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

Franklin O, Näsholm T, Högberg P, Högberg MN - New Phytol. (2014)

Bottom Line: Ectomycorrhizal symbiosis is omnipresent in boreal forests, where it is assumed to benefit plant growth.Instead, market mechanisms may generate self-stabilization of the mycorrhizal strategy via nitrogen depletion feedback, even if plant growth is ultimately reduced.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.

View Article: PubMed Central - PubMed

Affiliation: IIASA- International Institute for Applied Systems Analysis, A-2361, Laxenburg, Austria.

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Field measurements of ectomycorrhizal colonization intensity, for 125 species and 44 sites in the former Soviet Union (Akhmetzhanova et al., 2012), show high frequency of observations at very high or relatively low colonization intensity and fewer observations at intermediate colonization intensity, as predicted by our model. Statistical testing by k-means cluster analysis separated two clusters centered at high (95%) and low (21%) values with P < 0.0001. The colonization intensity is measured in per cent of maximal colonization intensity, based on the mean number of mycorrhizal root tips per root length for each species at each site, relative to a reference scale (Akhmetzhanova et al., 2012).
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fig05: Field measurements of ectomycorrhizal colonization intensity, for 125 species and 44 sites in the former Soviet Union (Akhmetzhanova et al., 2012), show high frequency of observations at very high or relatively low colonization intensity and fewer observations at intermediate colonization intensity, as predicted by our model. Statistical testing by k-means cluster analysis separated two clusters centered at high (95%) and low (21%) values with P < 0.0001. The colonization intensity is measured in per cent of maximal colonization intensity, based on the mean number of mycorrhizal root tips per root length for each species at each site, relative to a reference scale (Akhmetzhanova et al., 2012).

Mentions: When soil N availability increases to a level where a nonmycorrhizal strategy can invade, EMF only persist if their utility for a plant matches that of nonmycorrhizal roots, which requires EMF to invest more in N uptake (increase u) than in the absence of a nonmycorrhizal strategy (Fig.3 versus Fig. S2). However, EMF will not increase u more than necessary as this would reduce fitness. For a plant this means a switch from a clear advantage of the mycorrhizal strategy to equal utility of mycorrhizal and nonmycorrhizal roots. At the same time, there exists a u that allows the mycorrhizal strategy to invade a resident nonmycorrhizal strategy. Thus, both root strategies may coexist under further increasing soil N availability until EMF are forced to allocate all resources to N uptake (u→1, leaving nothing for reproductive growth), making the symbiosis unviable. Although mutual invasibility and convergence of the utilities of the alternative root strategies do not imply strictly equal frequency, they suggest that, on average, mycorrhizal and nonmycorrhizal roots coexist in similar proportions. These results agree with the patterns typically observed in gradients of increasing soil N availability: while plant growth gradually increases there is almost complete mycorrhizal root colonization under a range of low soil N availability, followed by coexistence of nonmycorrhizal and mycorrhizal roots, and finally disappearance of EMF (Taylor et al., 2000; Högberg et al., 2003; Nilsson et al., 2005; Kjøller et al., 2012). A corresponding negative trend was also found for soil mycelia where ectomycorrhizal species declined and disappeared (Högberg et al., 2014). Furthermore, because the increasing fungal allocation to N uptake components occurs at the expense of reproductive allocation (increased u), it agrees with empirically observed reductions in fruiting-body (reproductive structures) production at high N additions (Peter et al., 2001; Hasselquist et al., 2012). Although many factors influence at which point the plants switch between a pure mycorrhizal strategy and a mixed strategy with both mycorrhizal and nonmycorrhizal roots, the model implies that along environmental gradients there should always be abrupt shifts between very high (≈ 100%) mycorrhizal colonization and much lower colonization. Although not supported by all studies (e.g. Børja & Nilsen, 2009) this threshold behavior agrees with observations of ectomycorrhizal colonization intensity across a wide-ranging data set comprising 125 species and 44 sites (Akhmetzhanova et al., 2012), which were clustered at very high or relatively low values (Fig.5).


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

Franklin O, Näsholm T, Högberg P, Högberg MN - New Phytol. (2014)

Field measurements of ectomycorrhizal colonization intensity, for 125 species and 44 sites in the former Soviet Union (Akhmetzhanova et al., 2012), show high frequency of observations at very high or relatively low colonization intensity and fewer observations at intermediate colonization intensity, as predicted by our model. Statistical testing by k-means cluster analysis separated two clusters centered at high (95%) and low (21%) values with P < 0.0001. The colonization intensity is measured in per cent of maximal colonization intensity, based on the mean number of mycorrhizal root tips per root length for each species at each site, relative to a reference scale (Akhmetzhanova et al., 2012).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4199275&req=5

fig05: Field measurements of ectomycorrhizal colonization intensity, for 125 species and 44 sites in the former Soviet Union (Akhmetzhanova et al., 2012), show high frequency of observations at very high or relatively low colonization intensity and fewer observations at intermediate colonization intensity, as predicted by our model. Statistical testing by k-means cluster analysis separated two clusters centered at high (95%) and low (21%) values with P < 0.0001. The colonization intensity is measured in per cent of maximal colonization intensity, based on the mean number of mycorrhizal root tips per root length for each species at each site, relative to a reference scale (Akhmetzhanova et al., 2012).
Mentions: When soil N availability increases to a level where a nonmycorrhizal strategy can invade, EMF only persist if their utility for a plant matches that of nonmycorrhizal roots, which requires EMF to invest more in N uptake (increase u) than in the absence of a nonmycorrhizal strategy (Fig.3 versus Fig. S2). However, EMF will not increase u more than necessary as this would reduce fitness. For a plant this means a switch from a clear advantage of the mycorrhizal strategy to equal utility of mycorrhizal and nonmycorrhizal roots. At the same time, there exists a u that allows the mycorrhizal strategy to invade a resident nonmycorrhizal strategy. Thus, both root strategies may coexist under further increasing soil N availability until EMF are forced to allocate all resources to N uptake (u→1, leaving nothing for reproductive growth), making the symbiosis unviable. Although mutual invasibility and convergence of the utilities of the alternative root strategies do not imply strictly equal frequency, they suggest that, on average, mycorrhizal and nonmycorrhizal roots coexist in similar proportions. These results agree with the patterns typically observed in gradients of increasing soil N availability: while plant growth gradually increases there is almost complete mycorrhizal root colonization under a range of low soil N availability, followed by coexistence of nonmycorrhizal and mycorrhizal roots, and finally disappearance of EMF (Taylor et al., 2000; Högberg et al., 2003; Nilsson et al., 2005; Kjøller et al., 2012). A corresponding negative trend was also found for soil mycelia where ectomycorrhizal species declined and disappeared (Högberg et al., 2014). Furthermore, because the increasing fungal allocation to N uptake components occurs at the expense of reproductive allocation (increased u), it agrees with empirically observed reductions in fruiting-body (reproductive structures) production at high N additions (Peter et al., 2001; Hasselquist et al., 2012). Although many factors influence at which point the plants switch between a pure mycorrhizal strategy and a mixed strategy with both mycorrhizal and nonmycorrhizal roots, the model implies that along environmental gradients there should always be abrupt shifts between very high (≈ 100%) mycorrhizal colonization and much lower colonization. Although not supported by all studies (e.g. Børja & Nilsen, 2009) this threshold behavior agrees with observations of ectomycorrhizal colonization intensity across a wide-ranging data set comprising 125 species and 44 sites (Akhmetzhanova et al., 2012), which were clustered at very high or relatively low values (Fig.5).

Bottom Line: Ectomycorrhizal symbiosis is omnipresent in boreal forests, where it is assumed to benefit plant growth.Instead, market mechanisms may generate self-stabilization of the mycorrhizal strategy via nitrogen depletion feedback, even if plant growth is ultimately reduced.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.

View Article: PubMed Central - PubMed

Affiliation: IIASA- International Institute for Applied Systems Analysis, A-2361, Laxenburg, Austria.

Show MeSH
Related in: MedlinePlus