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Effects of root dominate over aboveground litter on soil microbial biomass in global forest ecosystems

Effects of root dominate over aboveground litter on soil microbial biomass in global forest... Background: Inputs of above- and belowground litter into forest soils are changing at an unprecedented rate due to continuing human disturbances and climate change. Microorganisms drive the soil carbon (C) cycle, but the roles of above- and belowground litter in regulating the soil microbial community have not been evaluated at a global scale. Methods: Here, we conducted a meta-analysis based on 68 aboveground litter removal and root exclusion studies across forest ecosystems to quantify the roles of above- and belowground litter on soil microbial community and compare their relative importance. Results: Aboveground litter removal significantly declined soil microbial biomass by 4.9% but root exclusion inhibited it stronger, up to 11.7%. Moreover, the aboveground litter removal significantly raised fungi by 10.1% without altering bacteria, leading to a 46.7% increase in the fungi-to-bacteria (F/B) ratio. Differently, root exclusion significantly decreased the fungi by 26.2% but increased the bacteria by 5.7%, causing a 13.3% decrease in the F/B ratio. Specifically, root exclusion significantly inhibited arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and actinomycetes by 22.9%, 43.8%, and 7.9%, respectively. The negative effects of aboveground litter removal on microbial biomass increased with mean annual temperature and precipitation, whereas that of root exclusion on microbial biomass did not change with climatic factors but amplified with treatment duration. More importantly, greater effects of root exclusion on microbial biomass than aboveground litter removal were consistent across diverse forest biomes (expect boreal forests) and durations. Conclusions: These data provide a global evidence that root litter inputs exert a larger control on microbial biomass than aboveground litter inputs in forest ecosystems. Our study also highlights that changes in above- and belowground litter inputs could alter soil C stability differently by shifting the microbial community structure in the opposite direction. These findings are useful for predicting microbe-mediated C processes in response to changes in forest management or climate. Keywords: Forest ecosystems, soil microorganisms, Fungi, Litter, Root, Carbon input, Meta-analysis * Correspondence: qwang@iae.ac.cn Huitong Experimental Station of Forest Ecology, CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Jing et al. Forest Ecosystems (2021) 8:38 Page 2 of 9 Introduction importance due to soil ecological complexity and spatial Intensified human disturbances and climate change have heterogeneity (Culina et al. 2018). A quantitative synthe- greatly influenced above- and belowground litter (root) in- sis that reveals the global-scale patterns of above- and puts to forest soils. For example, harvesting forest prod- belowground litter effects on soil microorganisms and ucts significantly decreases the aboveground litter input compares their relative importance is urgently needed. (Achat et al. 2015), but nutrient deposition may increase The effects of above- and belowground litter on soil litter inputs more from aboveground than belowground microorganisms may vary depending on climate or for- parts via enhanced plant growth and decreased root-to- est biomes because forest productivity (Huston and shoot ratios (Song et al. 2019;Li et al. 2020). These Wolverton 2009), biomass allocation (Luo et al. 2012), changes in litter inputs can profoundly alter soil carbon and litter decomposition rate (Luo et al. 2012; See et al. (C) stocks, because plant litters are the main source of C 2019) are dependent on climate. A previous meta- into the soil (Lajtha et al. 2018; Reynolds et al. 2018). analysis has revealed that the microbial biomass in sub- However, we currently have insufficient capability to pre- tropical forests is more sensitive to aboveground litter dict the litter-induced changes in soil C dynamics. This is removal than that in temperate forests (Xu et al. 2013). mainly due to a critical knowledge gap on the general pat- Nevertheless, evidence is lacking on whether the effect terns of soil microorganism response to litter changes in of belowground litter on soil microorganisms is also cli- forest ecosystems, where approximately one-third of the matic- or biome-dependent. Moreover, litter inputs and terrestrial C is stored in soil (Dixon 1994). associated priming effect (defined as litter input triggers Soil microorganisms play a key role in soil C forma- decomposition of pre-existing SOC) are dependent on tion and stabilization (Schimel and Schaeffer 2012; Jing time (Huo et al. 2017; Wu et al. 2018), indicating that et al. 2019) and respond rapidly to changes in above- litter effects on soil microorganisms may vary over time. and belowground litter (Brant et al. 2006; Wang et al. However, this speculation remains untested. 2017a; Jing et al. 2019). Numerous studies have quanti- To address the above-mentioned issues, we performed fied the roles of above- and belowground litter in driving a meta-analysis of the soil microbial community in re- the soil microbial community via litter removal experi- sponse to aboveground litter removal and root exclusion ments (Hogberg et al. 2007; Weintraub et al. 2013;Xu by collecting 68 published litter experiments conducted et al. 2013; Wang et al. 2017a; vanden Enden et al., in forest ecosystems. Our study seeks to (1) quantify the 2018; Jing et al. 2019). Despite these efforts, to what ex- effects of above- and belowground litter on microbial tent above- and belowground litter influence soil micro- community, (2) compare their relative importance, and organisms remains largely unknown due to diverse (3) explore the environmental factors that can explain microbial responses. For instance, the microbial biomass the various effects of litter exclusion on the microbial has been reported to increase (Feng et al. 2002; Pisani biomass across studies. et al. 2016), decrease (Högberg and Högberg 2002;Li et al. 2004; Weintraub et al. 2013), or to change insig- Methods nificantly under litter exclusion treatments (Blazier et al. Data collection 2008; Prevost-Boure et al. 2011). Besides, the microbial Peer-reviewed journal articles published before December community structure indicated by the fungi-to-bacteria 2020 were searched using the Web of Science (http:// ratio (F/B) also decreases (Brant et al. 2006) or increases apps.webofknowledge.com/) and the China National (Pisani et al. 2016; Wang et al. 2017b) in response to re- Knowledge Infrastructure (http://www.cnki.net/). The moving litters. Moreover, above- and belowground lit- searched terms were “(carbon input OR litter inputs OR ters differ in chemical properties, turnover rates, and litter manipulation OR litter removal OR detrital input pathways entering into the soil (Hatton et al. 2015; and removal treatment OR root exclusion OR trenching Fulton-Smith and Cotrufo 2019; Sokol et al. 2019), OR girdling) AND (microbe OR microbial OR phospho- meaning that they may exert different controls on soil lipid fatty acid OR PLFA) AND (forest)”. To minimize microorganisms. Aboveground litters are traditionally publication bias, only studies that satisfied the following believed to be equal to or more important than roots in criteria were included in this meta-analysis. (1) Only field affecting the microbial community (Li et al. 2004; Wang experiments were selected; (2) The control and treatment et al. 2017a). This notion clashes with the emerging evi- plots were established in the same climatic types, domin- dence that root exclusion inhibits the microbial biomass ant plant groups, and soil conditions; (3) The means, greater than aboveground litter removal (vanden Enden standard deviations (or standard errors) and numbers of et al., 2018; Liu et al. 2019). Unfortunately, to date, few replicates were reported; (4) Only the latest results were studies have compared the importance of above- and be- used if multiple observations were made at different times lowground litters to the soil microbial community, and in the same study site; (5) Only the topmost soil layer was thus are unlikely to identify the global relative included if multiple soil depths were reported; (6) Jing et al. Forest Ecosystems (2021) 8:38 Page 3 of 9 Different litter-removal treatments, soil or vegetation and MAP ranging from − 4.9 °C to 35 °C, and from 420 types in the same study were regarded as an independent to 5000 mm, respectively. We collected data directly study. Ultimately, a total of 60 aboveground litter removal from either tables or indirectly from figures by using and 71 root exclusion experiments obtained from 68 pa- GetData Graph Digitizer 2.24 software. pers met the criteria above and were utilized for this meta-analysis (Supporting Information). Meta analysis For each of the selected studies (Fig. 1), we extracted We used the natural log of the response ratio (lnRR), de- data of total microbial biomass, the biomass of fungi, bac- fined as the ‘effect size’ to determine the significance of teria, Gram-positive bacteria (GP), Gram-negative bacteria microbial responses to above- or belowground input re- (GN), actinomycetes (ACT), arbuscular mycorrhizal fungi moval (Hedges et al. 1999). For a given variable, the re- (AMF), ectomycorrhizal fungi (EMF), fungi-to-bacteria ra- sponse ratio (RR) was calculated as below: tio (F/B) and the ratio of Gram-positive to Gram-negative bacteria (GP/GN). If the case study used both chloroform t lnRR ¼ ln ¼ ln X − ln X ð1Þ t c fumigation (CF) and phospholipid fatty acid (PLFA) X methods to measure microbial biomass, we chose the where X and X are the means of litter removal treat- t c former as Ren et al. (2017) did. Methods for determining ments and the control, respectively. The variance within the fungal and bacterial biomass included PLFA (Jing each study was calculated by: et al. 2019) and microscope (Subke et al. 2004). Root ex- clusion included trenching and girdling experiments, be- 2 2 s s t c cause these two methods yield quantitatively similar v ¼ þ ð2Þ 2 2 n X n X outcomes for microbial biomass (P >0.05, Fig. S1). t t c c Besides the information on microbes, we also recorded where s , n versus s , n are the standard deviation and t t c c forest biomes (boreal, temperate, and sub/tropical for- sample size under litter removal and control treatments, ests), mean annual temperature (MAT), mean annual respectively. precipitation (MAP), experimental duration [grouped We calculated the weight (w) of each lnRR by the in- into short (< 3 years) and long duration (≥3 years)], dis- verse of variance as below: solved organic C (DOC), and other soil properties (e.g. soil temperature, and soil moisture). If studies did not w ¼ ð3Þ report climate variables, the WorldClim data (http:// www.worldclim.com/) were used to reconstruct climate values based on latitude and longitude. These data cov- Finally, the mean variance-weighted effect size lnRR ered a wide gradient of climatic conditions, with MAT for all observations was calculated as Eq. 4 using a fixed Fig. 1 Global distribution of locations of studies included in this meta-analysis Jing et al. Forest Ecosystems (2021) 8:38 Page 4 of 9 effects model in MetaWin software (2.1) (Hedges et al. enrichment in the F/B ratio (Fig. 2a, P < 0.01). However, 1999; Ren et al. 2017). root exclusion significantly increased bacteria by 5.7% and decreased fungi by 26.2%, resulting in a 13.3% de- ðÞ w  lnRR i i crease in the F/B ratio (Fig. 2b, all P < 0.05). In detail, lnRR ¼ P ð4Þ þþ ðÞ w root exclusion significantly increased GP bacteria by 4.2%, but significantly inhibited AMF, EMF, and ACT by If 95% confidence intervals (CIs) of lnRR did not ++ 22.9%, 43.8%, and 7.9%, respectively (Fig. 2b, all P < overlap with 0, then effects were significant at P < 0.05. 0.05). Moreover, aboveground litter removal and root The changes caused by input treatments for a certain re- exclusion increased the GP/GN bacteria ratio to a simi- sponse variable were calculated as: lar extent (Fig. 2, both P < 0.05). PercentageðÞ % ¼ expðÞ lnRR −1 100% ð5Þ þþ Factors controlling the microbial responses The statistic differences between the effect sizes of Regression analysis revealed that across all forest ecosys- aboveground litter removal (ALR) and that of root ex- tems, the lnRR of soil microbial biomass to aboveground clusion (RE) were analyzed by between-group heterogen- litter removal increased with MAT (Fig. 3a, R = 0.129, eity (Ren et al. 2017; Chen and Chen 2018). Regression P < 0.01) and MAP (Fig. 3b, R = 0.111, P < 0.01), but did and correlation analyses were adopted to examine the not change with experimental duration or other soil var- relationships of lnRRs of microbial biomass and F/B ra- iables (Figs. 3c–d and Table S1). Regarding forest bi- tio to duration, climatic variables and soil properties omes, above-ground litter removal significantly inhibited using SPSS 22.0 software (SPSS Inc.). the microbial biomass in sub/tropical forests (P < 0.05) but not in temperate forests or boreal forests (Fig. 4). Results Conversely, the microbial biomass response to root ex- Effects of above- and belowground litter on the soil clusion did not show any significant correlation with microbial community MAT or MAP (Figs. 3a–b, both P > 0.05) but decreased At the global scale, aboveground litter removal signifi- linearly with experimental duration (Fig. 3c, R = 0.135, cantly decreased the total microbial biomass by 4.9% P = 0.003), with a 90.8% greater response in long- com- (Fig. 2a, P < 0.05). In comparison to the above-ground pared to short-term studies (Fig. 4, P = 0.001). Moreover, litter removal, root exclusion caused a stronger decline the stronger effect of root exclusion than aboveground in the microbial biomass, reaching11.7% (Fig. 2b, P < litter removal on microbial biomass was consistent 0.05). The aboveground litter removal significantly en- across diverse forest biomes (except boreal forests) and hanced fungi by 10.1% (P < 0.05) but showed no effect durations (all P ≤ 0.005). on other specific microbial groups, leading to a 46.7% Fig. 2 Effects of ALR (a) and RE (b) on soil microbial community. The number of observations for each variable is shown next to the point. Error bars represent 95% CIs. AMF, arbuscular mycorrhizal fungi; EMF, ectomycorrhizal fungi; GP, Gram-positive bacteria; GN, Gram-negative bacteria; ACT, actinomycetes; F/B, fungi to bacteria ratio; ALR, aboveground litter removal; RE, root exclusion Jing et al. Forest Ecosystems (2021) 8:38 Page 5 of 9 Fig. 3 Relationships of lnRR of microbial biomass with MAT, MAP, duration, and lnRR of DOC. Red and blue lines represent ALR and RE effects, respectively. ALR, aboveground litter removal; RE, root exclusion Based on the current limited number of observations, the aboveground litter-induced changes in the F/B ratio exhibited significantly positive correlations with treat- ment duration (P < 0.01, Table S1) but did not show any significant correlation with climatic variables or soil properties. By contrast, the effects of root exclusion on the F/B ratio significantly increased with the lnRR of soil nitrate nitrogen but decreased with the lnRR of soil am- monium nitrogen (both P < 0.05, Table S1). Discussion Distinct roles of above- and belowground litter on the microbial community Our results showed that globally, aboveground litter re- moval decreased microbial biomass by an average of 4.9% (Fig. 2a), suggesting that aboveground litter is an important C source for microbial growth. This finding confirms the aboveground litter effects on microbial bio- mass reported earlier (Xu et al. 2013), but the magni- tudes of effects differ, which may be partly due to the different numbers of observations (55 studies vs. 14 studies for our analysis vs. previous analysis, respect- ively) and data source (more temperate and boreal stud- ies in our analysis than previous one). DOC, which is a Fig. 4 The lnRR of microbial biomass to ALR and RE. The variables are categorized into different forest biomes and durations. The labile soil C that depends strongly on plant C inputs number of observations for each variable is shown next to the point. (Sokol et al. 2019), significantly decreased with above- Error bars represent 95% CIs. ALR, aboveground litter removal; RE, ground litter removal (Fig. S2). This may contribute to root exclusion decreases in microbial biomass with aboveground litter Jing et al. Forest Ecosystems (2021) 8:38 Page 6 of 9 removal, because soil microbes are highly dependent on removing aboveground litter and root shift the microbial DOC (Fig. 3d; Ren et al. 2017; Li et al. 2019). Import- community structure in the opposite direction. It is antly, this study, as the first, revealed that root exclusion commonly accepted that a high F/B ratio has greater po- reduced microbial biomass to a larger extent than above- tential to benefit soil C-sequestration because fungi in- ground litter removal (Fig. 2), thus supporting the vest more C to growth, produce more recalcitrant newly-developing view that root litter inputs exert a residues, and stimulate aggregate formation which se- stronger control on microbial biomass than aboveground quester C from microbial decomposition than bacteria litter does (vanden Enden et al., 2018; Liu et al. 2019). do (Strickland and Rousk 2010; Jing et al. 2019). Thus, Root-derived DOC are nearly three times more than the present findings imply that reducing root inputs or aboveground litter-derived DOC (Sokol et al. 2019). relative allocation tend to induce greater soil C vulner- Thus, the greater decline in DOC under root exclu- ability than the loss of aboveground litter. Therefore, sion than aboveground litter removal (Fig. S2) likely further studies on soil C storage and stability in response contributes to the lower microbial biomass under root to above- and belowground litter exclusion are exclusion. necessary. We also found that litter exclusion showed diverse ef- fects on microbial groups. Aboveground litter removal Different factors controlling the responses of microbial significantly increased fungi but had no effects on bac- biomass teria (Fig. 2a), suggesting that fungi are more sensitive to We focused our discussion on the microbial biomass be- aboveground litter alterations than bacteria. Continuous cause the F/B ratio was relatively insufficient to draw aboveground litter removal decreases soil labile C (Fig. firm conclusions. We found that climate-related vari- S2; vanden Enden et al., 2018) and increases recalcitrant ables are key factors regulating the effect of aboveground C compounds (Pisani et al. 2016). In this case, relative to litter on microbial biomass, with more pronounced bacteria, fungi have higher capability of acquiring recal- aboveground litter effect in higher MAT and MAP re- citrant C via producing C-degrading enzymes and re- gions (i.e., sub/tropical forests; Figs. 3a, b and 4). This locating nutrients by fungal hyphal (Strickland and finding suggests that the microbial biomass in warmer Rousk 2010). Furthermore, fungi have higher C use effi- and wetter forests would be more vulnerable to future ciency, and thus higher biomass yield efficiency (Strick- aboveground litter loss than that in colder and drier for- land and Rousk 2010; Kallenbach et al. 2016). These ests. Similar results have been reported in a previous may increase fungal biomass under aboveground litter meta-analysis (Xu et al. 2013). Aboveground litters indir- removal. ectly enter into the soil by leaching and bioturbation Different from aboveground litter removal, root exclu- (Vidal et al. 2017). Higher MAT and MAP are not only sion significantly inhibited fungi, especially AMF and accompanied with more production of aboveground lit- EMF (Fig. 2b). These results are consistent with those of ter (Luo et al. 2012), fast litter decomposition (Campo C-labelling studies, which shows that fungi utilize most and Merino 2016; See et al. 2019) but also with stronger of rhizodeposition-derived C (Denef et al. 2009; Bai et al. leaching and more soil fauna (Xu et al. 2020). These can 2016) but offer global evidence that fungi especially explain why soil microbes are more reliant on above- mycorrhizal fungi rely much on root-derived C input. ground inputs in warmer and wetter forests. The lack of This finding is not surprising, because mycorrhiza fungi, correlation between microbial biomass under above- as a large fungal biomass pool, form symbiosis with the ground litter removal and experimental duration may be roots of over 90% plants (Brundrett and Tedersoo 2018) because soil microorganisms adjust their community and receive up to 22% of net photosynthetic products structure (Fig. 2a) or their C utilization strategies (Wang (Hobbie 2006). However, it is surprising that root exclu- et al. 2019) to maintain their biomass over time after re- sion stimulated bacterial biomass (Fig. 2b), as bacteria moving aboveground litter. also have high ability of utilizing root-derived C (Huang Surprisingly, the effect of root exclusion on the micro- et al. 2020). This may be due to that the loss of fungi bial biomass did not change with MAT or MAP (Fig. 3a with root exclusion alleviates the antagonistic effects to- and b). However, it should be noted that the existing wards bacterial growth (Schneider et al. 2010) and pro- two observations on microbial biomass in boreal forests vides their residues for utilization by bacteria (Ryckeboer remained unchanged under root exclusion (Fig. 4), et al. 2003; Apostel et al., 2018). which limits our ability to confirm whether root effects Given these diverse responses of microbial groups, our on microbial biomass is consistent across the globe. study offers new insights into the variations of the F/B Therefore, further studies should be carried out in these ratio associated with removing litter inputs, which was forests to provide a quantitative estimation of the re- stimulated by aboveground litter removal but decreased sponse of microbial biomass to root exclusion. While we by root exclusion (Fig. 2). This result suggests that the observed that the reductions in microbial biomass with Jing et al. Forest Ecosystems (2021) 8:38 Page 7 of 9 root exclusion became larger as experimental duration finding further brings a challenge to describe the effects went longer (Figs. 3c and 4), lacking a saturating re- of multiple drivers on the response ratio of microbial sponse and suggesting that root effects on microorgan- biomass, which is similar to many other meta-analysis isms is lasting and deepening. Long-term root exclusion studies that lacking sufficient associated measurements leads to a shift in microbial utilization from labile C (Ren et al. 2017; Yang et al. 2020). Therefore, microbial pools to recalcitrant C pools in soils (Pisani et al. 2016; community and soil property responses should be exam- Wu et al. 2018). Given that fungi have high ability of ined simultaneously under the context of removing lit- utilizing recalcitrant C compounds as described above ters in future experimental research. Despite above- (Strickland and Rousk 2010; Meng et al. 2020), signifi- mentioned limitations, our study is the first meta- cant inhibitions in fungi with root exclusion (Fig. 2b) is analysis elucidating litter roles in the microbial commu- likely unable to meet the microbial C needs for growth, nity and providing a global picture for understanding and ultimately decreasing microbial biomass over time. the relative importance of above- versus belowground Furthermore, the long-term root exclusion has less com- litter in regulating the microbial community in forest pensation effect from dead roots, because nearly 92% ecosystems. fine roots and 80% coarse roots are decomposed beyond three-year according to global root decomposition rate Conclusions (Silver and Miya 2001). This time-dependent effect of To our knowledge, this current meta-analysis study is root litter indicates that the root importance on soil mi- the first global syntheses to quantitatively evaluate the croorganisms would be underestimated by short-term roles of above- and belowground litter on the soil micro- experiments. Thus, more long-term experiments con- bial community in forest ecosystems. Our synthesis ducted in forest ecosystems are urgently needed to gain showed that root litter was stronger than aboveground insights into microbial responses to root exclusion at the litter for microbial biomass worldwide. More import- global scale. antly, the root effect amplified over time, but effect of Although factors controlling the responses of micro- aboveground litter was dependent on climate (i.e., forest bial biomass to aboveground litter removal and root ex- biomes). Furthermore, removing litter from above- and clusion differed, we did observe that the greater belowground shifted the microbial community structure influence of belowground litter inputs on the soil micro- in the opposite direction, which could have profound bial biomass than aboveground litter inputs is consistent but different effects on the global soil C cycle. These across diverse forest biomes (expect boreal forests) and findings highlight the importance and different roles of treatment durations (Fig. 4). Similarly, 35.7% studies, aboveground and root litters, which should be fully con- which simultaneously removing aboveground and below- sidered when predicting microbe-mediated processes ground litters, showed that the effects of roots on micro- and establishing forest management strategies with a bial biomass are larger than that of aboveground litter in changing climate. temperate forests (Wang et al. 2017a; vanden Enden et al., 2018) and sub/tropical forests (Wang et al. 2017b; Wu et al. 2018; Liu et al. 2019). We thus emphasize that Supplementary Information C allocation should be considered when projecting The online version contains supplementary material available at https://doi. org/10.1186/s40663-021-00318-8. microbe-derived soil C changes in response to climate change and forest managements in forest ecosystems. Additional file 1: Fig. S1. The root removal effect on microbial biomass However, the generally weak accounts of variations in by trenching and girdling methods. The numbers in the right of figure microbial biomass under litter exclusion by all variables represents the number of case studies. Fig.S2. Effects of ALR and RE on dissolved organic carbon. The numbers in the right of figure represents considered here point to the complex nature of micro- the number of case studies. ALR, above-ground litter removal; RE, root ex- bial responses to litter exclusion. Climatic variables indi- clusion. Table S1. Correlation coefficients of the effect size of sol micro- vidually accounted for 24% of the overall variations in bial biomass and F/B ratio to above-ground litter removal (ALR) and root exclusion (RE) with climatic variables and soil properties microbial biomass under aboveground litter removal, whereas the experimental duration and DOC explained 50.2% of changes in microbial biomass under root exclu- Acknowledgements sion. Although litter exclusion significantly influences We thank the anonymous reviewers for helpful suggestions on manuscript preparation. soil temperature and soil moisture (Xu et al. 2013; Zhang et al. 2020), which may alter microbial responses due to their close linkages (Wang et al. 2019; Rasmussen Authors’ contributions YJ designed the study, data preparation, analysis, and wrote the paper. QW et al. 2020), we did not observe these soil properties in- provided the paper editing. PT and WL participated in the data preparation fluence microbial response to litter exclusion based on and processing. ZS and HY provided suggestion to improve the paper our limited number of observations (Table S1). This quality. All the authors read and approved the final manuscript. Jing et al. 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Effects of root dominate over aboveground litter on soil microbial biomass in global forest ecosystems

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Abstract

Background: Inputs of above- and belowground litter into forest soils are changing at an unprecedented rate due to continuing human disturbances and climate change. Microorganisms drive the soil carbon (C) cycle, but the roles of above- and belowground litter in regulating the soil microbial community have not been evaluated at a global scale. Methods: Here, we conducted a meta-analysis based on 68 aboveground litter removal and root exclusion studies across forest ecosystems to quantify the roles of above- and belowground litter on soil microbial community and compare their relative importance. Results: Aboveground litter removal significantly declined soil microbial biomass by 4.9% but root exclusion inhibited it stronger, up to 11.7%. Moreover, the aboveground litter removal significantly raised fungi by 10.1% without altering bacteria, leading to a 46.7% increase in the fungi-to-bacteria (F/B) ratio. Differently, root exclusion significantly decreased the fungi by 26.2% but increased the bacteria by 5.7%, causing a 13.3% decrease in the F/B ratio. Specifically, root exclusion significantly inhibited arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and actinomycetes by 22.9%, 43.8%, and 7.9%, respectively. The negative effects of aboveground litter removal on microbial biomass increased with mean annual temperature and precipitation, whereas that of root exclusion on microbial biomass did not change with climatic factors but amplified with treatment duration. More importantly, greater effects of root exclusion on microbial biomass than aboveground litter removal were consistent across diverse forest biomes (expect boreal forests) and durations. Conclusions: These data provide a global evidence that root litter inputs exert a larger control on microbial biomass than aboveground litter inputs in forest ecosystems. Our study also highlights that changes in above- and belowground litter inputs could alter soil C stability differently by shifting the microbial community structure in the opposite direction. These findings are useful for predicting microbe-mediated C processes in response to changes in forest management or climate. Keywords: Forest ecosystems, soil microorganisms, Fungi, Litter, Root, Carbon input, Meta-analysis * Correspondence: qwang@iae.ac.cn Huitong Experimental Station of Forest Ecology, CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Jing et al. Forest Ecosystems (2021) 8:38 Page 2 of 9 Introduction importance due to soil ecological complexity and spatial Intensified human disturbances and climate change have heterogeneity (Culina et al. 2018). A quantitative synthe- greatly influenced above- and belowground litter (root) in- sis that reveals the global-scale patterns of above- and puts to forest soils. For example, harvesting forest prod- belowground litter effects on soil microorganisms and ucts significantly decreases the aboveground litter input compares their relative importance is urgently needed. (Achat et al. 2015), but nutrient deposition may increase The effects of above- and belowground litter on soil litter inputs more from aboveground than belowground microorganisms may vary depending on climate or for- parts via enhanced plant growth and decreased root-to- est biomes because forest productivity (Huston and shoot ratios (Song et al. 2019;Li et al. 2020). These Wolverton 2009), biomass allocation (Luo et al. 2012), changes in litter inputs can profoundly alter soil carbon and litter decomposition rate (Luo et al. 2012; See et al. (C) stocks, because plant litters are the main source of C 2019) are dependent on climate. A previous meta- into the soil (Lajtha et al. 2018; Reynolds et al. 2018). analysis has revealed that the microbial biomass in sub- However, we currently have insufficient capability to pre- tropical forests is more sensitive to aboveground litter dict the litter-induced changes in soil C dynamics. This is removal than that in temperate forests (Xu et al. 2013). mainly due to a critical knowledge gap on the general pat- Nevertheless, evidence is lacking on whether the effect terns of soil microorganism response to litter changes in of belowground litter on soil microorganisms is also cli- forest ecosystems, where approximately one-third of the matic- or biome-dependent. Moreover, litter inputs and terrestrial C is stored in soil (Dixon 1994). associated priming effect (defined as litter input triggers Soil microorganisms play a key role in soil C forma- decomposition of pre-existing SOC) are dependent on tion and stabilization (Schimel and Schaeffer 2012; Jing time (Huo et al. 2017; Wu et al. 2018), indicating that et al. 2019) and respond rapidly to changes in above- litter effects on soil microorganisms may vary over time. and belowground litter (Brant et al. 2006; Wang et al. However, this speculation remains untested. 2017a; Jing et al. 2019). Numerous studies have quanti- To address the above-mentioned issues, we performed fied the roles of above- and belowground litter in driving a meta-analysis of the soil microbial community in re- the soil microbial community via litter removal experi- sponse to aboveground litter removal and root exclusion ments (Hogberg et al. 2007; Weintraub et al. 2013;Xu by collecting 68 published litter experiments conducted et al. 2013; Wang et al. 2017a; vanden Enden et al., in forest ecosystems. Our study seeks to (1) quantify the 2018; Jing et al. 2019). Despite these efforts, to what ex- effects of above- and belowground litter on microbial tent above- and belowground litter influence soil micro- community, (2) compare their relative importance, and organisms remains largely unknown due to diverse (3) explore the environmental factors that can explain microbial responses. For instance, the microbial biomass the various effects of litter exclusion on the microbial has been reported to increase (Feng et al. 2002; Pisani biomass across studies. et al. 2016), decrease (Högberg and Högberg 2002;Li et al. 2004; Weintraub et al. 2013), or to change insig- Methods nificantly under litter exclusion treatments (Blazier et al. Data collection 2008; Prevost-Boure et al. 2011). Besides, the microbial Peer-reviewed journal articles published before December community structure indicated by the fungi-to-bacteria 2020 were searched using the Web of Science (http:// ratio (F/B) also decreases (Brant et al. 2006) or increases apps.webofknowledge.com/) and the China National (Pisani et al. 2016; Wang et al. 2017b) in response to re- Knowledge Infrastructure (http://www.cnki.net/). The moving litters. Moreover, above- and belowground lit- searched terms were “(carbon input OR litter inputs OR ters differ in chemical properties, turnover rates, and litter manipulation OR litter removal OR detrital input pathways entering into the soil (Hatton et al. 2015; and removal treatment OR root exclusion OR trenching Fulton-Smith and Cotrufo 2019; Sokol et al. 2019), OR girdling) AND (microbe OR microbial OR phospho- meaning that they may exert different controls on soil lipid fatty acid OR PLFA) AND (forest)”. To minimize microorganisms. Aboveground litters are traditionally publication bias, only studies that satisfied the following believed to be equal to or more important than roots in criteria were included in this meta-analysis. (1) Only field affecting the microbial community (Li et al. 2004; Wang experiments were selected; (2) The control and treatment et al. 2017a). This notion clashes with the emerging evi- plots were established in the same climatic types, domin- dence that root exclusion inhibits the microbial biomass ant plant groups, and soil conditions; (3) The means, greater than aboveground litter removal (vanden Enden standard deviations (or standard errors) and numbers of et al., 2018; Liu et al. 2019). Unfortunately, to date, few replicates were reported; (4) Only the latest results were studies have compared the importance of above- and be- used if multiple observations were made at different times lowground litters to the soil microbial community, and in the same study site; (5) Only the topmost soil layer was thus are unlikely to identify the global relative included if multiple soil depths were reported; (6) Jing et al. Forest Ecosystems (2021) 8:38 Page 3 of 9 Different litter-removal treatments, soil or vegetation and MAP ranging from − 4.9 °C to 35 °C, and from 420 types in the same study were regarded as an independent to 5000 mm, respectively. We collected data directly study. Ultimately, a total of 60 aboveground litter removal from either tables or indirectly from figures by using and 71 root exclusion experiments obtained from 68 pa- GetData Graph Digitizer 2.24 software. pers met the criteria above and were utilized for this meta-analysis (Supporting Information). Meta analysis For each of the selected studies (Fig. 1), we extracted We used the natural log of the response ratio (lnRR), de- data of total microbial biomass, the biomass of fungi, bac- fined as the ‘effect size’ to determine the significance of teria, Gram-positive bacteria (GP), Gram-negative bacteria microbial responses to above- or belowground input re- (GN), actinomycetes (ACT), arbuscular mycorrhizal fungi moval (Hedges et al. 1999). For a given variable, the re- (AMF), ectomycorrhizal fungi (EMF), fungi-to-bacteria ra- sponse ratio (RR) was calculated as below: tio (F/B) and the ratio of Gram-positive to Gram-negative bacteria (GP/GN). If the case study used both chloroform t lnRR ¼ ln ¼ ln X − ln X ð1Þ t c fumigation (CF) and phospholipid fatty acid (PLFA) X methods to measure microbial biomass, we chose the where X and X are the means of litter removal treat- t c former as Ren et al. (2017) did. Methods for determining ments and the control, respectively. The variance within the fungal and bacterial biomass included PLFA (Jing each study was calculated by: et al. 2019) and microscope (Subke et al. 2004). Root ex- clusion included trenching and girdling experiments, be- 2 2 s s t c cause these two methods yield quantitatively similar v ¼ þ ð2Þ 2 2 n X n X outcomes for microbial biomass (P >0.05, Fig. S1). t t c c Besides the information on microbes, we also recorded where s , n versus s , n are the standard deviation and t t c c forest biomes (boreal, temperate, and sub/tropical for- sample size under litter removal and control treatments, ests), mean annual temperature (MAT), mean annual respectively. precipitation (MAP), experimental duration [grouped We calculated the weight (w) of each lnRR by the in- into short (< 3 years) and long duration (≥3 years)], dis- verse of variance as below: solved organic C (DOC), and other soil properties (e.g. soil temperature, and soil moisture). If studies did not w ¼ ð3Þ report climate variables, the WorldClim data (http:// www.worldclim.com/) were used to reconstruct climate values based on latitude and longitude. These data cov- Finally, the mean variance-weighted effect size lnRR ered a wide gradient of climatic conditions, with MAT for all observations was calculated as Eq. 4 using a fixed Fig. 1 Global distribution of locations of studies included in this meta-analysis Jing et al. Forest Ecosystems (2021) 8:38 Page 4 of 9 effects model in MetaWin software (2.1) (Hedges et al. enrichment in the F/B ratio (Fig. 2a, P < 0.01). However, 1999; Ren et al. 2017). root exclusion significantly increased bacteria by 5.7% and decreased fungi by 26.2%, resulting in a 13.3% de- ðÞ w  lnRR i i crease in the F/B ratio (Fig. 2b, all P < 0.05). In detail, lnRR ¼ P ð4Þ þþ ðÞ w root exclusion significantly increased GP bacteria by 4.2%, but significantly inhibited AMF, EMF, and ACT by If 95% confidence intervals (CIs) of lnRR did not ++ 22.9%, 43.8%, and 7.9%, respectively (Fig. 2b, all P < overlap with 0, then effects were significant at P < 0.05. 0.05). Moreover, aboveground litter removal and root The changes caused by input treatments for a certain re- exclusion increased the GP/GN bacteria ratio to a simi- sponse variable were calculated as: lar extent (Fig. 2, both P < 0.05). PercentageðÞ % ¼ expðÞ lnRR −1 100% ð5Þ þþ Factors controlling the microbial responses The statistic differences between the effect sizes of Regression analysis revealed that across all forest ecosys- aboveground litter removal (ALR) and that of root ex- tems, the lnRR of soil microbial biomass to aboveground clusion (RE) were analyzed by between-group heterogen- litter removal increased with MAT (Fig. 3a, R = 0.129, eity (Ren et al. 2017; Chen and Chen 2018). Regression P < 0.01) and MAP (Fig. 3b, R = 0.111, P < 0.01), but did and correlation analyses were adopted to examine the not change with experimental duration or other soil var- relationships of lnRRs of microbial biomass and F/B ra- iables (Figs. 3c–d and Table S1). Regarding forest bi- tio to duration, climatic variables and soil properties omes, above-ground litter removal significantly inhibited using SPSS 22.0 software (SPSS Inc.). the microbial biomass in sub/tropical forests (P < 0.05) but not in temperate forests or boreal forests (Fig. 4). Results Conversely, the microbial biomass response to root ex- Effects of above- and belowground litter on the soil clusion did not show any significant correlation with microbial community MAT or MAP (Figs. 3a–b, both P > 0.05) but decreased At the global scale, aboveground litter removal signifi- linearly with experimental duration (Fig. 3c, R = 0.135, cantly decreased the total microbial biomass by 4.9% P = 0.003), with a 90.8% greater response in long- com- (Fig. 2a, P < 0.05). In comparison to the above-ground pared to short-term studies (Fig. 4, P = 0.001). Moreover, litter removal, root exclusion caused a stronger decline the stronger effect of root exclusion than aboveground in the microbial biomass, reaching11.7% (Fig. 2b, P < litter removal on microbial biomass was consistent 0.05). The aboveground litter removal significantly en- across diverse forest biomes (except boreal forests) and hanced fungi by 10.1% (P < 0.05) but showed no effect durations (all P ≤ 0.005). on other specific microbial groups, leading to a 46.7% Fig. 2 Effects of ALR (a) and RE (b) on soil microbial community. The number of observations for each variable is shown next to the point. Error bars represent 95% CIs. AMF, arbuscular mycorrhizal fungi; EMF, ectomycorrhizal fungi; GP, Gram-positive bacteria; GN, Gram-negative bacteria; ACT, actinomycetes; F/B, fungi to bacteria ratio; ALR, aboveground litter removal; RE, root exclusion Jing et al. Forest Ecosystems (2021) 8:38 Page 5 of 9 Fig. 3 Relationships of lnRR of microbial biomass with MAT, MAP, duration, and lnRR of DOC. Red and blue lines represent ALR and RE effects, respectively. ALR, aboveground litter removal; RE, root exclusion Based on the current limited number of observations, the aboveground litter-induced changes in the F/B ratio exhibited significantly positive correlations with treat- ment duration (P < 0.01, Table S1) but did not show any significant correlation with climatic variables or soil properties. By contrast, the effects of root exclusion on the F/B ratio significantly increased with the lnRR of soil nitrate nitrogen but decreased with the lnRR of soil am- monium nitrogen (both P < 0.05, Table S1). Discussion Distinct roles of above- and belowground litter on the microbial community Our results showed that globally, aboveground litter re- moval decreased microbial biomass by an average of 4.9% (Fig. 2a), suggesting that aboveground litter is an important C source for microbial growth. This finding confirms the aboveground litter effects on microbial bio- mass reported earlier (Xu et al. 2013), but the magni- tudes of effects differ, which may be partly due to the different numbers of observations (55 studies vs. 14 studies for our analysis vs. previous analysis, respect- ively) and data source (more temperate and boreal stud- ies in our analysis than previous one). DOC, which is a Fig. 4 The lnRR of microbial biomass to ALR and RE. The variables are categorized into different forest biomes and durations. The labile soil C that depends strongly on plant C inputs number of observations for each variable is shown next to the point. (Sokol et al. 2019), significantly decreased with above- Error bars represent 95% CIs. ALR, aboveground litter removal; RE, ground litter removal (Fig. S2). This may contribute to root exclusion decreases in microbial biomass with aboveground litter Jing et al. Forest Ecosystems (2021) 8:38 Page 6 of 9 removal, because soil microbes are highly dependent on removing aboveground litter and root shift the microbial DOC (Fig. 3d; Ren et al. 2017; Li et al. 2019). Import- community structure in the opposite direction. It is antly, this study, as the first, revealed that root exclusion commonly accepted that a high F/B ratio has greater po- reduced microbial biomass to a larger extent than above- tential to benefit soil C-sequestration because fungi in- ground litter removal (Fig. 2), thus supporting the vest more C to growth, produce more recalcitrant newly-developing view that root litter inputs exert a residues, and stimulate aggregate formation which se- stronger control on microbial biomass than aboveground quester C from microbial decomposition than bacteria litter does (vanden Enden et al., 2018; Liu et al. 2019). do (Strickland and Rousk 2010; Jing et al. 2019). Thus, Root-derived DOC are nearly three times more than the present findings imply that reducing root inputs or aboveground litter-derived DOC (Sokol et al. 2019). relative allocation tend to induce greater soil C vulner- Thus, the greater decline in DOC under root exclu- ability than the loss of aboveground litter. Therefore, sion than aboveground litter removal (Fig. S2) likely further studies on soil C storage and stability in response contributes to the lower microbial biomass under root to above- and belowground litter exclusion are exclusion. necessary. We also found that litter exclusion showed diverse ef- fects on microbial groups. Aboveground litter removal Different factors controlling the responses of microbial significantly increased fungi but had no effects on bac- biomass teria (Fig. 2a), suggesting that fungi are more sensitive to We focused our discussion on the microbial biomass be- aboveground litter alterations than bacteria. Continuous cause the F/B ratio was relatively insufficient to draw aboveground litter removal decreases soil labile C (Fig. firm conclusions. We found that climate-related vari- S2; vanden Enden et al., 2018) and increases recalcitrant ables are key factors regulating the effect of aboveground C compounds (Pisani et al. 2016). In this case, relative to litter on microbial biomass, with more pronounced bacteria, fungi have higher capability of acquiring recal- aboveground litter effect in higher MAT and MAP re- citrant C via producing C-degrading enzymes and re- gions (i.e., sub/tropical forests; Figs. 3a, b and 4). This locating nutrients by fungal hyphal (Strickland and finding suggests that the microbial biomass in warmer Rousk 2010). Furthermore, fungi have higher C use effi- and wetter forests would be more vulnerable to future ciency, and thus higher biomass yield efficiency (Strick- aboveground litter loss than that in colder and drier for- land and Rousk 2010; Kallenbach et al. 2016). These ests. Similar results have been reported in a previous may increase fungal biomass under aboveground litter meta-analysis (Xu et al. 2013). Aboveground litters indir- removal. ectly enter into the soil by leaching and bioturbation Different from aboveground litter removal, root exclu- (Vidal et al. 2017). Higher MAT and MAP are not only sion significantly inhibited fungi, especially AMF and accompanied with more production of aboveground lit- EMF (Fig. 2b). These results are consistent with those of ter (Luo et al. 2012), fast litter decomposition (Campo C-labelling studies, which shows that fungi utilize most and Merino 2016; See et al. 2019) but also with stronger of rhizodeposition-derived C (Denef et al. 2009; Bai et al. leaching and more soil fauna (Xu et al. 2020). These can 2016) but offer global evidence that fungi especially explain why soil microbes are more reliant on above- mycorrhizal fungi rely much on root-derived C input. ground inputs in warmer and wetter forests. The lack of This finding is not surprising, because mycorrhiza fungi, correlation between microbial biomass under above- as a large fungal biomass pool, form symbiosis with the ground litter removal and experimental duration may be roots of over 90% plants (Brundrett and Tedersoo 2018) because soil microorganisms adjust their community and receive up to 22% of net photosynthetic products structure (Fig. 2a) or their C utilization strategies (Wang (Hobbie 2006). However, it is surprising that root exclu- et al. 2019) to maintain their biomass over time after re- sion stimulated bacterial biomass (Fig. 2b), as bacteria moving aboveground litter. also have high ability of utilizing root-derived C (Huang Surprisingly, the effect of root exclusion on the micro- et al. 2020). This may be due to that the loss of fungi bial biomass did not change with MAT or MAP (Fig. 3a with root exclusion alleviates the antagonistic effects to- and b). However, it should be noted that the existing wards bacterial growth (Schneider et al. 2010) and pro- two observations on microbial biomass in boreal forests vides their residues for utilization by bacteria (Ryckeboer remained unchanged under root exclusion (Fig. 4), et al. 2003; Apostel et al., 2018). which limits our ability to confirm whether root effects Given these diverse responses of microbial groups, our on microbial biomass is consistent across the globe. study offers new insights into the variations of the F/B Therefore, further studies should be carried out in these ratio associated with removing litter inputs, which was forests to provide a quantitative estimation of the re- stimulated by aboveground litter removal but decreased sponse of microbial biomass to root exclusion. While we by root exclusion (Fig. 2). This result suggests that the observed that the reductions in microbial biomass with Jing et al. Forest Ecosystems (2021) 8:38 Page 7 of 9 root exclusion became larger as experimental duration finding further brings a challenge to describe the effects went longer (Figs. 3c and 4), lacking a saturating re- of multiple drivers on the response ratio of microbial sponse and suggesting that root effects on microorgan- biomass, which is similar to many other meta-analysis isms is lasting and deepening. Long-term root exclusion studies that lacking sufficient associated measurements leads to a shift in microbial utilization from labile C (Ren et al. 2017; Yang et al. 2020). Therefore, microbial pools to recalcitrant C pools in soils (Pisani et al. 2016; community and soil property responses should be exam- Wu et al. 2018). Given that fungi have high ability of ined simultaneously under the context of removing lit- utilizing recalcitrant C compounds as described above ters in future experimental research. Despite above- (Strickland and Rousk 2010; Meng et al. 2020), signifi- mentioned limitations, our study is the first meta- cant inhibitions in fungi with root exclusion (Fig. 2b) is analysis elucidating litter roles in the microbial commu- likely unable to meet the microbial C needs for growth, nity and providing a global picture for understanding and ultimately decreasing microbial biomass over time. the relative importance of above- versus belowground Furthermore, the long-term root exclusion has less com- litter in regulating the microbial community in forest pensation effect from dead roots, because nearly 92% ecosystems. fine roots and 80% coarse roots are decomposed beyond three-year according to global root decomposition rate Conclusions (Silver and Miya 2001). This time-dependent effect of To our knowledge, this current meta-analysis study is root litter indicates that the root importance on soil mi- the first global syntheses to quantitatively evaluate the croorganisms would be underestimated by short-term roles of above- and belowground litter on the soil micro- experiments. Thus, more long-term experiments con- bial community in forest ecosystems. Our synthesis ducted in forest ecosystems are urgently needed to gain showed that root litter was stronger than aboveground insights into microbial responses to root exclusion at the litter for microbial biomass worldwide. More import- global scale. antly, the root effect amplified over time, but effect of Although factors controlling the responses of micro- aboveground litter was dependent on climate (i.e., forest bial biomass to aboveground litter removal and root ex- biomes). Furthermore, removing litter from above- and clusion differed, we did observe that the greater belowground shifted the microbial community structure influence of belowground litter inputs on the soil micro- in the opposite direction, which could have profound bial biomass than aboveground litter inputs is consistent but different effects on the global soil C cycle. These across diverse forest biomes (expect boreal forests) and findings highlight the importance and different roles of treatment durations (Fig. 4). Similarly, 35.7% studies, aboveground and root litters, which should be fully con- which simultaneously removing aboveground and below- sidered when predicting microbe-mediated processes ground litters, showed that the effects of roots on micro- and establishing forest management strategies with a bial biomass are larger than that of aboveground litter in changing climate. temperate forests (Wang et al. 2017a; vanden Enden et al., 2018) and sub/tropical forests (Wang et al. 2017b; Wu et al. 2018; Liu et al. 2019). We thus emphasize that Supplementary Information C allocation should be considered when projecting The online version contains supplementary material available at https://doi. org/10.1186/s40663-021-00318-8. microbe-derived soil C changes in response to climate change and forest managements in forest ecosystems. Additional file 1: Fig. S1. The root removal effect on microbial biomass However, the generally weak accounts of variations in by trenching and girdling methods. The numbers in the right of figure microbial biomass under litter exclusion by all variables represents the number of case studies. Fig.S2. Effects of ALR and RE on dissolved organic carbon. The numbers in the right of figure represents considered here point to the complex nature of micro- the number of case studies. ALR, above-ground litter removal; RE, root ex- bial responses to litter exclusion. Climatic variables indi- clusion. Table S1. Correlation coefficients of the effect size of sol micro- vidually accounted for 24% of the overall variations in bial biomass and F/B ratio to above-ground litter removal (ALR) and root exclusion (RE) with climatic variables and soil properties microbial biomass under aboveground litter removal, whereas the experimental duration and DOC explained 50.2% of changes in microbial biomass under root exclu- Acknowledgements sion. Although litter exclusion significantly influences We thank the anonymous reviewers for helpful suggestions on manuscript preparation. soil temperature and soil moisture (Xu et al. 2013; Zhang et al. 2020), which may alter microbial responses due to their close linkages (Wang et al. 2019; Rasmussen Authors’ contributions YJ designed the study, data preparation, analysis, and wrote the paper. QW et al. 2020), we did not observe these soil properties in- provided the paper editing. PT and WL participated in the data preparation fluence microbial response to litter exclusion based on and processing. ZS and HY provided suggestion to improve the paper our limited number of observations (Table S1). This quality. All the authors read and approved the final manuscript. Jing et al. 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Journal

"Forest Ecosystems" – Springer Journals

Published: Jun 17, 2021

Keywords: Forest ecosystems, soil microorganisms; Fungi; Litter; Root; Carbon input; Meta-analysis

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