A meta-analysis of the effects of climate change on the mutualism between plants and arbuscular mycorrhizal fungi

Abstract

Climate change and other anthropogenic activities have the potential to alter the dynamics of resource exchange in the mutualistic symbiosis between plants and mycorrhizal fungi, potentially altering its stability. Arbuscular mycorrhizal (AM) fungi, which interact with most plant species, are less cold-tolerant than other groups of fungi; warming might therefore lead to increased fungal-mediated nutrient transfers to plants, which could strengthen the mutualism. By stimulating photosynthesis, rising CO₂ could reduce the carbon cost of supporting AM fungi, which may also strengthen the mutualism. Furthermore, rising temperature and CO₂ could have stronger effects on the mutualism in wild plants than in domesticated plants because the process of domestication can reduce the dependence of plants on mycorrhizal fungi. We conducted a multi-level random effects meta-analysis of experiments that quantified the strength of the mutualism as plant growth response to AM fungal inoculation (i.e., mycorrhizal growth response) under contrasting temperature and CO₂ treatments that spanned the Last Glacial Maximum (LGM) to those expected with future climate change. We tested predictions using a three-level mixed effects meta-regression model with temperature or CO₂, domestication status and their interaction as moderators. Increases from subambient to ambient temperature stimulated mycorrhizal growth response only for wild, but not for domesticated plant species. An increase from ambient to superambient temperature stimulated mycorrhizal growth response in both wild and domesticated plants, but the overall temperature effect was not statistically significant. By contrast, increased CO₂ concentration, either from subambient to ambient or ambient to super ambient levels, did not affect mycorrhizal growth response in wild or domesticated plants. These results suggest the mutualism between wild plants and AM fungi was likely strengthened as temperature rose from the past to the present and that forecasted warming due to climate change may have modest positive effects on the mutualistic responses of plants to AM fungi. Mutualistic benefits obtained by plants from AM fungi may not have been altered by atmospheric CO₂ increases from the past to the present, nor are they likely to be affected by a forecasted CO₂ increase. This meta-analysis also identified gaps in the literature. In particular, (i) a large majority of studies that examined temperature effects on the mutualism focus on domesticated species (>80% of all trials) and (ii) very few studies examine how rising temperature and CO₂, or other anthropogenic effects, interact to influence the mutualism. Therefore, to predict the stability of the mycorrhizal mutualism in the Anthropocene, future work should prioritize wild plant species as study subjects and focus on identifying how climate change factors and other human activities interact to affect plant responses to AM fungi.

Keywords: climate change; mutualism; nitrogen; phosphorus; plant biomass; root colonization.