The impact of soil warming on fine root trait responses of trees, deciduous vs. coniferous: a meta-analysis

Climate change with the associated increase in soil temperature and changes in precipitation exposes forests to increased drought and heat stresses (Easterling et al., 2000; IPCC, 2014). Soil warming is one of the key limiting factors for forest growth and productivity, affecting soil carbon (C) cycling and storage (Melillo et al., 2011; Kilpeläinen et al., 2022). The resilience of forest ecosystems and functioning depends largely on belowground processes, which are mainly regulated by tree fine roots (i.e., roots < 2 mm in diameter) and their functional traits (Freschet et al., 2017). Yet little is known about the sensitivity of forest ecosystems, especially tree fine roots, to the predicted warming, and existing findings are extremely contradictory (Reich et al., 2022; Kwatcho Kengdo et al., 2022). Therefore, understanding the detailed mechanisms of the trees’ root adaptations to soil temperature changes is crucial for evaluating the functionality and resilience of different tree species to the ongoing soil warming episodes.

Fine root systems exhibit plastic responses to changing environmental conditions through modifications in fine root biomass (FRB) and its morphological traits to improve soil resource uptake and tree performance (Weemstra et al., 2020). The morphological traits of fine roots indicate plant adaptation and ecosystem functions in response to environmental shifts determining plants’ water and nutrient acquisition strategies (Nikolova et al., 2020). However, better elucidation of the linkages between root morphology, biomass allocation, and their function needs to be assessed (Iversen, 2014). Fine root diameter (D), specific root length (SRL), and specific root area (SRA) are commonly quantified in the literature and are known to be associated with critical forest processes, such as soil resource acquisition, and C cycling (Makita et al., 2012; Weemstra et al., 2020).

Based on global studies, the responses of fine roots to soil warming appear inconsistent (Wang et al., 2021; Kwatcho Kengdo et al., 2022). FRB has been found to increase (Leppälammi-Kujansuu et al., 2013) or decrease (Melillo et al., 2011; Zhou et al., 2011) with various soil temperatures of different forest biomes, associated with soil nitrogen (N) availability. In a long-term soil warming experiment, Parts et al. (2019) revealed that spruce fine roots were longer, and their SRL and SRA increased toward warmer soils. Wang et al. (2021), in their meta-analysis, found that fine root morphological traits were unaffected by the soil warming treatment, whereas FRB increased in warmer soils across the studied terrestrial ecosystems. However, warming-induced responses of fine root traits could depend upon potential interaction with other environmental factors (e.g. soil water content, N availability, soil depth, and meteorological condition) (Bai et al., 2013; Wang et al., 2021). Besides, fine root trait responses vary widely among tree species, maintaining the tree’s specific acclimation to changing environmental shifts (Nikolova et al., 2020; Rezapour et al., 2022). For example, deciduous species having thinner fine roots and lower soil organic C stocks are favored over coniferous species for their resilience toward ongoing climate change (Jandl et al., 2021).

Here, we collected data on fine root biomass and morphology under changing soil warming experiments from literature across different biomes to examine the global patterns in the responses of trees’ fine roots to soil warming changes considering various warming magnitudes and soil depth. Also, comparing deciduous and coniferous tree species in similar experimental settings will contribute to a better understanding of the belowground responses of forests with different tree species. By performing a meta-analysis, the following research questions were addressed. (I) Whether and how fine roots adjust their biomass and morphology to changes in soil warming? (II) Whether and how fine roots of different tree species (deciduous vs. coniferous) respond to various soil warming magnitudes?

The present meta-analysis demonstrates considerable fine-root biomass alteration but not morphological plasticity to soil warming in deciduous and coniferous trees at the global scale. This finding was consistent with previous studies (Lin et al., 2010; Wang et al., 2021) and may be related to the higher fine root growth rate and production resulting from the enhanced photosynthetic rates in warmer soils (Malhotra et al., 2020). However, our results revealed that warming effects on fine-root biomass decreased with the increasing magnitude of warming, which is probably a consequence of increased root mortality at elevated temperatures (Wang et al., 2021). Moreover, we found that the observed FRB warming responses varied among deciduous and coniferous trees, which is in line with the previously reported species-specific fine root trait responses to changing environments (Leuschner & Hertel, 2003; Förster et al., 2021; Rezapour et al., 2022).

In contrast to biomass, we found that fine root morphological traits (i.e. SRL, SRA, and D) were unresponsive to soil warming. Contrary to our findings, others have shown that fine root morphology is responsive to higher soil temperatures (Feng et al., 2017; Parts et al., 2019). For example, Björk et al. (2007) observed that fine root SRA and SRL increased under warmer environments to optimize soil resource acquisition and maintain growth. Moreover, the insignificant responses of fine root morphological traits observed in our study could be ascribed to limited data availability and the lower morphological sample numbers compared to the biomass data. Therefore, a further study with sufficient observations is required to understand warming-induced changes in fine root morphology better.

Furthermore, the heterogeneity of fine-root responses to soil and climate conditions may result from interactions with different environmental factors (Zhang et al., 2018) and vary across species (Förster et al., 2021). In this regard, we assume that an interaction between soil warming and soil depth, varied with other soil properties (e.g. moisture, N content, and acidity), resulting in fine root responses. For example, in our study, soil depth affected fine root SRA, and D, probably due to acclimation to resource uptake induced by warming and altered soil water content (Weemstra et al., 2020; Kwatcho Kengdo et al., 2022). Similar to our results, several studies found plasticity in fine root morphological traits to soil depth, although their responses differed between deciduous and coniferous species (Leuschner et al., 2004; Kirfel et al., 2019). It has been reported that beech stands produce fine roots with higher SRA and SRL and lower root tissue density in the organic layer than in the mineral soil layer. In contrast, pine stands exhibited a similar root morphology in both layers (Förster et al., 2021). Kirfel et al. (2019) consistently observed fine roots with higher SRA and SRL, implying a greater nutrient capacity in the organic layer than in the mineral soil.

In this context, we highlight that the warming responses of the fine root functional traits of trees still need a more detailed assessment considering the complex interaction of soil temperature with its potential environmental modifiers.

The present meta-analysis suggests that soil warming may influence trees to allocate more biomass to fine roots. In contrast, the morphological plasticity of fine roots was less influenced by increased soil temperatures. However, our study points out the necessity of further multi-factor change experiments to assess global warming impacts on forest ecosystems, including interactive effects of environmental factors. Our results have shown that the fine roots responses to soil warming are species-specific. These results provide insight into how forest ecosystems respond to environmental changes, with implications for future forest ecosystem modelling.

The data set used for the present meta-analysis and correspondence references is provided in the supplementary file. Available online: https://mi.emu.ee/et/teadusinfo/metsanduslikud-uurimused/contents/2022/vol-77/.