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Positive soil priming effects are the rule at a global scale

Article in Global Change Biology · September 2024

DOI: 10.1111/gcb.17502

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Received: 30 June 2024 | Revised: 18 August 2024 | Accepted: 27 August 2024

DOI: 10.1111/gcb.17502

RESEARCH ARTICLE

Positive soil priming effects are the rule at a global scale

Shengwen Xu1 | Manuel Delgado-­Baquerizo2 | Yakov Kuzyakov3,4 | Yan Wu1 |

Lihu Liu1 | Yuyi Yang5 | Yaying Li6,7 | Yongxiang Yu1 | Biao Zhu8 |
1,6,7
Huaiying Yao
1
Research Center for Environmental Ecology and Engineering, School of Environmental Ecology and Biological Engineering, Wuhan Institute of Technology,
Wuhan, China
2
Laboratorio de Biodiversidad y Funcionamiento Ecosistémico, Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain
3
Department of Agricultural Soil Science, Department of Soil Science of Temperate Ecosystems, University of Göttingen, Göttingen, Germany
4
Peoples Friendship University of Russia (RUDN University), Moscow, Russia
5
Hubei Key Laboratory of Wetland Evolution & Ecological Restoration, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China
6
Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, Ningbo Urban Environment Observation and Research Station, Chinese
Academy of Sciences, Ningbo, China
7
Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China
8
Institute of Ecology and Ministry of Education Key Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University,
Beijing, China

Correspondence
Yongxiang Yu and Huaiying Yao, Research Abstract
Center for Environmental Ecology and
Priming effects of soil organic matter decomposition are critical to determine carbon
Engineering, School of Environmental
Ecology and Biological Engineering, budget and turnover in soil. Yet, the overall direction and intensity of soil priming re-
Wuhan Institute of Technology, Wuhan
mains under debate. A second-­order meta-­analysis was performed with 9296-­paired
430205, China.
Email: [email protected]; [email protected] observations from 363 primary studies to determine the intensity and general direc-
tion of priming effects depending on the compound type, nutrient availability, and
Funding information
MCIN/AEI/10.13039/501100011033, ecosystem type. We found that fresh carbon inputs induced positive priming effects
Grant/Award Number: I + D + i project
(+37%) in 97% of paired observations. Labile compounds induced larger priming ef-
PID2020-­115813RA-­I 00; RUDN
University Strategic Academic fects (+73%) than complex organic compounds (+33%). Nutrients (e.g., N, P) added
Leadership Program; China Scholarship
with organic compounds reduced the intensity of priming effects compared to com-
Council, Grant/Award Number:
NO. 202408420228; China pounds without N and P, reflecting “nutrient mining from soil organic matter” as one
Scholarship Council, Grant/Award
of the main mechanisms of priming effects. Notably, tundra, lakebeds, wetlands, and
Number: TED2021-­130908B-­C41/
AEI/10.13039/501100011033/Uni; volcanic soils showed much larger priming effects (+125%) compared to soils under
National Natural Science Foundation of
forests, croplands, and grasslands (+24…+32%). Our findings highlight that positive
China, Grant/Award Number: 42021005,
42477135 and 42277109 priming effects are predominant in most soils at a global scale. Optimizing strategies
to incorporate fresh organic matter and nutrients is urgently needed to offset the
priming-­induced accelerated organic carbon turnover and possible losses.

KEYWORDS
nutrient availability, second-­order meta-­analysis, soil organic carbon, soil priming effect,
terrestrial ecosystems

Glob Change Biol. 2024;30:e17502. wileyonlinelibrary.com/journal/gcb © 2024 John Wiley & Sons Ltd. | 1 of 10
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1 | I NTRO D U C TI O N published meta-­analyses. We compiled the intensity of PEs depend-

ing on compound type, nutrient availability, and ecosystem type
Soil is the largest organic carbon (C) pool in terrestrial ecosystems that are commonly considered in meta-­analyses. By integrating the
(Jobbágy & Jackson, 2000). Changes in the decomposition rates of quality and redundancy of primary studies into a multilevel meta-­
soil organic matter (SOM) are of major concern for climate change analytical model, we aimed to: (1) provide a robust overall estimate
policy agendas regarding organic carbon stocks and carbon dioxide of the intensity of global PEs, and (2) determine the intensity of PEs
(CO2) emissions (Lal, 2004; Lal et al., 2004). Fresh C inputs from under common scenarios.
natural (e.g., plant litter and rhizodeposition from living roots) and
anthropogenic (e.g., fertilizers, compost, and biochar) sources con-
tribute to soil C sequestration. However, they could also accelerate 2 | M ATE R I A L S A N D M E TH O DS
SOM decomposition, leading to the release of CO2 through micro-
bial mineralization (Guenet et al., 2018). The changes in microbial 2.1 | Systematic literature survey, inclusion
mineralization of SOM in response to pulses or continuous inputs criteria, and data extraction
of fresh C are known as priming effects (PE; Kuzyakov, 2010). Fresh
C inputs could accelerate microbial mineralization of SOM, referred We collected peer-­reviewed meta-­analyses on the PEs using the
to as “positive PE”, and lead to accelerations of C turnover in soils. Web of Science (http://​w ww.​webof​knowl​edge.​com) and China
Alternatively, C inputs can retard the microbial mineralization of National Knowledge Infrastructure (http://​w ww.​cnki.​net). The last
SOM, referred to as “negative PE”, which would increase C seques- search was done on April 12, 2024, using the following search string:
tration in soils over a long period (Liu et al., 2020). While current TS = (meta-­analysis OR review) AND (soil OR terrestrial) AND (“prim-
earth system models (ESMs) suggest that C inputs primarily increase ing effect” OR “decomposition” OR “mineralization”). The screened
SOC stocks, there is an imperative need to increase the accuracy 95 full-­text papers have been checked manually for the following
of ESMs to account for contradictory SOC responses due to PEs inclusion criteria. Retained meta-­analyses had to (i) examine the
(IPCC, 2019). intensity of soil PE under controlled or field conditions, (ii) analyze
Growing understanding of the PE as a mediator of delicate C the effects of one or several factors on PE intensity, (iii) specify the
balance between soil and atmosphere has rekindled interest, with type of effect size for the PE (e.g., natural log-­transformed response
70% of studies on the topic of soil PE published in the last decade ratios and Hedges'd), and (iv) present adequate statistics corre-
(Bernard et al., 2022; Heimann & Reichstein, 2008). Yet, much un- sponding to effect sizes (confidence intervals (CI), standard errors
certainty remains regarding the intensity and direction of PE due to (SE), and number of observations). Finally, 12 meta-­analyses were
the complex microbial mechanisms involved, which arise from differ- retained (Table S1). The detailed list can be found in the Supporting
ences in compound complexity, nutrient availability, and ecosystem Information. The effect sizes and 95% CIs were extracted from the
types, leading to variable and sometimes conflicting results (Hamer text or figures (using WebPlotDigitizer, https://​autom​eris.​io/​WebPl​
& Marschner, 2005; Qiao et al., 2014). Whilst mechanisms remain otDig​itizer.​html) for subsequent analyses.
elusive, a basic understanding of the intensity and direction of PE
is crucial to guide agricultural management and sequester C in soils
(Singh et al., 2010). 2.2 | Data aggregation
The global patterns of direction and intensity of PEs have been
gradually revealed in studies and supported by first-­order meta-­ The outcomes of published meta-­analyses were categorized into
analyses (Mo et al., 2022; Sun et al., 2019). These statistically inde- three common categories: (i) Compound type comprised of complex
pendent and methodologically comparable first-­order meta-­analyses (plant-­derived or polymerized carbon such as plant residues, biochar
examined the intensity of PEs in different contexts, such as response etc.) and labile (soluble low molecular weight organic compounds
to crop residue inputs and nutrient additions (Feng & Zhu, 2021; Qin, such as glucose and amino acids) compounds; (ii) Nutrient availability
Chen, et al., 2024). Thus far, there is a lack of synthesized results of comprised of compounds without nitrogen (N) and phosphorus (P;
global PE intensity on these existing meta-­analyses. A second-­order Comp without N, P), compounds containing N (Comp con N), com-
meta-­analysis provides a systematic approach to combine mean ef- pounds containing P (Comp con P), and compounds containing N and
fect sizes across first-­order meta-­analyses that report the intensity P (Comp con N, P); (iii) Ecosystem type comprised of cropland, for-
of PEs. This approach provides the overall estimate of the global PE est, grassland, and others (tundra, lakebeds, wetlands, and volcanic
intensity by augmenting sample size and assessing the quality and soils). The detailed descriptions of these categories and correspond-
overlap of primary studies included in first-­
order meta-­
analyses ing effect sizes and metrics can be found on the Figshare repository
(Bergquist et al., 2023; Oh, 2020). Quantitative synthesis of global (Data S1, 10.6084/m9.figshare.25603185). In each included meta-­
soil PE intensity helps determine the contribution of the PE to SOM analysis, the effect size of PE was expressed in percent change (%)
decomposition in ESMs. or natural log-­transformed response ratios (lnRR), or Hedges'd. The
Here, we take up the challenge to reveal the general pattern ratios were converted into percent changes, allowing us to compare
of PEs through an up-­
to-­
date and comprehensive evaluation of effects between meta-­analyses (Equation (1)).
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XU et al. 3 of 10

Percent change of PE ( % ) = (exp (lnRR) − 1) × 100 (1) proposed by Beillouin et al. (2022, 2023). Briefly, we assessed each
meta-­analysis based on eight criteria (a score of 1 was allocated
In addition, due to standardized mean difference metrics for those fulfilling the description (0 if not), total score = 8), serving
(Hedges'd) containing negative numbers and insufficient informa- as a quality proxy (specific criteria are detailed in Table S3). The
tion, it was not possible to transform the Hedges'd into percentage pseudo-­correlation (Cor (x, y)) between meta-­analyses was es-
changes (Hedges et al., 1999). The recorded pairwise data of primary timated as Cor (x, y) = (2 × m/(n1 + n2)), where m is the number of
studies were provided by the corresponding authors upon our re- overlapped primary studies, while n1 and n2 represent the total
quest. We calculated the percent change of PE using the following number of primary studies in two respective (x and y) meta-­analysis
formula (Equation (2)). (Figure S1; Beillouin et al., 2023). We thus calculated a variance–co-
variance matrix based on quality scores and pseudo-­correlations.
Caddition − Ccontrol
Percent change of PE ( % ) = × 100 (2) The covariance was calculated from pseudo-­correlation (Cor (x, y))
Ccontrol
and variance (Var, weighted by the quality score) of the two meta-­
Where Ccontrol and C addition are SOC-­derived CO2-­C in control analyses (Equation (5); Doi & Thalib, 2008).
and substrate addition treatment, respectively. All effect sizes in
(5)
√ √
Covariance = Cor (x, y) × Var (x) × Var (y)
retained meta-­analyses (including effect sizes k = 66) have been con-
verted into percent changes. Three meta-­analyses considered the The covariance matrix is incorporated as the adjusted variance in
decomposition of SOM over time and removed temporal dependen- the multilevel meta-­analytical model. All steps described above are
cies, wherein repeated measurements within incubations were ag- implemented in the R package “MetaSynthesis” (https://​github.​com/​
gregated into an overall mean. For specific procedures and details, dbeil​louin/​​MetaS​ynthesis).
please see Liao et al. (2008). Overall, the multilevel meta-­analytical model used to estimate
the overall percent change in PE is nested with random effects (mul-
tiple effect sizes were nested in each meta-­analysis cluster). The
2.3 | Second-­order meta-­analysis number of primary studies corresponding to a specific moderator is
often unavailable within the meta-­analysis. Therefore, a simplified
To estimate the overall effect of factors on PE, we adapted a mul- mixed-­
effect model, without considering the quality and redun-
tilevel meta-­analytical model (Beillouin et al., 2023). This model dancy of primary studies nor the clustering of effect sizes, was used
encompassed a variance–covariance matrix considering the preci- to determine the effects of moderators on PE.
sion, quality, and redundancy of retained first-­order meta-­analyses
(Equation (3)).
2.4 | Statistical and sensitivity analyses
Yij = μ + βi + φij + εij (3)

Where Yij is the jth effect size of the ith meta-­analysis (one meta-­ Restricted maximal likelihood (REML) estimation was used in all
analysis may correspond to several effect sizes), μ is the mean es- meta-­analytical models (Langan et al., 2019). Estimates were pre-
timated effect, βi is the random meta-­analysis effect size between sented in percent change of PE with their 95% CI in brackets. The
meta-­analyses (between-­cluster heterogeneity), φij is the random omnibus tests for moderators (QM indicates heterogeneity among
effect size effect within the ith meta-­analysis (within-­cluster hetero- the studies, and I2 indicates the variation across studies that is
geneity), and ε ij is the sampling error associated with the jth effect due to heterogeneity rather than chance) were also reported
th
size of the i meta-­analysis (sampling error). (Viechtbauer, 2007). All meta-­analytical models were conducted
The weight of each effect size is determined by the inverse of using the R package “metafor” (version 4.4–0; Viechtbauer, 2010).
its variance to account for sample size and sampling error (Marín-­ The model results were plotted by the package “orchaRd” (version
Martínez & Sánchez-­Meca, 2010). The variance was calculated from 2.0; Nakagawa et al., 2023). The multiple comparisons among mod-
the mean and confidence interval (Equation (4)). erators were conducted using the general linear hypotheses in pack-
age “multcomp” (version 1.4–25).
Variance = (abs (CI − mean)∕1.96)2 (4)
Publication bias, where studies with significant outcomes are
The quality of individual meta-­analyses depends on the clarity of preferentially published, was assessed with the funnel plot (publica-
inclusion and exclusion criteria, the evaluation of model heteroge- tion bias considered present if p ≤ .05 in Egger's test) and Rosenthal's
neity, or the assessment of publication bias (Beillouin et al., 2022). method of fail-­safe numbers (Rosenthal, 1979). DFBETAS values (i.e.,
Additionally, pairwise meta-­analyses exhibited pseudo-­correlation, how many standard deviations the estimated coefficients change
where effect sizes were non-­independent due to the inclusion of after excluding the ith case from the model) in leave-­one-­out diag-
repeated primary studies (Nakagawa et al., 2017). We then cor- nostics were also calculated to identify the presence of outliers and
rected the results of the multilevel model considering the quality influential cases (any DFBETAS values larger than 1; Viechtbauer &
and non-­independence of the meta-­analyses, following the strategy Cheung, 2010).
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4 of 10 XU et al.

3 | R E S U LT S and wetlands with standard deviations >1) that greatly affected the
results. After exclusions, the average PE intensity was 28% (SE = 4%;
3.1 | Positive priming effects are dominant at a Figure S2).
global scale

The retained 12 meta-­analyses met the criteria for the second-­ 3.2 | Priming effects depend on compound type,
order meta-­analysis and included 363 primary studies. Most (8 of nutrient availability, and ecosystem type
12) meta-­analyses collected primary studies on a global scale. A
large number of paired observations (i.e., treatment versus con- Fresh compound inputs, regardless of the type, contributed to
trol, n = 9296) were included in our dataset. The commonly con- positive PEs: a + 33% increase after additions of complex organic
sidered factors were nutrient availability (n = 9296), followed by compounds, and a + 73% increase after additions of labile com-
ecosystem type (n = 8005). Paired observations regarding com- pounds (Figure 3). The intensity of PE induced by labile compounds
pound types were mainly from PE induced by complex organic was higher than that induced by complex compounds (α = 10%,
compounds (e.g., biochar, straw, and litter residues). Nutrient avail- p = .06). Compared with compounds without N and P, intensities
ability observations were mainly from PE induced by compounds of PEs induced by compounds containing N, and P either alone or
without N and P (e.g., glucose, cellulose, or sucrose). Besides com- together were lower (albeit with little influence on the model out-
mon ecosystem types (croplands, forests, and grasslands), some come, QM = 2.6, p > .05). In contrast, ecosystem type as a modera-
studies investigated PE in tundra, lakebeds, wetlands, and volcanic tor explained a large proportion of the variance (QM = 11.8, p < .01;
soils (i.e., others; Figure 1, Figure S1). Table S5). PEs in tundra, lakebeds, wetlands, and volcanic soils (i.e.,
Globally, most (n = 9003) reported paired observations were others) were extremely higher (+125%) than those in most upland
positive PEs (i.e., lower 95% CI >0 in meta-­analyses; Figure 2a). The soils under croplands, forests, or grasslands (p < .05; Figure 4).
variance of individual effect sizes in the multilevel model was ad-
justed for meta-­analysis quality scores and non-­independence. The
multilevel model revealed that the average PE intensity was 37% 4 | DISCUSSION
(increase in SOC-­derived CO2-­C loss due to compound inputs com-
pared with controls) to date (Figure 2b). There was asymmetry in the Our study reveals positive PEs are the most prevalent in terrestrial
funnel plot, indicating publication bias. A leave-­one-­out diagnostic ecosystems worldwide. To our knowledge, this is the most com-
identified one study (the one meta-­analysis reported PE in tundra prehensive second-­
order meta-­
analysis dataset on the PE topic.

F I G U R E 1 Distribution of changes in priming effects (PE) depending on compound type, nutrient availability, and ecosystem type (left
panel). Each point represents an effect size in retained meta-­analyses. The truncated violin plot represents the distribution of effect sizes
within each of the categories, with 25, 50, and 75% quantiles (k represents the number of effect sizes). The paired observations (n) for each
category were shown in pie charts (right panel). Comp without N, P: Compounds without N and P; Comp con N: Compounds containing N;
Comp con P: Compounds containing P; Comp con N, P: Compounds containing N and P.
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XU et al. 5 of 10

F I G U R E 2 The number of paired observations reporting positive (lower 95% CI >0), negative (upper 95% CI <0), and no change (95% CI
overlapping zero) priming effects among included meta-­analyses (a). Cumulative forest plot of all included effect sizes from meta-­analyses.
Scores represent the quality assessment of the meta-­analyses and are further used to adjust the variance. Bold numbers indicate overall
estimates in the multilevel meta-­analytical model (b). Comp without N, P: Compounds without N and P; Comp con N: Compounds containing
N; Comp con P: Compounds containing P; Comp con N, P: Compounds containing N and P.

We estimate that the priming-­induced SOM loss is 37% (increase biochar (as a complex compound) was overestimated in acidic soils
in SOC-­derived CO2) to date, with most (97%) paired observations because carbonates within biochar ash were neutralized and re-
being positive PEs (Figure 2). This suggests that fresh C inputs ac- leased as CO2 (Luo et al., 2011).
celerate SOM decomposition globally, with negative consequences Compared with the intensified positive PE (+50%) induced by
for soil-­derived CO2 mitigation and climate regulation. organic compounds without N and P, additions of compounds with
Labile compounds, mainly include small and soluble organic nutrients (N, P, alone or together) suppressed SOM decomposition.
molecules (e.g., glucose and amino acids), induced higher positive Both negative and positive PEs were common by additions of com-
PEs than complex compounds, such as plant-­d erived or polymer- pounds with nutrients (Figure 3). This finding implies that increased
ized C (e.g., biochar; Figure 3, Figure 4). Available C and N, in the nutrient availability decreases SOM decomposition. If attempts are
soluble part of labile compounds, will accelerate respiratory ac- made to interpret our results at the local scale, we follow the es-
tivity and extracellular enzyme production by internal microbial tablished conceptual model that links microbial nutrient mining and
metabolism. This leads to accelerated SOC mineralization through stoichiometric decomposition theories (Li et al., 2023). Specifically,
“microbial activation” and “triggering effect” (Fang et al., 2018; in soils with few available N or P, the releases of microbial extracel-
Kuzyakov et al., 2000). However, the relationship between the in- lular enzymes and decomposition rates of SOM are accelerated if
tensity of PEs and compound type cannot be simply interpreted. compounds containing N or P match the stoichiometric C: N: P ratios
In soils with N limitation, the lack of N in labile compounds may of decomposers (i.e., stoichiometric decomposition theory; Chen
deoptimize the nutrient status of soil microorganisms, and thus et al., 2014). In contrast, in soils well supplied with N or P, increased
suppress microbial mineralization of SOM (Fontaine et al., 2003). nutrient availability could suppress the N or P mineralization from
The disregarded soil properties (especially pH) also weakened the SOM (i.e., microbial nutrient mining; Feng et al., 2021). Globally, PEs
associations between compound type and PE intensity based on reduced by nutrient addition may attributed to most investigated
changes in CO2 efflux from soils, yielding inconsistent conclu- soils (especially cropland soils) being free of N or P limitation (Batool
sions (Wang & Kuzyakov, 2024). For example, the PE induced by et al., 2022; Ringeval et al., 2024).
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6 of 10 XU et al.

F I G U R E 3 Orchard plot showing the

mean estimates of percent change (%)
of PE with red circles, 95% confidence
interval with thick whisker, and 95%
prediction interval with thin whisker.
Bold numbers indicate estimates in model
results while asterisks denote statistical
significance (**p < .01, ***p < .001). k
represents the number of effect sizes
within each category (A). Comp without
N, P: Compounds without N and P; Comp
con N: Compounds containing N; Comp
con P: Compounds containing P; Comp
con N, P: Compounds containing N and P.

PEs in tundra, lakebed, wetland, and volcanic soils with high and grassland soils, but all PEs were positive (Perveen et al., 2019).
SOC densities and stocks are disproportionately less investigated This reaffirms the universality of positive PEs, but variations in PE
compared to other ecosystem types (Ding et al., 2023; Maes cannot be attributed to land use only. Previous meta-­analyses at-
et al., 2024; Wilhelm et al., 2022; Figure 1). Intensive positive PEs tributed the difference in PE intensity to SOC content among eco-
were common in tundra, lakebeds, wetlands, and volcanic soils systems, suggesting that lower SOC content induces higher PEs (Luo
compared to most upland soils (Figure 4). Microbial mineralization et al., 2016; Sun et al., 2019). Overall, our results support the idea
is constrained primarily due to low temperatures (in tundra soils), that the SOM decomposition is a widespread strategy of microbial
recalcitrant properties of SOC (in volcanic soils), high carbon burial nutrient acquisition since positive PEs were maintained despite dif-
rates and associated hydrological anaerobic conditions (in lakebeds ferent land uses.
and wetlands soils; Hicks et al., 2022; Iimura et al., 2020; Johnston This study has several broader implications. First, our work indi-
et al., 2019; Steinmuller et al., 2019). Thus, the compound inputs can cates that PEs are mostly positive worldwide, suggesting a substan-
readily alleviate the energy limitation for microbial metabolism and tial acceleration of SOM decomposition in response to the entrance
enzyme production and stimulate the SOC decomposition (Wang & of fresh carbon into the soil system. This knowledge is critical to
Kuzyakov, 2023). Consistent with previous reports of quantified PEs properly predict atmosphere-­
soil carbon balance across biomes.
from various land uses across five continents, our results showed Our study further indicates that complex compounds, such as
the absence of difference in the PE intensity among cropland, forest, plant-­derived or polymerized carbon, reduce PEs compared to labile
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XU et al. 7 of 10

F I G U R E 4 Multiple comparisons results in subgroups. Error bars represent plus or minus SE of the mean, asterisks denote statistical
difference (*p < .05, Holm adjusted). The text next to the arrows represents the microbial mechanisms corresponding to changes in PE
intensity (B). Comp without N, P: Compounds without N and P; Comp con N: Compounds containing N; Comp con P: Compounds containing
P; Comp con N, P: Compounds containing N and P.

F I G U R E 5 Conceptual figure
describing the change of priming effects
(PE) intensity depending on compound
type, nutrient availability, and ecosystem
type. Without N, P: Compounds without
N and P; con N: Compounds containing N;
con P: Compounds containing P; con N, P:
Compounds containing N and P.

compounds. Encouraged by this, mixing plant residues of different increase in microbial respiration and CO2 release due to the acceler-
quality and combining biochar application with conventional fertil- ated turnover of microbial biomass, without actual decomposition of
ization regimes could be effective management in mitigating CO2 SOM) and real (long-­term increase in CO2 release from the enhanced
emissions from agroecosystems (Pingthaisong et al., 2024; Rasul mineralization of SOM) PEs (Blagodatskaya & Kuzyakov, 2008). To
et al., 2022). Based on the soil nutrient status, optimized applica- quantitatively evaluate the primed C from SOM decomposition, the
tions of nitrogen and phosphorus can reduce PEs while alleviating microbial biomass must be considered as an active driver, as well as
nutrient limitation and suppressing microbial mining of SOM (Qin, a separate active pool (Blagodatsky et al., 2010). Therefore, we may
Feng, et al., 2024). However, there are limitations that need to be overestimate the CO2 release from SOC decomposition since the ap-
acknowledged in our second-­order meta-­analysis. It is not possi- parent PEs mediated by microbial respiration and biomass turnover
ble from the available data to distinguish the apparent (short-­term are indistinguishable.
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13652486, 2024, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17502 by Huaiying Yao - Cas-Institute Of Urban Environment , Wiley Online Library on [09/09/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8 of 10 XU et al.

5 | CO N C LU S I O N S DATA AVA I L A B I L I T Y S TAT E M E N T

The data that supports the findings of this study are available in the
Our second-­
order meta-­
analysis provided critical insights into supplementary material of this article. Datasets are openly available
the overall direction and magnitude of priming effects globally. in Figshare at https://​doi.​org/​10.​6084/​m9.​figsh​are.​25603185.
(i) Organic compound inputs caused positive (+37%) priming ef-
fects in soils globally, with most observations (97%) reporting ORCID
positive PEs. Consequently, priming commonly accelerates SOM Shengwen Xu https://orcid.org/0000-0002-0534-0835
decomposition and turnover. (ii) Labile compounds caused larger Manuel Delgado-­Baquerizo https://orcid.
positive PEs (+73%) than complex organic compounds (+33%). (iii) org/0000-0002-6499-576X
Increased nutrient (N, P, alone or together) availability reduced Yakov Kuzyakov https://orcid.org/0000-0002-9863-8461
the intensity of PEs and potentially benefited SOC sequestration. Yan Wu https://orcid.org/0009-0005-5027-3474
iv) PEs in tundra, lakebeds, wetlands, and volcanic soils were four Lihu Liu https://orcid.org/0000-0001-7026-769X
times higher than those in most upland soils under croplands, for- Yuyi Yang https://orcid.org/0000-0001-9807-6844
ests, or grasslands (Figure 5). This knowledge is critical to better Yaying Li https://orcid.org/0000-0002-4053-1952
understand how fresh C inputs will influence the soil-­atmosphere Yongxiang Yu https://orcid.org/0000-0002-4282-947X
C balance on our planet. Biao Zhu https://orcid.org/0000-0001-9858-7943
Huaiying Yao https://orcid.org/0000-0002-1932-8765
AU T H O R C O N T R I B U T I O N S
Shengwen Xu: Conceptualization; data curation; formal analy- REFERENCES
sis; methodology; software; visualization; writing – original Batool, M., Sarrazin, F. J., Attinger, S., Basu, N. B., Van Meter, K., & Kumar,
draft; writing – review and editing. Manuel Delgado-­Baquerizo: R. (2022). Long-­term annual soil nitrogen surplus across Europe
(1850–2019). Scientific Data, 9(1), 612. https://​doi.​org/​10.​1038/​
Conceptualization; supervision; writing – review and editing. Yakov
s4159​7-­​022-­​01693​-­​9
Kuzyakov: Conceptualization; writing – review and editing. Yan Wu: Beillouin, D., Cardinael, R., Berre, D., Boyer, A., Corbeels, M., Fallot, A.,
Data curation. Lihu Liu: Writing – review and editing. Yuyi Yang: Feder, F., & Demenois, J. (2022). A global overview of studies about
Writing – review and editing. Yaying Li: Writing – review and ed- land management, land-­use change, and climate change effects
on soil organic carbon. Global Change Biology, 28(4), 1690–1702.
iting. Yongxiang Yu: Conceptualization; data curation; funding ac-
https://​doi.​org/​10.​1111/​gcb.​15998​
quisition; methodology; writing – review and editing. Biao Zhu: Beillouin, D., Corbeels, M., Demenois, J., Berre, D., Boyer, A., Fallot, A.,
Conceptualization; writing – review and editing. Huaiying Yao: Feder, F., & Cardinael, R. (2023). A global meta-­analysis of soil or-
Conceptualization; funding acquisition; project administration; re- ganic carbon in the Anthropocene. Nature Communications, 14(1),
3700. https://​doi.​org/​10.​1038/​s 4146​7-­​023-­​39338​-­​z
sources; supervision; writing – review and editing.
Bergquist, M., Thiel, M., Goldberg, M. H., & van der Linden, S. (2023).
Field interventions for climate change mitigation behaviors: A
AC K N OW L E D G M E N T S second-­order meta-­analysis. Proceedings of the National Academy
We sincerely thank all colleagues who provided published data of Sciences, 120(13), e2214851120. https://​doi.​org/​10.​1073/​pnas.​
for our second-­order meta-­analysis. This research was supported 22148​51120​
Bernard, L., Basile-­Doelsch, I., Derrien, D., Fanin, N., Fontaine, S., Guenet,
by the National Natural Science Foundation of China (42021005,
B., Karimi, B., Marsden, C., & Maron, P.-­A . (2022). Advancing the
42477135, 42277109). S. X. acknowledges support from the China mechanistic understanding of the priming effect on soil organic
Scholarship Council (CSC) under the NO. 202408420228. Y. K. ac- matter mineralisation. Functional Ecology, 36(6), 1355–1377. https://​
knowledges support from RUDN University Strategic Academic doi.​org/​10.​1111/​1365-­​2435.​14038​
Blagodatskaya, Е., & Kuzyakov, Y. (2008). Mechanisms of real and appar-
Leadership Program. M. D-­B. acknowledges support from TED2021-­
ent priming effects and their dependence on soil microbial biomass
130908B-­C41/AEI/10.13039/501100011033/Unión Europea and community structure: Critical review. Biology and Fertility of
NextGenerationEU/PRTR and the Spanish Ministry of Science Soils, 45(2), 115–131. https://​doi.​org/​10.​1007/​s0037​4-­​008-­​0334-­​y
and Innovation for the I + D + i project PID2020-­115813RA-­I 00 Blagodatsky, S., Blagodatskaya, E., Yuyukina, T., & Kuzyakov, Y. (2010).
Model of apparent and real priming effects: Linking microbial ac-
funded by MCIN/AEI/10.13039/501100011033. We gratefully ac-
tivity with soil organic matter decomposition. Soil Biology and
knowledge Jiguang Feng, Xiaojie Li, and Xudong Wang from Peking Biochemistry, 42(8), 1275–1283. https://​doi.​org/​10.​1016/j.​soilb​io.​
University, Peng Tian from Anhui Agricultural University, as well as 2010.​0 4.​0 05
Chaorong Ge, Haoxin Fan, Ningguo Zheng, and Chuyuan Liao from Chen, R., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., Lin,
X., Blagodatskaya, E., & Kuzyakov, Y. (2014). Soil C and N availabil-
Wuhan Institute of Technology for their invaluable assistance.
ity determine the priming effect: Microbial N mining and stoichio-
metric decomposition theories. Global Change Biology, 20(7), 2356–
C O N FL I C T O F I N T E R E S T S TAT E M E N T 2367. https://​doi.​org/​10.​1111/​gcb.​12475​
The authors declare that they have no known competing financial Ding, Y., Wang, D., Zhao, G., Chen, S., Sun, T., Sun, H., Wu, C., Li, Y.,
Yu, Z., Li, Y., & Chen, Z. (2023). The contribution of wetland plant
interests or personal relationships that could have appeared to influ-
litter to soil carbon pool: Decomposition rates and priming effects.
ence the work reported in this paper.
 |

13652486, 2024, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17502 by Huaiying Yao - Cas-Institute Of Urban Environment , Wiley Online Library on [09/09/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
XU et al. 9 of 10

Environmental Research, 224, 115575. https://​doi.​org/​10.​1016/j.​en- Lal, R., Griffin, M., Apt, J., Lave, L., & Morgan, M. G. (2004). Managing
vres.​2023.​115575 soil carbon. Science, 304(5669), 393. https://​doi.​org/​10.​1126/​scien​
Doi, S. A. R., & Thalib, L. (2008). A quality-­effects model for meta-­ ce.​1093079
analysis. Epidemiology, 19(1), 94–100. https://​doi.​org/​10.​1097/​EDE.​ Langan, D., Higgins, J. P. T., Jackson, D., Bowden, J., Veroniki, A. A.,
0b013​e3181​5c24e7 Kontopantelis, E., Viechtbauer, W., & Simmonds, M. (2019). A com-
Fang, Y., Nazaries, L., Singh, B. K., & Singh, B. P. (2018). Microbial mech- parison of heterogeneity variance estimators in simulated random-­
anisms of carbon priming effects revealed during the interaction of effects meta-­analyses. Research Synthesis Methods, 10(1), 83–98.
crop residue and nutrient inputs in contrasting soils. Global Change https://​doi.​org/​10.​1002/​jrsm.​1316
Biology, 24(7), 2775–2790. https://​doi.​org/​10.​1111/​gcb.​14154​ Li, X. J., Feng, J. G., Zhang, Q. F., & Zhu, B. (2023). Warming inhibits
Feng, J., Tang, M., & Zhu, B. (2021). Soil priming effect and its responses the priming effect of soil organic carbon mineralization: A meta-­
to nutrient addition along a tropical forest elevation gradient. analysis. Science of the Total Environment, 904, 8. https://​doi.​org/​10.​
Global Change Biology, 27(12), 2793–2806. https://​doi.​org/​10.​1111/​ 1016/j.​scito​tenv.​2023.​166170
gcb.​15587​ Liao, C., Peng, R., Luo, Y., Zhou, X., Wu, X., Fang, C., Chen, J., & Li, B.
Feng, J., & Zhu, B. (2021). Global patterns and associated drivers of (2008). Altered ecosystem carbon and nitrogen cycles by plant in-
priming effect in response to nutrient addition. Soil Biology and vasion: A meta-­analysis. New Phytologist, 177(3), 706–714. https://​
Biochemistry, 153, 108118. https://​doi.​org/​10.​1016/j.​soilb​io.​2020.​ doi.​org/​10.​1111/j.​1469-­​8137.​2007.​02290.​x
108118 Liu, X.-­J. A., Finley, B. K., Mau, R. L., Schwartz, E., Dijkstra, P., Bowker, M.
Fontaine, S., Mariotti, A., & Abbadie, L. (2003). The priming effect of A., & Hungate, B. A. (2020). The soil priming effect: Consistent across
organic matter: A question of microbial competition? Soil Biology ecosystems, elusive mechanisms. Soil Biology and Biochemistry, 140,
and Biochemistry, 35(6), 837–843. https://​doi.​org/​10.​1016/​S0038​ 107617. https://​doi.​org/​10.​1016/j.​soilb​io.​2019.​107617
-­​0717(03)​0 0123​-­​8 Luo, Y., Durenkamp, M., De Nobili, M., Lin, Q., & Brookes, P. C. (2011).
Guenet, B., Camino-­Serrano, M., Ciais, P., Tifafi, M., Maignan, F., Soong, Short term soil priming effects and the mineralisation of biochar
J. L., & Janssens, I. A. (2018). Impact of priming on global soil carbon following its incorporation to soils of different pH. Soil Biology and
stocks. Global Change Biology, 24(5), 1873–1883. https://​doi.​org/​10.​ Biochemistry, 43(11), 2304–2314. https://​doi.​org/​10.​1016/j.​soilb​io.​
1111/​gcb.​14069​ 2011.​07.​020
Hamer, U., & Marschner, B. (2005). Priming effects in soils after com- Luo, Z. K., Wang, E. L., & Sun, O. J. (2016). A meta-­analysis of the tempo-
bined and repeated substrate additions. Geoderma, 128(1), 38–51. ral dynamics of priming soil carbon decomposition by fresh carbon
https://​doi.​org/​10.​1016/j.​geode​rma.​2004.​12.​014 inputs across ecosystems. Soil Biology & Biochemistry, 101, 96–103.
Hedges, L. V., Gurevitch, J., & Curtis, P. S. (1999). The meta-­analysis of https://​doi.​org/​10.​1016/j.​soilb​io.​2016.​07.​011
response ratios in experimental ecology. Ecology, 80(4), 1150–1156. Maes, S. L., Dietrich, J., Midolo, G., Schwieger, S., Kummu, M., Vandvik,
https://​d oi.​o rg/​10.​1890/​0 012-­​9658(1999)​0 80[1150:​T MAORR]​ V., Aerts, R., Althuizen, I. H. J., Biasi, C., Björk, R. G., Böhner, H.,
2.0.​CO;​2 Carbognani, M., Chiari, G., Christiansen, C. T., Clemmensen, K.
Heimann, M., & Reichstein, M. (2008). Terrestrial ecosystem carbon dy- E., Cooper, E. J., Cornelissen, J. H. C., Elberling, B., Faubert, P., …
namics and climate feedbacks. Nature, 451(7176), 289–292. https://​ Dorrepaal, E. (2024). Environmental drivers of increased ecosys-
doi.​org/​10.​1038/​natur​e 06591 tem respiration in a warming tundra. Nature, 629(8010), 105–113.
Hicks, L. C., Yuan, M., Brangarí, A., Rousk, K., & Rousk, J. (2022). Increased https://​doi.​org/​10.​1038/​s 4158​6-­​024-­​07274​-­​7
above-­and belowground plant input can both trigger microbial ni- Marín-­Martínez, F., & Sánchez-­Meca, J. (2010). Weighting by inverse
trogen mining in subarctic tundra soils. Ecosystems, 25(1), 105–121. variance or by sample size in random-­ effects meta-­analysis.
https://​doi.​org/​10.​1007/​s1002​1-­​021-­​00642​-­​8 Educational and Psychological Measurement, 70(1), 56–73. https://​
Iimura, Y., Tanaka, D., Nagao, S., Fujitake, N., & Ohtsuka, T. (2020). doi.​org/​10.​1177/​0 0131​6 4409​3 44534
The mineralization rate of black soil carbon in the deep layers of Mo, F., Ren, C., Yu, K., Zhou, Z., Phillips, R. P., Luo, Z., Zhang, Y., Dang,
Japanese volcanic ash soil may be easily accelerated by labile car- Y., Han, J., Ye, J.-­S., Vinay, N., Liao, Y., Xiong, Y., & Wen, X. (2022).
bon supply. Soil Science and Plant Nutrition, 66(3), 415–420. https://​ Global pattern of soil priming effect intensity and its environmental
doi.​org/​10.​1080/​0 0380​768.​2020.​1753481 drivers. Ecology, 103(11), e3790. https://​doi.​org/​10.​1002/​ecy.​3790
IPCC. (2019). Climate change and land: IPCC special report on climate Nakagawa, S., Lagisz, M., O'Dea, R. E., Pottier, P., Rutkowska, J., Senior,
change, desertification, land degradation, sustainable land manage- A. M., Yang, Y., & Noble, D. W. A. (2023). orchaRd 2.0: An R pack-
ment, food security, and greenhouse gas fluxes in terrestrial ecosystems. age for visualising meta-­analyses with orchard plots. Methods in
Jobbágy, E. G., & Jackson, R. B. (2000). The vertical distribution of soil Ecology and Evolution, 14(8), 2003–2010. https://​doi.​org/​10.​1111/​
organic carbon and its relation to climate and vegetation. Ecological 2041-­​210X.​14152​
Applications, 10(2), 423–436. https://​doi.​org/​10.​1890/​1051-­​ Nakagawa, S., Noble, D. W. A., Senior, A. M., & Lagisz, M. (2017). Meta-­
0761(2000)​010[0423:​T VDOSO]​2.0.​CO;​2 evaluation of meta-­analysis: Ten appraisal questions for biologists.
Johnston, E. R., Hatt, J. K., He, Z., Wu, L., Guo, X., Luo, Y., Schuur, E. A. G., BMC Biology, 15(1), 18. https://​doi.​org/​10.​1186/​s1291​5-­​017-­​0357-­​7
Tiedje, J. M., Zhou, J., & Konstantinidis, K. T. (2019). Responses of Oh, I.-­S. (2020). Beyond meta-­analysis: Secondary uses of meta-­analytic
tundra soil microbial communities to half a decade of experimental data. Annual Review of Organizational Psychology and Organizational
warming at two critical depths. Proceedings of the National Academy Behavior, 7(1), 125–153. https://​doi.​org/​10.​1146/​annur​ev-­​orgps​
of Sciences, 116(30), 15096–15105. https://​doi.​org/​10.​1073/​pnas.​ ych-­​01211​9-­​045006
19013​07116​ Perveen, N., Barot, S., Maire, V., Cotrufo, M. F., Shahzad, T., Blagodatskaya,
Kuzyakov, Y. (2010). Priming effects: Interactions between living and E., Stewart, C. E., Ding, W., Siddiq, M. R., Dimassi, B., Mary, B., &
dead organic matter. Soil Biology and Biochemistry, 42(9), 1363– Fontaine, S. (2019). Universality of priming effect: An analysis using
1371. https://​doi.​org/​10.​1016/j.​soilb​io.​2010.​0 4.​0 03 thirty five soils with contrasted properties sampled from five conti-
Kuzyakov, Y., Friedel, J. K., & Stahr, K. (2000). Review of mechanisms and nents. Soil Biology and Biochemistry, 134, 162–171. https://​doi.​org/​
quantification of priming effects. Soil Biology and Biochemistry, 32(11), 10.​1016/j.​soilb​io.​2019.​03.​027
1485–1498. https://​doi.​org/​10.​1016/​S0038​-­​0717(00)​00084​-­​5 Pingthaisong, W., Blagodatsky, S., Vityakon, P., & Cadisch, G. (2024).
Lal, R. (2004). Soil carbon sequestration impacts on global climate Mixing plant residues of different quality reduces priming effect and
change and food security. Science, 304(5677), 1623–1627. https://​ contributes to soil carbon retention. Soil Biology and Biochemistry,
doi.​org/​10.​1126/​scien​ce.​1097396 188, 109242. https://​doi.​org/​10.​1016/j.​soilb​io.​2023.​109242
 |

13652486, 2024, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17502 by Huaiying Yao - Cas-Institute Of Urban Environment , Wiley Online Library on [09/09/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 of 10 XU et al.

Qiao, N., Schaefer, D., Blagodatskaya, E., Zou, X., Xu, X., & Kuzyakov, Viechtbauer, W. (2007). Accounting for heterogeneity via random-­
Y. (2014). Labile carbon retention compensates for CO2 released effects models and moderator analyses in meta-­analysis. Journal of
by priming in forest soils. Global Change Biology, 20(6), 1943–1954. Psychology, 215(2), 104–121. https://​doi.​org/​10.​1027/​0 044-­​3409.​
https://​doi.​org/​10.​1111/​gcb.​12458​ 215.2.​104
Qin, J. J., Chen, N., Scriber, K. E., II, Liu, J. B., Wang, Z. Q., Yang, K. J., Viechtbauer, W. (2010). Conducting meta-­analyses in R with the metafor
Yang, H. Q., Liu, F. H., Ding, Y. Y., Latif, J., & Jia, H. Z. (2024). Carbon package. Journal of Statistical Software, 36(3), 1–48. https://​doi.​org/​
emissions and priming effects derived from crop residues and their 10.​18637/​​jss.​v 036.​i03
responses to nitrogen inputs. Global Change Biology, 30(1), 16. Viechtbauer, W., & Cheung, M. W.-­L . (2010). Outlier and influence di-
https://​doi.​org/​10.​1111/​gcb.​17115​ agnostics for meta-­analysis. Research Synthesis Methods, 1(2), 112–
Qin, W., Feng, J., Zhang, Q., Yuan, X., Zhou, H., & Zhu, B. (2024). Nitrogen 125. https://​doi.​org/​10.​1002/​jrsm.​11
and phosphorus addition mediate soil priming effects via affecting Wang, C., & Kuzyakov, Y. (2023). Energy use efficiency of soil microor-
microbial stoichiometric balance in an alpine meadow. Science of ganisms: Driven by carbon recycling and reduction. Global Change
the Total Environment, 908, 168350. https://​doi.​org/​10.​1016/j.​scito​ Biology, 29(22), 6170–6187. https://​doi.​org/​10.​1111/​gcb.​16925​
tenv.​2023.​168350 Wang, C., & Kuzyakov, Y. (2024). Soil organic matter priming: The pH
Rasul, M., Cho, J., Shin, H.-­S., & Hur, J. (2022). Biochar-­induced priming effects. Global Change Biology, 30(6), e17349. https://​doi.​org/​10.​
effects in soil via modifying the status of soil organic matter and 1111/​gcb.​17349​
microflora: A review. Science of the Total Environment, 805, 150304. Wilhelm, R. C., Lynch, L., Webster, T. M., Schweizer, S., Inagaki, T. M.,
https://​doi.​org/​10.​1016/j.​scito​tenv.​2021.​150304 Tfaily, M. M., Kukkadapu, R., Hoeschen, C., Buckley, D. H., &
Ringeval, B., Demay, J., Goll, D. S., He, X., Wang, Y.-­P., Hou, E., Matej, Lehmann, J. (2022). Susceptibility of new soil organic carbon to
S., Erb, K.-­H., Wang, R., Augusto, L., Lun, F., Nesme, T., Borrelli, P., mineralization during dry-­ wet cycling in soils from contrasting
Helfenstein, J., McDowell, R. W., Pletnyakov, P., & Pellerin, S. (2024). ends of a precipitation gradient. Soil Biology and Biochemistry, 169,
A global dataset on phosphorus in agricultural soils. Scientific Data, 108681. https://​doi.​org/​10.​1016/j.​soilb​io.​2022.​108681
11(1), 17. https://​doi.​org/​10.​1038/​s 4159​7-­​023-­​02751​-­​6
Rosenthal, R. (1979). The file drawer problem and tolerance for null re-
sults. Psychological Bulletin, 86(3), 638–641. https://​doi.​org/​10.​ S U P P O R T I N G I N FO R M AT I O N
1037/​0 033-­​2909.​86.3.​638
Additional supporting information can be found online in the
Singh, B. K., Bardgett, R. D., Smith, P., & Reay, D. S. (2010). Microorganisms
and climate change: Terrestrial feedbacks and mitigation options. Supporting Information section at the end of this article.
Nature Reviews Microbiology, 8(11), 779–790. https://​doi.​org/​10.​
1038/​nrmic​ro2439
Steinmuller, H. E., Dittmer, K. M., White, J. R., & Chambers, L. G. (2019).
Understanding the fate of soil organic matter in submerging coastal How to cite this article: Xu, S., Delgado-­Baquerizo, M.,
wetland soils: A microcosm approach. Geoderma, 337, 1267–1277. Kuzyakov, Y., Wu, Y., Liu, L., Yang, Y., Li, Y., Yu, Y., Zhu, B., &
https://​doi.​org/​10.​1016/j.​geode​rma.​2018.​0 8.​020 Yao, H. (2024). Positive soil priming effects are the rule at a
Sun, Z. L., Liu, S. G., Zhang, T. A., Zhao, X. C., Chen, S., & Wang, Q. K.
global scale. Global Change Biology, 30, e17502. https://doi.
(2019). Priming of soil organic carbon decomposition induced by
exogenous organic carbon input: A meta-­analysis. Plant and Soil, org/10.1111/gcb.17502
443(1–2), 463–471. https://​doi.​org/​10.​1007/​s1110​4-­​019-­​04240​-­​5

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