scholarly journals The Mycorrhizal Tragedy of the Commons

Author(s):  
Nils Henriksson ◽  
Oskar Franklin ◽  
Lasse Tarvainen ◽  
John Marshall ◽  
Judith Lundberg-Felten ◽  
...  

The mycorrhizal symbiosis is ubiquitous in boreal forests. Trees and plants provide their fungal partners with photosynthetic carbon in exchange for soil nutrients like nitrogen, which is critical to the growth and survival of the plants. But plant carbon allocation to mycorrhizal symbionts can also fuel nitrogen immobilization, hampering tree growth. Here we present results from field and greenhouse experiments combined with mathematical modelling, showing that mycorrhizal fungi can be simultaneously mutualistic to an individual tree and parasitic to the networked community of trees. Mycorrhizal networks connect multiple plants and fungi, and we show that each tree gains additional nitrogen at the expense of its neighbors by supplying more carbon to the fungi. But this additional carbon supply eventually aggravates nitrogen immobilization in the shared fungal biomass. Individual trees may thus independently benefit from increasing their carbon investment to mycorrhiza, while causing a decline in nitrogen availability for the whole plant community. We illustrate the evolutionary underpinnings of this situation by drawing on the analogous the tragedy of the commons, and explain how rising atmospheric CO2 may lead to greater nitrogen immobilization in the future.

2021 ◽  
Author(s):  
Nils Henriksson ◽  
Oskar Franklin ◽  
Lasse Tarvainen ◽  
John Marshall ◽  
Judith Lundberg-Felten ◽  
...  

<p>Ectomycorrhizal fungi (EMF) play a key role in the cycling of nitrogen (N) and carbon (C) in boreal forests. Trees receive growth-limiting N in exchange for allocating C to their mycorrhizal symbionts, but supplying the fungi with C can also cause N immobilization, which hampers tree growth. We present results from field and greenhouse experiments combined with mathematical modelling, showing that these are not conflicting outcomes.</p><p>Under N limitation, which is the general case in boreal forests, the plant host has been observed to continue supplying its ectomycorrhizal partner with C, and even increasing this C investment, while the fungus reduces mobilization of N to its host (Corrêa et al. 2008, 2010). N is thus withheld under conditions of limiting availability, and the host tree cannot unlock it by supplying the EMF with more C, because such an investment results in further diminishing N returns. Critical to this question is the observation that more than one fungus can form mycorrhiza on a given tree and that several trees can be connected to a given fungal individual (Southworth et al. 2005).</p><p>We hypothesize that plants sharing common ectomycorrhizal symbionts compete with each other for N by exporting C to the EMF network, and vice versa for a fungus. The fungi making up the EMF network export N to hosts if it is absorbed in excess of their own growth demand, which is limited by C; Exporting more than this would reduce their growth, exporting less would reduce their competitiveness for plant C (Näsholm 2013, Franklin 2014). This hypothesis has specific and predictable implications for relationship between plant C export to EMF and N uptake: At the community level, increasing plant C supply to EMF would increase both fungal N uptake and N use, but as soil N availability gradually becomes limiting, uptake should saturate while EMF N use continued to increase, leading to declining N export to plants.</p><p>We conducted two experiments, one in potted mesocosms and the other in a boreal forest setting. Belowground C flux was reduced by shading and/or stem strangling, which is a treatment whereby the flow of C to the root system is physically restricted by blocking transport through the phloem in the stem (Björkman 1944; Henriksson et al. 2015). Strangling a subset of seedlings growing in the same pot accomplishes two things: 1) the total belowground C flux is decreased, and 2) each seedling’s relative contribution to that flux is altered.</p><p>Based on measurements and mathematical modelling, we conclude that belowground C allocation by trees can indeed fuel N immobilization, reducing the amount of N to be distributed among the trees. But we also found that individual trees received nutritional benefits in proportion to their C contribution to the fungal network. We illustrate the evolutionary underpinnings of this situation by drawing on the analogous tragedy of the commons (Hardin 1968), where the shared mycorrhizal network is the commons, and explain how rising atmospheric CO<sub>2</sub> may lead to greater nitrogen immobilization in the future.</p>


2020 ◽  
Author(s):  
Oskar Franklin ◽  
Torgny Näsholm ◽  
Nils Henriksson

<p><strong>The mycorrhizal tragedy of the commons</strong></p><p>It is increasingly recognized that plant C allocation to mycorrhizal symbionts plays a critical role for plant nutrition and the future global CO<sub>2</sub> fertilization effect on plants (Terrer et al., 2019). At the same time its future impacts are hard to predict because we do not fully understand the mechanisms underlying the symbiosis. The traditional view of mycorrhizal symbiosis always helping plants has been challenged by observations of negative effects, e.g. on tree N uptake (Näsholm et al., 2013), which makes it difficult to understand why the symbiosis has evolved and why it is so widespread.</p><p>We propose, and tested, a theory explaining the contrasting findings by showing that mycorrhizal symbiosis can be both mutualistic and parasitic at the same time. Plants and fungi are connected in a mycorrhizal network where each fungus has multiple plant partners and vice versa. Each plant can gain additional N at the expense of the other plants by supplying more C to the fungi, i.e. paying a higher C price for N. At the same time the additional C supply increases N immobilization in fungal biomass, which reduces the total N export to all plants. Thus, an individual plant can gain N at the expense of its neighbors while the negative side effects are shared among all, resulting in a tragedy of the commons effect that reduces plant N uptake and drives N immobilization in the soil.</p><p>While some observations support this hypothesis, it had not yet been thoroughly tested experimentally – until now. Based on laboratory and field experiments in boreal pine forest we tested both key components of this hypothesis - individual level mutualism and the community parasitism (decline in plant N uptake). We also estimated the strength of the fungal discrimination among its plant partners, which drives the competitive C for N trading. Finally, we highlight potential consequences of these mechanisms for boreal forest C allocation and responses to rising CO<sub>2</sub>.</p><p><strong>References</strong></p><p>Näsholm, T. et al., 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytologist, 198(1): 214-221.</p><p>Terrer, C. et al., 2019. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nature Climate Change, 9(9): 684-689.</p>


2021 ◽  
Vol 4 ◽  
Author(s):  
Muhammad Usman ◽  
Tania Ho-Plágaro ◽  
Hannah E. R. Frank ◽  
Monica Calvo-Polanco ◽  
Isabelle Gaillard ◽  
...  

Global climate changes have serious consequences on natural ecosystems and cause diverse environmental abiotic stressors that negatively affect plant growth and development. Trees are dependent on their symbiosis with mycorrhizal fungi, as the hyphal network significantly improves the uptake of water and essential mineral nutrients by colonized roots. A number of recent studies has enhanced our knowledge on the functions of mycorrhizal associations between fungi and plant roots. Moreover, a series of timely studies have investigated the impact and benefit of root symbioses on the adaptation of plants to climate change-associated stressors. Trees in temperate and boreal forests are increasingly exposed to adverse environmental conditions, thus affecting their durable growth. In this mini-review, we focus our attention on the role mycorrhizal symbioses play in attenuating abiotic stressors imposed on trees facing climatic changes, such as high temperatures, drought, salinity, and flooding.


2014 ◽  
Author(s):  
David J. Hardisty ◽  
Howard Kunreuther ◽  
David H. Krantz ◽  
Poonam Arora

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