Climate change with the associated increase in soil temperature and changes in precipitation exposes forests to increased drought and heat stresses (Easterling
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
Based on global studies, the responses of fine roots to soil warming appear inconsistent (Wang
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?
We performed a global meta-analysis with 149 paired observations from 43 published studies between 1999 and 2020 that investigated fine root trait responses of tree species to various soil-warming magnitudes across the world’s biomes ranging from tropical to boreal (Supplementary data). Data compiled into the present research were taken from either experimental warming or natural gradients; thus the impact of geographic regions were not considered for further statistical analyses. Fine roots as roots with a diameter of < 2 mm were the most commonly measured root size in the available publications, and we included this root sampling category in our meta-analysis. The following fine root traits were extracted from each study: fine root biomass referred to as (FRB, g m-2), and fine root morphological indicators, including diameter (D, mm), specific root length (SRL, m g-1) referred to as root length divided by the dry weight of fine roots, and specific root area (SRA, m2 kg-1), which is known as a clear soil characteristic (Lõhmus
The literature was searched via the Web of Science, Google Scholar, and FRED database using a combination of keywords including “fine roots biomass”, “fine roots morphology or fine root diameter, or D, specific root length or SRL, and specific root area or SRA”, “soil warming or soil temperature” (Supplementary data). The current meta-database includes only publications from studies that reported the warming magnitude and the means, the number of sample sizes/replications, and the standard deviations or standard error of fine-root traits. The present data were directly compiled from tables or extracted from figures by PLOT DIGITIZER (
We applied the following criteria to select appropriate publications: only soil warming manipulation (with control and treatment) data were chosen; control and treatment had the same initial conditions and were reported for the same tree species; the means, standard deviations/errors, and sample sizes/replications of the fine root variables were reported. If treatments were performed at multiple sites or across years in one study, they were considered independent observations.
All statistical analyses were conducted in CMA statistical software, version 3 (Comprehensive Meta-Analysis Version 3). The meta-analysis was performed by calculating the effect size for each study using the standardized mean differences method and determining the sum of the effect sizes.
I2 from the fixed effects model was calculated for quantifying inconsistency (Higgins & Thompson, 2002):
Q is known as the chi-squared statistic, which is used to assess the statistical heterogeneity in the meta-analyses, and df indicates its degrees of freedom (Higgins & Thompson, 2002). If the I2 index was insignificant, the fixed effects model was used. Sensitivity analysis was used to detect unfitting effect sizes in the meta-analysis; if outliers and extreme effects were identified and removed, the analysis was repeated. In this meta-analysis, a statistical index (classic fail-safe N) was used to investigate the publication bias. If the publication bias was detected and non-significant findings were reported, the results of that study were not included in the meta-analysis (if there is no publication bias, the graph is symmetrical, and the amount of scatter around the intervention effect size decreases with increasing sample size). Tree species (deciduous and coniferous) were considered the discrete moderator variable, and soil depth and warming magnitude were used as continuous moderator variables for the meta-regression model.
Compared with the control, soil warming increased FRB (p=0.001, n=42; Figure 1). The effect size for FRB decreased with the increasing magnitude of warming (p=0.00, Table 1; Figure 2A).
Summary of the meta-regression model, P values <0.05 are significant.
Fine root traits | Moderator variables | Tree species | Covariate | Coefficient | Standard Error | 95% Lower | 95% Upper | Z-value | Two-tailed P-value | R2 |
---|---|---|---|---|---|---|---|---|---|---|
FRB | Warming magnitude | Overall | Intercept | 2.13 | 0.581 | 0.99 | 3.27 | 3.67 | 0.00 | 0.28 |
Warming magnitude | -0.53 | 0.178 | -0.87 | -0.18 | -2.99 | 0.00 | ||||
Coniferous | Intercept | 3.21 | 0.796 | 1.64 | 4.77 | 4.03 | 0.00 | 0.56 | ||
Warming magnitude | -0.84 | 0.235 | -1.30 | -0.38 | -3.59 | 0.00 | ||||
Deciduous | Intercept | 1.02 | 0.733 | -0.41 | 2.46 | 1.40 | 0.16 | 0.01 | ||
Warming magnitude | -0.11 | 0.255 | -0.61 | 0.38 | -0.44 | 0.66 | ||||
Soil depth | Overall | Intercept | -0.00 | 0.58 | -1.16 | 1.14 | -0.01 | 0.98 | 0.07 | |
Soil depth | 0.05 | 0.04 | -0.02 | 0.13 | 1.38 | 0.16 | ||||
Coniferous | Intercept | 0.21 | 0.96 | -1.67 | 2.10 | 0.22 | 0.82 | 0.08 | ||
Soil depth | 0.05 | 0.05 | -0.06 | 0.16 | 0.85 | 0.39 | ||||
Deciduous | Intercept | -0.34 | 0.93 | -2.18 | 1.49 | -0.37 | 0.71 | 0.20 | ||
Soil depth | 0.12 | 0.09 | -0.06 | 0.32 | 1.28 | 0.20 | ||||
SRA | Warming magnitude | Overall | Intercept | -1.06 | 1.78 | -4.55 | 2.42 | -0.60 | 0.54 | 0.42 |
Warming magnitude | 0.73 | 0.46 | -0.18 | 1.64 | 1.57 | 0.11 | ||||
Soil depth | Intercept | -1.03 | 1.36 | -3.70 | 1.63 | -0.76 | 0.44 | 0.65 | ||
Soil depth | 0.14 | 0.07 | 0.00 | 0.29 | 1.99 | 0.04 | ||||
SRL | Warming magnitude | Overall | Intercept | -1.06 | 1.78 | -4.55 | 2.42 | -0.60 | 0.54 | 0.42 |
Warming magnitude | 0.73 | 0.46 | -0.18 | 1.64 | 1.57 | 0.11 | ||||
Soil depth | Intercept | -1.03 | 1.36 | -3.70 | 1.63 | -0.76 | 0.44 | 0.65 | ||
0.14 | 0.07 | 0.00 | 0.29 | 1.99 | 0.04 | |||||
D | Warming magnitude | Overall | Intercept | 0.49 | 0.51 | -0.52 | 1.50 | 0.95 | 0.34 | 1.00 |
Warming magnitude | -0.13 | 0.06 | -0.25 | -0.00 | -2.06 | 0.03 | ||||
Soil depth | Intercept | -2.82 | 0.95 | -4.68 | -0.95 | -2.97 | 0.00 | 1.00 | ||
Soil depth | 0.16 | 0.05 | 0.04 | 0.27 | 2.77 | 0.00 |
At the species level, the mean effect size of the warming magnitude on the FRB of coniferous trees was larger than the FRB of deciduous trees (mean effect sizes were 0.69 and 0.57; p=0.06, and p=0.26, respectively; Figure 1). The meta-regression model showed a significant negative effect on coniferous FRB (R2=0.56, p=0.00, Table 1; Figure 2C); with the increase of one unit in warming, the effect size for FRB of the coniferous trees decreased by 0.84 units. By contrast, the warming magnitude did not significantly affect the FRB of the deciduous trees (R2=0.01, p=0.65, Table 1; Figure 2E). The Q statistic test revealed that 56% of the total heterogeneity is explained by the warming magnitude in the primary research of conifers compared to only 1% in the study of deciduous species. In general, tree species did not explain a large share of heterogeneity (Table 1).
Further, the effect size for FRB did not vary with increasing soil depth as a moderator variable, neither in coniferous nor deciduous tree species (Table 1; Figure 2 B, D, and F).
Fine root morphological traits showed no significant responses to soil warming (i.e. SRL: p=0.15, n=12; SRA: p=0.08, n=6; D: p=0.38, n=5), (Figure 1). With the increasing magnitude of warming and soil depth, the effect size for SRL did not change in either deciduous or coniferous species (Table 1). Only soil depth had a significant positive effect on the effect sizes of SRA and fine root D (Table 1). With an increase of one centimeter in soil depth, the effect size increased by 0.14 units in SRA and by 0.16 in root D (p=0.04, p=0.00, respectively; Table 1). According to the R2 values of the regression model, soil depth explained a large share of total heterogeneity in both morphological indicators (Table 1).
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
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
Furthermore, the heterogeneity of fine-root responses to soil and climate conditions may result from interactions with different environmental factors (Zhang
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: