This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as doi:
10.1029/2017JG004308
The responses of forest fine root biomass/necromass ratio to environmental factors depend on mycorrhizal type and latitudinal region
Cunguo Wang1, Zhao Chen1, Hong Yin1, Wei Guo1, Ying Cao1, Guojiao Wang1, Bei Sun1, Xuefei Yan1, Jiandong Li1, Tian-Hong Zhao1*, Ivano Brunner2, Guanhua Dai3, Yixiang Zheng4, Yiguo Zheng5, Weizhong Zu5 and Mai-He Li2,6*
1College of Agronomy, Shenyang Agricultural University, Shenyang, China,
2Swiss Federal Research Institute WSL, Zuercherstrasse, Birmensdorf, Switzerland,
3Research Station of Changbai Mountain Forest Ecosystems, Chinese Academy of Sciences, Antu, China,
4Forest Fire Protection Headquarters, Changbai Mountain Protection and Development Zone, Antu, China,
5Natural Conservation Management Center, Changbai Mountain Protection and Development Zone, Antu, China
6School of Geographical Sciences, Northeast Normal University, Changchun, China
Corresponding authors: Tian-Hong Zhao (zth1999@163.com); Mai-He Li (maihe.li@wsl.ch)
Key Points:
Fine root biomass/necromass (B/N) ratio of forest ecosystems are synthesized at a global scale.
Arbuscular mycorrhizas and ectomycorrhizas forests have similar average fine root B/N ratio, and the average B/N ratio is higher in temperate forests than in tropical and boreal forests.
Mycorrhizal types and latitudinal regions influence the fine root B/N responses to climate, topography, edaphic and stand properties.
This document is the accepted version of: Wang, C., Chen, Z., Yin, H., Guo, W., Cao, Y., Wang, G., … Li, M. -H. (2018). The responses of forest fine root biomass/necromass ratio to environmental factors depend on mycorrhizal type and latitudinal region. Journal of Geophysical Research G: Biogeosciences.
http://doi.org/10.1029/2017JG004308
Abstract
Fine root (≤ 2 mm in diameter) biomass/necromass (B/N) ratio, representing many dynamic key root parameters, can serve as a powerful measure of root vitality. Based on a global synthesis of fine root biomass and necromass in forest ecosystems, we describe a framework for recognizing responses of B/N ratio to biotic (e.g. mycorrhizal type) and abiotic (e.g.
latitudinal region) characteristics. Arbuscular mycorrhizas (AM) and ectomycorrhizas (ECM) forests had similar average B/N ratios (3.28 vs. 3.23). AM forest B/N ratio decreased with increasing altitude, stand density, tree age and soil carbon/nitrogen ratio (C/N), but increased with soil pH. In contrast, ECM forest B/N ratio increased with increasing mean annual
precipitation (MAP), altitude, stand density, but decreased with tree age. The average B/N ratio was higher in temperate forests (4.39) than in tropical (2.97) and boreal forests (2.40). The B/N ratio was relatively stable in temperate forests irrespective of changes in biotic and abiotic factors. In tropical forest, the B/N ratio was sensitive to mean annual temperature, altitude, soil C/N ratio and pH, whereas in boreal forests it was more sensitive to MAP, stand density and tree age. The late-successional forest B/N ratio was closely aligned with biotic and abiotic factors. Our analysis revealed that the relationships of B/N ratio with climate, topography, edaphic and stand characteristics were dependent on mycorrhizal types and latitudinal regions.
These findings provide a basis for large-scale prediction of fine root dynamics and for better understanding of belowground processes of global forest ecosystems in a changing world.
1 Introduction
Fine roots are very dynamic and have a fast turnover and thus contribute to the large flux of dead roots to the forest soils (McCormack et al., 2013). Fine root production, death and decomposition collectively determine the total size of a root population that is fine root biomass (the living fine roots) and necromass (the dead fine roots). Both parameters indicate how trees interact with their environments (Zang et al., 2011; McCormack et al., 2014). The biomass/necromass (B/N) ratio of fine roots can be a parameter of interest for assessing the way the forest ecosystem functions (Bakker, 1999). Since fine root B/N ratio is the balance among production, mortality of living fine roots and decomposition of dead fine roots, the factors that influence these processes should be considered to indentify the underlying
mechanisms (Powers & Peréz-Aviles, 2013). In addition, the B/N ratio is well correlated with a change of the amount of root tips (Persson, 1978), which are metabolic “hot spots” and play most active roles in nutrient and water uptake (Pregitzer, 2003). Thus, the B/N ratio also can give an indication on the absorptive capacity of the fine root systems (Clemensson-Lindell &
Persson, 1995). Actually, it has been applied by various scientists as a powerful measure of root vitality, even tree vitality (Godbold et al., 2003; Puhe, 2003; Leuschner et al., 2004;
Persson & Stadenberg, 2010).
The large majority of tree species possess mycorrhizas, a mutualistic relationship between plant roots and fungi (Bonfante & Genre, 2010), thus, forests can be grouped based on the mycorrhizal associations of the dominant trees. Arbuscular mycorrhizas (AM) and
ectomycorrhizas (ECM) are the most geographically widespread mycorrhizal groups (Read, 1991). The previous studies have showed that ECM and AM trees can possibly influence fine root morphology and architecture (Comas et al., 2014), leading to various nutrient economies (Lin et al., 2017). Some ECM trees obviously produce low quality roots that decompose slower relative to AM tree roots (Taylor et al., 2016). Consequently, soils in forests dominated by ECM trees have relatively more organic nitrogen than forests dominated by AM trees (Midgley & Phillips, 2014). ECM species are thought to be more efficient in terms of nitrogen acquisition and AM species in phosphorus acquisition (Kubisch et al., 2016).
Such differences may also explain why ECM trees dominate cool-temperate and boreal forests and AM trees are much more abundant in tropical and sub-tropical forests (Lang et al., 2011). However, as an indicator of root vitality, it is not known whether AM and ECM trees differ in their fine root B/N ratio, and how the ratios of the two mycorrhizal types vary along with climatic, edaphic and stand factors.
Forest ecosystems are frequently ranked along natural climatic-zone groupings such as boreal, temperate and tropical for comparisons of structure and function (Keith et al., 2009).
Temperate moist forests, occurring where temperatures are cool and precipitation is moderately high, have the highest biomass carbon stocks (Keith et al., 2009). Tropical, temperate and boreal forests diversely influence climate through physical, chemical and biological processes, and have different responses to the pressure from the global climate change (Bonan, 2008). The low temperature in boreal forests, which limits microbial activity, restrains fine root decomposition (Silver & Miya, 2001), which then results in greater
accumulation of dead fine roots compared to temperate or tropical forests, where higher temperatures may accelerate fine root mortality (Gill & Jackson, 2000). In general, it is observed that in tropical forests, regardless of the mycorrhizal types, a more open and rapid nitrogen cycling occurs (Corrales et al., 2016; Lin et al., 2017). Therefore, different soil nutrient availabilities and physicochemical properties will strongly influence tree fine root carbon allocation strategies in the different climate regions (Cairns et al., 1997). Additionally, seasonal drought in tropical forests could be a key factor for root death and turnover, and it
could signal roots to growth deeper in order to access deep soil water and/or nutrients (Yavitt
& Wright, 2001). Thus, the B/N ratio of forest ecosystem roots probably varies with climate regions.
Available information in the literature on fine root B/N ratio from measurements in forests is substantial (Majdi & Persson, 1993; Persson & Stadenberg, 2010). However, to our
knowledge, no study has tried to reveal the relationships of forest fine root B/N ratio with climate, soil, stand and geographical characteristics, as well as mycorrhizal types on a global scale, given the great indicative importance of fine root B/N ratio for belowground dynamics and further for responses of forest ecosystem carbon and nutrient cycles to further climatic change (Bakker, 1999; Persson & Stadenberg, 2010). The main objectives of this study were 1) to determine differences in fine root B/N ratios between ECM and AM forests and among boreal, temperate and tropical forests and 2) to develop a framework including biotic factors (e.g. stand density and tree age) and abiotic factors (e.g. climatic and edaphic) for revealing the possible influence factors on the variation of the fine root B/N ratio in global forest ecosystems.
2 Materials and Methods
2.1 Data collection
In order to obtain a global view on fine root B/N ratio, we compiled 136 papers that had data of both living and dead fine root mass, which all sourced from roots with diameter ≤ 2 mm in diameter (A list of data sources is found in Appendix 1). The 136 studies represented 169 forest sites (Figure S1), which contained a broad range of biotic, climatic and topography factors with tree ages ranging from 5 to 350 years, mean annual precipitation from 269 to 7500 mm, mean annual temperature from -7.3 to 29.3°C and altitude above sea level from 16 to 4050 m. We used GetData Graph Digitizer 2.26 to extract the data in studies where only graphical data were presented. If the sampling was conducted for multiple dates within the same stand, the average value was used. In cases where samplings included several stands, the data were treated separately. Climatic variables (mean annual temperature and mean annual precipitation) were recorded for each site. When not supplied directly in original reports, mean annual temperature and mean annual precipitation were obtained from the CRU TS 2.1 data set using site latitude and longitude (Mitchell & Jones, 2005). Several stand variables contained dominant tree species, tree age (year), stand density (no. ha-1), sampling depth (cm), soil carbon/nitrogen ratio (C/N) and pH as well as altitude of sampling sites (m).
We excluded the studies conducted in fertilized systems, pots or greenhouses. The sampled forests were classified into boreal (latitudes > 46° north or south), tropical (latitudes < 23.5°
north or south) and temperate (all regions excluding the boreal and tropical) forests. For mycorrhizal classification, forests were grouped into AM and ECM forests based on the mycorrhizal type of dominant tree species (Wang & Qiu, 2006; Brundrett, 2009). Moreover, forests were also classified into early-successional (including Betula, Pinus and Populus) and late-successional stands (including Fagus, Picea and Quercus)(Yuan & Chen, 2010), which both were dominated by ECM trees.
2.2 Statistical analysis
The original data were standardized to reduce skewness by natural logarithm-transformation prior to statistical analyses. One-way analysis of variance (ANOVA) was used to test the differences of fine root B/N ratio between AM and ECM forests and among boreal, temperate and tropical forests, as well as between early- and late-successional forests followed by Tukey’s post hoc comparisons when p < 0.05. Alternatively, we also run an ANCOVA model to analyze the effects of latitudinal region (boreal vs. temperate vs. tropical) and mycorrhizal type (AM vs. ECM) on fine B/N ratio. Moreover, a principal component analysis (PCA) was employed on the correlations among fine root B/N ratio, climate, altitude, stand and edaphic factors. We performed Pearson correlation analysis to determine the bivariate relationships between fine root B/N ratio and climate, latitude, altitude, stand and edaphic variables. All statistical analyses were conducted with R 3.3.3 (R Core Team, 2017).
3 Results
3.1 Fine root B/N ratio
There was no difference in the average fine root B/N ratio between AM and ECM forests (Table 1), while fine root B/N ratio in temperate forests was about 1.8 and 1.5 times higher than boreal and tropical forests, respectively (Table 1). Moreover, the average tree age of ECM forests was 1.9 times greater than AM forests. The stands dominated by AM forests had higher mean annual temperature, precipitation and soil pH, but lower soil C/N ratio compared to the ones dominated by ECM forests (Table 1). The significant differences between AM and ECM forests were found on tree age within the tropical region, altitude within the
temperate region, soil C/N ratio within the boreal region (Table 1). There were no differences in average B/N ratio, stand, environmental and edaphic parameters except for tree age
between stands dominated by early- and late-successional species. Tree age was higher in stands dominated by late-successional species than those by early-successional species (Table 2). Our results of ANCOVA indicated significant interactions of latitudinal region with mean annual precipitation (Table S1), stand density (Table S4), as well as mycorrhizal type with mean annual temperature (Table S2), altitude (Table S3), soil C/N ratio (Table S6) and pH (Table S7) on fine root B/N ratio. Principal component analysis showed that the first two axes accounted for 24.8% and 17.1 % of the total variation, respectively, with mean annual
temperature, precipitation, tree age and soil C/N ratio on the first axis and the other variables on the second axis (Figure 1).
3.2 Responses of fine root B/N ratio to environmental factors
Significant positive relationships were observed between fine root B/N ratio and mean annual precipitation in ECM forests and boreal forests (Figure 2a, b). Mean annual temperature was only significantly and positively associated with fine root B/N ratio of tropical forests (Figure 2d). Fine root B/N ratio significantly ascended in AM forests, whereas descended in ECM forests from low to high latitude (Figure 3a, b). Fine root B/N ratio greatly was increased in ECM forests and boreal forests, but was significantly decreased in AM forests and tropical forests with increasing altitude and stand density (Figures 3c, d and 4a, b). There were decreasing trends of fine root B/N ratio in the two mycorrhizal types and in boreal forests with increasing tree age (Figure 4c, d). AM forest and tropical forest fine root B/N ratio was negatively correlated with soil C/N ratio but positively correlated with soil pH (Figure 5). In contrast, ECM forest fine root B/N ratio was not related with soil C/N ratio and pH (Figure 5a, c). Late-successional forest B/N ratio showed significant increases with mean annual precipitation, altitude, and stand density, but decreases with latitude and tree age (Table 3).
For the early-successional forests there was a significant negative relationship only between B/N ratio and soil pH (Table 3). Furthermore, temperate forests did not change fine root B/N ratio along with the changing of climatic, edaphic and stand factors (Figures 2-5).
4 Discussion
Global information on fine root traits is particularly important to advance our understanding and to predict plant and ecosystem processes under changing environmental conditions (McCormack et al., 2017). The fine root B/N ratio in forest ecosystems combines many important ecological processes including production, mortality and decomposition of fine roots, and can be served as a powerful metric for identifying the absorptive capacity of fine
root systems (Persson & Stadenberg, 2010; Zang et al., 2011). Consequently, it is necessary to use the extensive literature on fine root biomass and necromass to elucidate large-scale variation characteristics of B/N ratio and link it with tree mycorrhizal traits and
environmental conditions (Iversen et al., 2017). This analysis is the first global assessment of fine root B/N ratio across tropical, temperate and boreal regions to develop a framework including climatic, altitude, edaphic and stand factors that account for the dynamic of fine roots of forest ecosystems. We found that changes in fine root B/N ratio along with gradients of abiotic and biotic factors were dependent on mycorrhizal types (AM vs. ECM) and
latitudinal regions (boreal vs. temperate vs. tropical).
4.1 Relationships between fine root B/N ratio and soil factors
In contradiction to our hypothesis, the AM forests had similar average fine root B/N ratios as ECM forests (Table 1), however, we observed contrasting responses of AM and ECM forest fine roots to the changes of climate, altitude, edaphic and stand factors (Figures 2-5). We conducted a principal component analysis and identified two primary dimensions in which soil pH and fine root B/N ratio had the highest scores on the second ordination axis (Figure 1). The AM forest fine root B/N ratio increased with increasing soil pH (Figure 5c). Soil acidity greatly determines the fungal symbiont and the functional effectiveness of
mycorrhizas (Danielson & Visser, 1989). It has been hypothesized that B/N ratio is linked with root vitality, so we can presume that lower fine root B/N with lower pH in AM forests indicates decreased nutrient and water uptake ability. During acidification, metals, especially aluminum, can exert toxic effects to trees by reducing fine root function and inhibiting nutrient uptake (Persson et al., 1995). Furthermore, soil acidity affects production and turnover of fine roots (Ostonen et al., 2007). Under acidic conditions fine roots have to be renewed more often to maintain their resource exploiting function, higher turnover rates and shorter life spans (Godbold et al., 2003; Richter et al., 2013), characterized by a reduced B/N ratio of fine roots in AM forests (Figure 5c).
More surprising was the finding that fine root B/N ratio for ECM forests maintained stable with soil pH (Figure 5c). The stands dominated by ECM trees had lower soil pH than those dominated by AM trees (Table 1). ECM and AM forests typically predominate under distinctive soil conditions, and their different relationships of fine root B/N ratios with soil pH may highlight fundamental differences in the behavior between the two different types of mycorrhizal fungi (AM vs. ECM). Fine roots of AM trees seem to be particularly sensitive to H-ions in acidic soil, whereas ECM roots may be more tolerant (Becerra et al., 2005;
Soudzilovskaia et al., 2015). Generally, ECM fungi are generally considered to be acidophilic (e.g. Cenococcum geophilum) and tolerate a range of pH from 3 to 5 (Becerra et al., 2005).
An increase in root colonization intensity by ECM fungi in acidic soils was observed by (Soudzilovskaia et al., 2015). Thus, ECM forests develop better than AM forests under low soil pH conditions, which could be attributed to ECM which provide a protective effect on the tree root systems (Danielson & Visser, 1989).
The previous meta-analysis was consistent with our results with ECM forests having higher average soil C/N ratios than AM forests (Averill et al., 2014; Lin et al., 2017). AM forests with lower soil C/N ratios tend to dominate in warm and wet habitats (Table 1) where nitrogen mineralization and nitrification processes are rapid (Midgley & Phillips, 2014).
Increased soil C/N ratios indicate nitrogen limitation of decomposer activity and, thus, low mineralization rates, which can explain subsequent accumulation of larger amounts of fine root necromass (Leuschner et al., 2007) and lower fine root B/N ratios in AM forest as shown in the present study (Figure 5a). In contrast, ECM trees are primarily distributed in cool forests or at high latitudinal region (Table 1), which might be attributed to the competitive advantage of ECM fungi over AM fungi in acquiring nitrogen directly from organic matter with the help of mycorrhizal fungi (Phillips et al., 2013; Lindahl & Tunlid, 2015).
Furthermore, mycorrhizal colonization rate is generally higher in ECM than in AM species, supporting the notion that ECM species rely heavily on mycorrhizal fungi for resource uptake (Guo et al., 2008; Chen et al., 2016; Cheeke et al., 2017; Chen et al., 2018). Moreover, litter including dead fine roots with a low nitrogen concentration produced in ECM forests in boreal and temperate forests hardly decompose due to strongly limiting soil biological processes in that cold climate (Soudzilovskaia et al., 2015; Lin et al., 2017). The litter under such harsh conditions is only transformed to raw acid humus (Brunner & Sperisen, 2013).
Based on the differences in their adaptations and distribution patterns, AM and ECM trees may be expected to respond differently to soil factors (Phillips et al., 2013). Therefore, the stand edaphic characteristics and their correlations with fine root B/N ratios seem to be mycorrhizal specific. Although only soil C/N ratio and pH are included in our analysis, they are important factors for carbon and nitrogen cycling processes via their direct influence on nutrient availability in the soil (Genenger et al., 2003; Högberg et al., 2007). Moving forward, the present results suggest that future research should focus on additional soil parameters that permit a complete comprehension of the ECM-AM-soil complex (Bennett et al., 2017).
4.2 Relationships between fine root B/N ratio and stand factors
Tree-age-related variation in fine roots is important for understanding complex carbon dynamics during stand development (Rosenvald et al., 2013). However, only a few studies have dealt with the influence of forest ageing on fine root B/N ratio. In this synthesis, we found a decreasing trend of fine root B/N ratio with increasing tree age for both AM and ECM forests (Figure 4c). Actually, the changes of fine root B/N ratio might be closely connected with changes in the nutrient and water demands of trees during their growth and development of the stand. Young forest stands in the most dynamic stage of tree growth have higher nutrient and water requirements, and, therefore, they need to build-up their root system quickly (Børja et al., 2008), indicating a higher fine root B/N ratio. The senescence of pioneer trees and, along with it, the increasing probabilities of insect (Stevens et al., 2002) and/or wind damage with tree age lead to a rising trend of root damage (Schulze et al., 2005; Yuan
& Chen, 2012). Thus, young stands are rather dominated by living fine roots, whereas old stands are dominated by a large pool of dead fine roots, which might be visualized by a decreased B/N ratio of fine roots as the forest stand gets older (Clemensson-Lindell &
Persson, 1995; Majdi & Persson, 1995). Furthermore, for naturally forests, competition among trees is higher in younger stands, where stand density is higher, leading to stronger root competition (Rosenvald et al., 2013). When stand age increases, stand density decreases and the mean tree dimensions (diameter at breast height) considerably increases (Figure S2).
Hence, stand density of forest stands seems to be an important factor influencing fine root growth dynamics of the stand (Børja et al., 2008). We also found clear hints for an important influence of the mycorrhizal types on the relationship between stand density and fine root B/N ratio (Figure 4a). The rising intra- and/or inter-specific competition with increasing stand density greatly shifts the fine root vitality (or resource absorption strategy) of AM and ECM trees and affects fine root B/N ratio by altering fine root production and mortality.
Furthermore, based on the available six major genera, we checked the relationships of fine root B/N ratio with environmental, stand, and edaphic factors for the different successional status. Although, there was no difference on fine root B/N ratio between forests dominated by early- (such as Betula, Pinus and Populus) and late-successional genera (such as Fagus, Picea and Quercus) in this analysis (Table 2), fine root B/N ratio of late-successional forests were closely aligned with climate, topography and stands factors (Table 3). These results are in accordance with many other studies which indicated that successional status strongly influence fine root dynamics and resource acquisition strategies (Yuan & Chen, 2010; Paz et
al., 2015). Therefore, we conclude- that above-ground variables such as stand density, tree age and successional status should be included in large-scale studies in order to improve usefulness of fine root biomass and necromass data.
4.3 Relationships between fine root B/N ratio and geographic factors
In fact, altitudinal and latitudinal gradients encompass multiple stress factors (e.g. low temperature stress, water and nutrient deficiency) that alter dependency of each other (Figure S3), suggesting that tree-root production, mortality and decomposition may be reasonably related to multiple environmental factors. This is also indicated by the contrasting
relationships with latitude (Figure 3a) and altitude (Figure 3c) for AM and ECM forest fine root B/N ratios. Forests located in higher altitude and latitude are characterized by low temperature and evaporation, which have further effects on metabolic processes and microbial activity (Reich et al., 2014). As a result, under such water-saturated, oxygen depleted and highly acidic soil conditions, decomposition processes are reduced, leading to larger accumulation of dead fine roots and lower B/N ratio (Silver et al., 1999; Hertel &
Wesche, 2008), which was also proved by the significant negative relationship between AM forest fine root B/N ratio and altitude above sea level (Figure 3c). In contrast, we observed that ECM forest fine root B/N ratio increased along with increasing altitude above sea level, suggesting that ECM forests may adapt better to lower temperate and higher precipitation than AM forests. In the present study, ECM forests were generally located in temperate and boreal regions, while AM forests were mainly situated in tropical region. One of the clearest differences observed among latitudinal regions was the significant relationship of fine root B/N ratio with altitude above sea level in tropical forests (Figure 3d). This probably reflects the greater magnitude of change in climatic conditions from low- to high-altitude stands in tropical forests relative to temperate and boreal forests, leading to the obvious altitude gradients in fine root B/N ratio in the tropics. Furthermore, the fine root B/N ratio in tropical forests was more highly correlated with mean annual temperature than with mean annual precipitation, suggesting that fine roots are driven more by temperature than by high water supply (Figure 2d). The results reported here indicate that water supply and demand appear to have a stronger influence on fine root B/N ratio in boreal forests (Figure 2b) than in tropical forests. In general, our results suggest that patterns of change in fine root B/N ratio does not generally follow a simple altitudinal gradient, and that these changes might be related to whether the dominant tree species are AM/ECM or in which region they are located (boreal vs. temperate vs. tropical).
It is surprising that we did not observe that temperate forest fine root B/N ratio was related with any factors in our analysis. The nature of the temperate forests dominated by ECM trees may have some impact, since ECM did not change fine root B/N ratio with soil C/N ratio and pH (Figure 5a, c). In the present study fine root B/N ratio varied up to 1.8 times among latitudinal regions with higher values in temperate forests and lower values in boreal and tropical forests (Table 1). An earlier report focused on root biomass allocation in global forests, and it predicted root biomass density was 33% and 10% higher in the temperate forests than in tropical and boreal forests, respectively (Cairns et al., 1997). The higher B/N ratio, reflecting absorptive capacity or dehydrogenase activity of fine roots
(Clemensson-Lindell & Persson, 1995), was consistent with greater net primary production in temperate forests (Huston & Wolverton, 2009). Globally, gross primary production of forests benefits from higher temperature and precipitation whereas net primary production saturates above either a threshold of 1500 mm precipitation or a mean annual temperature of 10°C (Luyssaert et al., 2007), values which are close to the mean annual precipitation and temperature in temperate forests (Table 1). The moderate temperature and precipitation regime in the temperate forests contributes the highest fine root B/N ratio, perhaps leading to the highest biomass carbon stocks (Keith et al., 2009). However, the consequences of a global change on forest ecosystems in temperate region may differ from those in boreal and tropical regions. Therefore, an analysis of more comprehensive datasets may reveal new or more stable relationships between fine root B/N ratio and environmental factors, given the sensitivity to changing environmental factor that vary between climate regions. Finally, our analyses have shown that fine root B/N ratio is a window in which biotic and abiotic forces are integrated and which, in turn, influence the performance of the forest ecosystem.
4.4 Limitation and implication
The generality and robustness of the present study are determined by the coverage of the data used. The observations of fine roots in this analysis are biased toward the northern
hemisphere and the Amazon forests (Figure S1). Fine root data scarcity in other forests which possess enormous biodiversity probably preclude accurate understanding of the dominated drive factors and of genus-specific fine root B/N ratio dynamics. There are multiple factors including climate, soil and stands incorporated in altitude and latitude gradients (Girardin et al., 2013; Reich et al., 2014). These factors independently and/or collectively determine fine root B/N ratio by living fine root mortality and dead fine root decomposition, which were
also strongly linked to plant community composition through root chemistry carbon allocation patterns (Girardin et al., 2013). Furthermore, the effects of mycorrhizal types on fine roots are highly uncertain due to the uneven distribution of AM and ECM forest study sites in boreal and tropical regions (Table 1). The construction of a quantitatively predictive model inclusive of all factors is still complicated because of a lack of process understanding, knowledge of species characteristics and fine root dynamics, and many interactions and feedback effects (Keith et al., 2009). Therefore, further efforts should be directed towards gathering more information about the relationships between fine root B/N ratio and easily measurable or available climatic, topographical, edaphic and stand-related factors to better integrate fine roots into ecosystem carbon pool and flux analyses.
5 Conclusions
Global environmental and climate change will result in warmer temperature, alterations of precipitation regimes and increased nitrogen deposition (with potential changes in soil C/N ratio and pH) in many regions. Fine root B/N ratio may respond to stress conditions such as nutrient imbalances, soil acidification, water saturation or drought (Persson & Stadenberg, 2010). Our analysis using a worldwide database revealed that responses of fine root B/N ratio to climate, altitude, edaphic and stand characteristics depend on the mycorrhizal types (AM vs. ECM) and latitudinal regions (boreal vs. temperate vs. tropical). The global patterns of forest fine root B/N ratio and their influencing factors revealed by the present study, provide a basis for large-scale prediction of fine root dynamics and for better understanding of belowground processes of global forest ecosystems in a changing world.
Acknowledgments
This work was financially supported by the Natural Science Foundation of China (Grant No.
31500354), China Postdoctoral Science Foundation (Grant No. 2016M601343) and the State Key Laboratory of Forest and Soil Ecology (Grant No. LFSE2015-12). We thank the many researchers who collected the field fine root data used in this analysis. Data used in this article will be available as part of the Fine-Root Ecology Database FRED
(http://roots.ornl.gov/) (Iversen et al., 2017).
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