.

Summary: The supply of carbon (C) from tree photosynthesis to ectomycorrhizal (ECM) fungi is known to decrease with increasing plant nitrogen (N) supply, but how this affects fungal nutrition and growth remains to be clarified. We placed mesh‐bags with quartz sand, with or without an organic N (¹⁵N‐, ¹³C‐labeled) source, in the soil along a natural N supply gradient in boreal forest, to measure growth and use of N and C by ECM extramatrical mycelia. Mycelial C : N declined with increasing N supply. Addition of N increased mycelial growth at the low‐N end of the gradient. We found an inverse relationship between uptake of added N and C; the use of added N was high when ambient N was low, whereas use of added C was high when C from photosynthesis was low. We propose that growth of ECM fungi is N‐limited when soil N is scarce and tree belowground C allocation to ECM fungi is high, but is C‐limited when N supply is high and tree belowground C allocation is low. This suggests that ECM fungi have a major role in soil N retention in nutrient‐poor, but less so in nutrient‐rich boreal forests.

Summary: 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.