Ecological Indicators 160 (2024) 111771

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original Articles

Global patterns of the interactive effects of N and P enrichment on

terrestrial microbial biomass
Shucheng Li a, 1, Shijie Zhang b, 1, Shiming Tang c, *, Sumei Duan a, Qingqin Shao a, Qiuwen Zhan a,
Ke Jin c
a
College of Agriculture, Anhui Science and Technology University, Feng yang 233100, China
b
Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical
Garden Mem. Sun Yat-Sen), No. 1 Qianhuhoucun, Zhongshanmen, Xuanwu District, Nanjing 210014, China
c
Key Laboratory for Model Innovation in Forage Production Efficiency, Ministry of Agriculture and Rural Affuirs, Institute of Grassland Research, Chinese Academy of
Agricultural Sciences, Hohhot 010010, China

A R T I C L E I N F O A B S T R A C T

Keywords: Nitrogen (N) and phosphorus (P) are key components in biogeochemical cycling and considerable efforts have
Interactive effect been made to understand the effects of their availability on microbial biomass. Nevertheless, the interplay be­
Meta-analysis tween N and P supply in modulating soil microbes remains unclear. We conducted a comprehensive global
Nitrogen addition
analysis of 108 studies spanning boreal to tropical regions to evaluate their interactive impacts on microbial
Phosphorus addition
Soil microbial biomass
biomass. The findings revealed a significant decrease in microbial biomass with N addition, whereas P supple­
mentation resulted in a notable increase in microbial biomass. Among the observed interactive effects, additive
effects were predominant. More importantly, we found that among all of the assessed factors, the impacts of N-P
interaction on soil microorganisms are dependent on changes in soil pH. In conclusion, our findings provide
valuable insights into the interactive effects of N and P enrichment on microbial biomass. These findings will
contribute to the development of global models that predict the impacts of N and P enrichment on soil microbes
and ecosystem functions.

1. Introduction understanding of the impact of N–P interactions on microbial biomass.

Soil microorganisms constitute a significant proportion of genetic
diversity within ecosystems and play indispensable roles in various
crucial ecological processes (Bardgett and van der Putten, 2014; Karhu
et al., 2014). Nitrogen (N) and phosphorus (P) are frequently limiting
soil elements that exert significant impacts on the growth of soil mi­
croorganisms, consequently modifying terrestrial functions (Liu et al.,
2012; Zhang et al., 2018). Over the course of 100 years, N inputs to the
terrestrial biosphere are estimated to be approximately twice as high as
the rate of P deposition (Peñuelas et al., 2012; IPCC, 2013). An imbal­
anced supply of N and P can exacerbate P limitation or result in co-
limitation of both nutrients, leading to significant impacts on microbi­
al biomass (Fleischer et al., 2019). Despite the growing body of research
on the effects of N and P addition on microorganisms, there is still
limited knowledge regarding their interactive effects and the underlying
mechanisms. Therefore, it is crucial to obtain a comprehensive
Numerous studies have demonstrated that both N and P addition can
individually affect microbial biomass (Wei et al., 2018; Ma et al., 2021).
N is an essential nutrient that plays a crucial role in the synthesis of
proteins and nucleic acids, which are vital for microbial metabolism and
growth; thus increased N availability can lead to an increase in microbial
biomass (Zhang et al., 2019). P is an essential nutrient for various
cellular processes including energy transfer, cell division, and nucleic
acid synthesis, such that P addition can also stimulate microbial growth
(Wu et al., 2022). However, compared to the individual effects of N and
P, their interactive effects on microbial biomass can be more complex.
Several studies have reported synergistic interactions, in which con­
current addition of N and P leads to higher microbial biomass than that
anticipated based on individual nutrient amendments (Molina-Herrera
and Romanya, 2015). This finding suggests that the combined avail­
ability of N and P can have a more pronounced effect on microbial
growth compared to either nutrient alone (Fleischer et al., 2019).

* Corresponding author.
E-mail address: tangsm001@126.com (S. Tang).
1
Equally contributed to this work.

https://doi.org/10.1016/j.ecolind.2024.111771
Received 12 December 2023; Received in revised form 14 February 2024; Accepted 17 February 2024
Available online 23 February 2024
1470-160X/© 2024 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-
nc/4.0/).
S. Li et al.
Fig. 1. Site locations studies included in this study. Shapes represent the types of ecosystems as indicated in the legend (a). Effects of N addition, P addition, and both
N and P addition on soil microbial biomass. Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero indicates no significance (b). The
numbers on the right side of the graph represent the quantity of observed values.
However, antagonistic interactions between N and P supply have also
been observed (Jiang et al., 2021). In N-rich conditions, the impact of P
addition on microbial biomass may be limited because N excess can
inhibit the uptake and utilization of P by microorganisms (Güsewell and
Gessner, 2009). Similarly, high P availability can suppress N fixation by
diazotrophic bacteria, leading to N limitation and subsequent reduction
in microbial biomass (Allgeier et al., 2011). All of these findings high­
light the complex and dynamic nature of nutrient interactions and their
impact on soil microbial communities. Further studies at the global scale
are needed to elucidate the underlying mechanisms and assess the im­
plications for ecosystem function and sustainability.
Interactions between N and P can have synergistic, antagonistic, or
neutral effects on microbial growth depending on various factors such as
precipitation, mean annual temperature, amendment duration, and
ecosystem type (Vitousek et al., 2010; Liu et al., 2013; He and Dijkstra,
2014; Li et al., 2024). Precipitation exerts control over soil nutrient
availability by modulating nutrient leaching and downward migration
(He and Dijkstra, 2014). Increased precipitation can lead to leaching of
N and P, reducing their availability and thereby limiting microbial
growth and metabolism (He and Dijkstra, 2014). Temperature fluctua­
tions can alter the physiological activity and metabolic processes of
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Ecological Indicators 160 (2024) 111771
microorganisms, thereby modifying their response to N–P interactions;
at lower (higher) temperatures, microorganisms generally exhibit
slower (accelerated) physiological activities and metabolic processes
(Xiao et al., 2018). The biogeochemical N-P cycle also exhibits temporal
dimensions: in the short term, the enrichment of nutrients can stimulate
microbial growth as a result of the immediate accessibility of additional
N and P resources (Vitousek et al., 2010), whereas over the longer term,
the impacts of N and P enrichment become more intricate and multi­
faceted. Microbial communities have the capacity to alter to long-term
nutrient utilization strategy, which can potentially result in the stabili­
zation or even reduction of microbial biomass (Su et al., 2015). This
adaptation process may entail alterations in microbial community
composition, shifts in nutrient utilization strategies, and the emergence
of nutrient limitations beyond N and P (Su et al., 2015). In different
ecosystem types, the N–P ratio and abundance of available N and P re­
sources vary, thereby influencing the ecological functions and commu­
nity structure of microorganisms (Deng et al., 2017). Therefore, a
comprehensive study is needed to elucidate the interactive effects of N
and P enrichment on terrestrial microbial biomass.
Soil pH plays a crucial role in determining nutrient availability and
enzymatic activity, which can subsequently impact the response of soil
S. Li et al.
Fig. 2. Weighted Hedges’ d for the effects on microbial biomass (a–i), and the frequency distribution of interaction types in individual studies for soil microbes.
Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero indicates no significance.
microbes to N and P inputs (Lu et al., 2014; Chen et al., 2016). In soils
with neutral to slightly acidic pH, high N availability can lead to
increased microbial biomass. However, acidic soils often have limited P
availability; thus, in low-pH soils, excess N can exacerbate P limitation,
leading to reduced microbial biomass (Turner et al., 2013; Spohn and
Schleuss, 2019). Conversely, in alkaline soils, P can form insoluble salts
with calcium and magnesium ions, reducing their binding with N and
increasing N availability, promoting microbial growth and biomass
production (da Silva Cerozi and Fitzsimmons, 2016). Therefore, soil pH
can influence the interactive effects of nutrient availability, with
different pH conditions leading to different nutrient limitations and
microbial responses. By considering pH-dependent interactions, we can
develop better strategies for nutrient management and enhance soil
health.
In this meta-analysis, 108 studies (Fig. 1 and Data S1) were used to
evaluate microbial biomass dynamics in response to N and P addition.
We partitioned the dataset according to precipitation level (≤400 mm,
400–800 mm, >800 mm), temperature (≤15 ◦ C, >15 ◦ C), amendment
duration (≤3 years, >3 years), and ecosystem type (grassland, forest,
tundra) to evaluate differences in soil microbial biomass responses
among studies. We further evaluated the contributions of pH, nitrate
(NO−3 ), ammonium (NH+
4 ), N and P application rates, and environmental
factors to soil microbial biomass. Our objectives were to quantitatively
assess the individual and interactive impacts on microbial biomass at a
global scale and elucidate the key factors that drive these effects.
2. Materials and methods
2.1. Data collection
The data used in this study were acquired through comprehensive
searches conducted on the Web of Science, Google Scholar, and China
National Knowledge Infrastructure (CNKI) search engines. The terms
used were “elevated nitrogen” OR “nitrogen enrichment” OR “nitrogen”
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Ecological Indicators 160 (2024) 111771
OR “elevated phosphorus” OR “phosphorus enrichment” OR “phos­
phorus” AND “microbial biomass” OR “microbial community” OR “mi­
crobial abundance” OR “fungi” OR “bacteria” OR “soil respiration” OR
“microbial respiration” OR “litter decomposition” OR “microbial activ­
ity.” The dataset included studies ranging from 1980 to 2023. Only
primary studies were used to obtain data. The inclusion criteria were as
follows: direct addition of N and P fertilizers to an outdoor environment
comprising both control and treatment groups; N and P addition to
terrestrial ecosystems without laboratory incubation; single N (eN) or P
(eP) addition and combined N and P addition (eNP) were conducted
under the same conditions at the same time; means and sample sizes
were available or could be calculated. When data were graphically
presented, numerical data were obtained using Engauge Digitizer
version 4.1. When reporting experimental data for consecutive years, we
selected only data from the final year in accordance with the statistical
assumption of independence among observations. Additionally, publi­
cations incorporating multiple experiments under diverse conditions,
such as varying N application rate and ecosystems, were recorded as
distinct observations.
2.2. Meta-analysis
Individual effect sizes were quantified using the response ratio
(lnRR) of treatment and control groups. Detailed explanations of the
weighting factor (W), variance (v), and the weighted mean response
ratio (RR++) are provided in the Supporting Information.
2.3. Interactive effects
Interactive effects were quantified using Hedges’ d. Detailed expla­
nations of individual effect size and the effects of N addition (dN), P
addition (dP), and their interactive effect (dNP) are described in the
Supporting Information.
S. Li et al.
Fig. 3. The effects on microbial biomass in response to precipitation. Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero in­
dicates no significance.
2.4. Model selection
We corrected the Akaike information criterion for small samples
prior to model selection. A larger weight indicated higher importance of
a predictor in the models. These values are considered as support for
each variable among all models. To identify the most important pre­
dictors, we set a cutoff of 0.8 using the gmulti package in the R software
(R Core Team, Vienna, Austria) (Calcagno and de Mazancourt, 2010).
3. Results
3.1. Individual and combined effects on microbial biomass
We assessed the effects of both separate and combined additions of N
and P (NP) on soil microbial biomass to explore both the specific effects
of N and P as well as any potential interactive effects (Fig. S1). In our
comprehensive analysis of multiple studies, N addition led to significant
decreases in total microbial biomass (13.4 % average decrease), bacte­
rial biomass (16.1 %), fungal biomass (17.4 %), arbuscular mycorrhizal
fungi (AMF) biomass (30.5 %), and the fungal/bacterial biomass ratio
(F/B; 7.5 %); there were no significant effects on other microbial groups
(Fig. 1b). By contrast, P addition resulted in significant increases in total
microbial biomass (8.7 %), fungal biomass (10.4 %), gram-positive (GP;
29.1 %) and gram-negative (GN; 11.3 %) biomass, F/B (6.1 %,), and the
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Ecological Indicators 160 (2024) 111771
GP/GN ratio (8.3 %) (Fig. 1c). Combined N and P addition resulted in a
significant increase in F/B (19.1 %), with little effect on other soil mi­
crobial groups (Fig. 1d).
3.2. Interactive effects on microbial biomass
In our analysis, additive interactive effects were more frequently
observed compared to synergistic or antagonistic interactive effects
(Fig. 2j, k). Additive interactions were dominant for bacterial biomass
(52.8 %), fungal biomass (60.6 %), AMF biomass (72.7 %), actinomycete
(ACT) biomass (75 %), GP biomass (44.5 %), F/B (64.5 %), and GP/GN
(47.1 %). Antagonistic interactive effects were dominant for GN biomass
(55.6 %); synergistic effects were dominant for total microbial biomass
(42.9 %).
The dominance of additive interactions was not significantly altered
by precipitation levels (Fig. 3). However, total microbial biomass, GP
biomass, and GN biomass exhibited synergistic effects under high pre­
cipitation conditions (Fig. 3) and antagonistic effects under both low
precipitation and low temperature conditions (Fig. 4). The general
pattern of additive interactive effects did not change significantly with
time or ecosystem type (Figs. 5 and 6).
S. Li et al.
Fig. 4. The effects on microbial biomass in response to temperature. Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero indicates
no significance.
3.3. Influences of environmental and experimental factors
The model revealed that soil pH was the most important predictor of
Hedges’ d++ for soil microbial biomass (Fig. 7) among the potential
factors examined (pH, P and N application rates, mean annual temper­
ature and precipitation, and NO−3 and NH+ 4 levels). The RRs of total
microbial, bacterial, fungal, AMF, GP, and GN biomass for NP addition
exhibited significant positive linear correlations with the RR of pH
(Fig. 8). Soil microbial biomass responses to mean annual temperature
and precipitation, N and P application rates, and soil organic carbon (C),
available N, and available P levels were barely significant (Table 1).
4. Discussion
We gathered data from 1445 observations spanning terrestrial eco­
systems worldwide with the aim of evaluating the interactive impacts of
N and P supply on microbial biomass. Our findings provide global evi­
dence that additive effects significantly dominate interactive effects on
soil microbes, which is important for understanding the functionality
and stability of soil ecosystems. Furthermore, our findings revealed that
the responses of microbial biomass to the interactive effects of N and P
addition were profoundly modulated by soil pH. Overall, these findings
offer valuable insights into the patterns of interactive effects, which will
inform global models to improve predictions of soil microbial responses
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Ecological Indicators 160 (2024) 111771
to N and P deposition.
4.1. Individual and combined effects on soil microbial biomass
We observed significant reductions in microbial biomass subsequent
to N addition (Fig. 1b). One possible explanation is the alteration of
nutrient competition between microbes and plants (Kuzyakov and Xu,
2013). With an increase in N availability, plants and microorganisms
become more actively engaged in obtaining N resources to meet their
growth and reproductive needs, which can lead to intensified nutrient
competition between plants and microorganisms (Bardgett et al., 1999).
Another factor is that soil acidification induced by N can elevate the
osmotic potential of the soil solution (Broadbent, 1965) and promote the
formation of recalcitrant compounds (Vitousek et al., 1997), which can
significantly decrease microbial biomass. In contrast to N addition, P
enrichment had a positive effect on soil microbes (Fig. 1c). One possible
mechanism is that P addition can alleviate nutrient constraints, stimu­
lating microbial growth and promoting microbial biomass accumulation
(Spohn and Schleuss, 2019). Simultaneous N and P addition had a
neutral effect on microbial biomass (Fig. 1d). N and P are two major
limiting factors for microbial growth; when N and P are added simul­
taneously, their availability remains relatively balanced, alleviating the
limitations on microorganisms for an overall neutral effect (Merchant
and Helmann, 2012).
S. Li et al.
Fig. 5. The effects on microbial biomass in response to duration. Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero indicates no
significance.
4.2. Interactive effects on soil microbial biomass
Previous studies found divergent interactive effects, for example,
additive or antagonistic interactions, on soil microbial biomass under N
and P addition (Jiang et al., 2021). These differences may have been the
result of insufficient full-factorial design of experiments globally (All­
geier et al., 2011). By contrast, we found that interactive effects of N and
P on microbial biomass were primarily additive (Fig. 2). When N and P
are simultaneously increased, microbial biomass generally increases,
but the extent of the increase may be limited. Although N addition can
lead to changes in nutrient competition and soil acidification, P addition
can promote microbial growth and alleviate nutrient limitations (Grif­
fiths et al., 2012). The positive impact of P addition on microbial
biomass can potentially outweigh the negative effects of N addition,
resulting in a net positive response of microbial communities to nutrient
enrichment (Ma et al., 2023). This finding underscores the significance
of taking into account the interactive effects of multiple nutrients on soil
microbial communities and their reactions to nutrient inputs.
Precipitation level, mean annual temperature, supply duration, and
ecosystem type may be crucial for assessing the interactive effects of
nutrients on microbial biomass (Rinnan et al., 2007; Zhang et al., 2018).
For example, under low precipitation and low mean annual temperature
regimes, N and P availability may be limited and the interactive effects
on microbial biomass may be more pronounced (Khalili et al., 2016; Sun
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Ecological Indicators 160 (2024) 111771
et al., 2021). Similarly, the ecosystem type and duration of nutrient
supply can affect the extent to which microbial communities can adapt
and respond to changes in nutrient availability (Rinnan et al., 2007).
Therefore, to comprehensively evaluate discrepancies caused by envi­
ronmental and experiment factors, we varied precipitation levels, mean
annual temperature, supply duration, and ecosystem type and detected
very little effect on the previously observed additive interactions
(Figs. 3–6). This finding suggests that the observed additive interactions
of N and P addition on microbial biomass are robust and not easily
influenced, indicating that the interactive effects on microbial biomass
are consistent across different environmental conditions and experi­
mental setups (Davidson and Howarth, 2007; Vitousek et al., 2010). In
addition to dominant additive interactive effects on microbial biomass,
we also found antagonistic and synergistic interactive effects in dry and
humid regions, respectively (Fig. 3). In humid regions with high pre­
cipitation, plant N and P uptake is stimulated, leading to increased plant
biomass and subsequent release of C into the soil through root exudation
and litter decomposition (Li et al., 2021). This increased C availability
can act as a substrate for microbial growth. When N and P are added in
combination, they further enhance the availability of these nutrients,
creating a synergistic effect on soil microbial biomass (Adekiya et al.,
2020). Under low temperature conditions, N and P uptake may be
limited as microbial metabolic activity slows, resulting in reduced
nutrient demand. Therefore, at low temperatures, N excess and P
S. Li et al. Ecological Indicators 160 (2024) 111771

Fig. 6. The effects on microbial biomass in response to ecosystem type. Values are the mean ± 95 % confidence interval (CI), where a CI overlapping with zero
indicates no significance.

Fig. 7. Contributors of various predictors in response to the interactive effect. Model-averaged importance of predictor variables. Predictors with importance values
>0.8 are considered to be important.

limitation may occur simultaneously, leading to the inhibition of mi­ perspectives for designing terrestrial soil microbial biomass models.
crobial growth (Xiao et al., 2018). To promote microbial growth at low
temperatures, it is necessary to appropriately adjust the supply of both
nutrients to meet the requirements of microbes. Overall, the interactive
effects on microbial biomass observed in our study provide new

7
S. Li et al. Ecological Indicators 160 (2024) 111771

Fig. 8. Correlations between the response of microbial biomass and the response of soil pH.

Table 1
The effect of mean annual temperature (MAT), mean annual precipitation (MAP), N application rate, P application rate, SOC, available N and available P on response
(RR) of soil microbial biomass.
Variable MAT MAP N application rate P application rate SOC available N available P

df p df p df p df p df p df p df p

Total biomass 227 0.330 227 0.322 161 0.507 31 0.951 65 0.446 68 0.077 5 0.053
Bacterial biomass 229 0.257 232 0.153 150 0.061 38 0.876 87 0.893 71 0.801 22 0.968
Fungal biomass 244 0.139 247 0.006 166 0.023 38 0.05 78 0.495 79 0.859 22 0.879
AMF 85 0.203 85 0.171 61 0.000 10 0.061 29 0.233 31 0.219 na na
ACT 72 0.172 75 0.728 50 0.156 10 0.217 31 0.658 19 0.1 na na
GP 93 0.096 93 0.397 63 0.211 10 0.228 35 0.686 29 0.252 na na
GN 93 0.322 93 0.318 63 0.949 10 0.455 35 0.646 29 0.139 na na

Bold values indicate P ≤ 0.05.

4.3. Underlying mechanisms of the interactive effects on soil microbial soil pH, nutrient availability, and microbial communities is crucial for
biomass comprehending the ecological dynamics in soil ecosystems.

To further evaluate the underlying mechanisms driving the interac­
tive effects of N and P addition on microbial biomass, we tested the
effects of several variables including environmental factors and soil
physicochemical properties. Our analysis showed that pH changes were
the most important factor driving these interactive effects (Fig. 7 and
Table 1). Specifically, soil pH can modify the availability of N and P to
microorganisms. Nitrification, which is the conversion of ammonium to
nitrate, is pH-dependent, with optimal pH ranges for nitrifiers differing
from those of other microbial functional groups. Consequently, soil
acidification induced by N addition can affect the activity and compo­
sition of microbes involved in nitrogen cycling (Lu et al., 2014). Simi­
larly, the application of P fertilizers can alter the nutrient balance in the
soil, affecting the activity of soil microorganisms. Microbial metabolism
can produce acidic or alkaline substances, thereby influencing soil pH
(Mao et al., 2016). The combined effect of N and P additions is enhanced
or diminished depending on the specific pH conditions of the soil. The
significant correlation between microbial biomass and soil pH further
supported our results (Fig. 8). Together, our findings demonstrate that
soil pH can act as a driver of the interactive effects of N and P additions
on microbial biomass. Understanding the complex interplay between
4.4. Uncertainties and implications
The majority of previous experiments employed a unifactorial design
to investigate microbial responses to global changes, resulting in limited
data availability pertaining to reciprocal interactions between N and P.
Future studies can enhance the reliability and stability of their results by
expanding sample sizes and increasing the number of experimental
replicates. Moreover, the interactive effects of N and P addition can
influence the regulation of soil acidity, further altering the patterns of
N–P interactions. Unfortunately, the mechanisms underlying soil acidi­
fication from N–P interactions remain poorly understood, introducing
uncertainties in predicting microbial changes. Future efforts should aim
for a comprehensive understanding of the mechanisms governing global
N–P interactions, with a focus on the regulatory mechanisms of acidi­
fication, which will significantly contribute to the advancement of mi­
crobial transformation predictions.
5. Conclusion
In summary, our findings provide large-scale evidence that additive

8
S. Li et al.
interactions dominate the interactive effects of increased N and P
deposition on microbial biomass. Changes in soil pH play a vital role in
altering the interactive effects of nutrient supply on soil microbial
biomass at global scales, which will enhance our understanding of the
mechanism underlying these effects. Overall, our findings reconciled
conflicting evidence on a global scale and provide empirical estimates of
microbial biomass responses to N and P addition that will contribute to
improving predictions of soil microbial changes under increasing N and
P concentrations.
CRediT authorship contribution statement
Shucheng Li: Writing – original draft, Methodology, Data curation.
Shijie Zhang: Writing – original draft, Methodology, Data curation.
Shiming Tang: Funding acquisition, Conceptualization. Sumei Duan:
Writing – review & editing. Qingqin Shao: Writing – review & editing.
Qiuwen Zhan: Writing – review & editing. Ke Jin: Writing – review &
editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgments
We express our utmost gratitude to Professor Chen Hongyang for his
invaluable assistance in paper composition and data analysis. We extend
our thanks to Dr. Chen Lei for his insightful suggestions during the final
stages of manuscript revision. Additionally, we are deeply appreciative
of the unwavering support and assistance provided by my beloved
partner, Wei Aoping, throughout the writing process. We also extend our
gratitude to all colleagues and institutions who provided assistance
during the course of our paper composition, particularly Professor Wu
Yanpei for assistance in literature retrieval and data organization, as
well as the many authors who provided data support throughout our
research. Funding was provided by the Foundation of National Key R&D
Program of China (2022YFD1900300), Bringing Talents of Inner
Mongolia (2023NMRC003) the Natural Science Foundation of Inner
Mongolia (2021MS03081), the Foundation of Anhui Science and Tech­
nology University (NXYJ20192, 2021zrzd09), and the Natural Science
Foundation of Jiangsu Province (grant number BK20210166), the Open
Fund Project of Jiangsu Key Laboratory for the Research and Utilization
of Plant Resources (grant number JSPKLB202204), and the “Double
Innovation Doctor” Fund for High-Level Entrepreneurial and Innovative
Talents Introduction of Jiangsu Province of China (grant number
JSSCBS20211313(032102903)).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ecolind.2024.111771.
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