Journal of

Plant Ecology
Research Article
Seasonal droughts drive up carbon gain in a subtropical
forest
Brian Njoroge1,2,3, Yuelin Li1,2,3,*, Dennis Otieno4,5, Shizhong Liu1,2,3, Simin Wei1,2,3,

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Ze Meng1,2, Qianmei Zhang1,2, Deqiang Zhang1,2, Juxiu Liu1,2,3, Guowei Chu1,2,
Fasih Ullah Haider1,2 and John Tenhunen5
1
Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy
of Sciences, Guangzhou 510650, China, 2Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden,
Chinese Academy of Sciences, Guangzhou 510650, China, 3University of Chinese Academy of Sciences, Beijing 100039, China,
4
Department of Botany, Jaramogi Oginga Odinga University of Science and Technology, Bondo 210-40601, Kenya, 5Department of Plant
Ecology, University of Bayreuth, 95440 Bayreuth, Germany

*Corresponding author. E-mail: yuelin@scib.ac.cn, yuelin.li@uni-bayreuth.de

Handling Editor: Geoff Wang

Received: 7 June 2022, First Decision: 23 July 2022, Accepted: 20 August 2022, Online Publication: 7 September 2022

Abstract
The study aimed to show that droughts are increasing in frequency and intensity in the Dinghushan Biosphere
Reserve and to illustrate the effects of seasonal droughts on carbon gain in a subtropical forest. This is in response
to the threat posed by increased droughts due to global climate change. We used four drought indices to
accurately determine periods of drought and periods of increased precipitation. Thereafter, the measured eddy
ux and soil moisture content data collected from 2003 to 2014 were compared between the droughts and
wet periods to determine drought impacts on the ecosystem carbon gain. Drought accounted for about 20%
of the 12-year study period, with the highest drought events and severity occurring between 2012 and 2013.
The average annual precipitation and air temperature during the study period were 1404.57 ± 43.2 mm and
22.65 ± 0.1 °C, respectively, showing a decrease of 523 mm in precipitation and an increase of 2.55 °C in
temperature, compared with the 30-year records (1990–2020). Contrary to most published data for most forest
ecosystems globally, Dinghushan Biosphere Reserve recorded signicant carbon gain during 60% of the drought
period.
Keywords drought, climate change, carbon gain, Dinghushan Biosphere Reserve, eddy ux

季节性干旱驱动亚热带森林的碳积累
摘要本研究旨在表明处于南亚热带的鼎湖山生物圈保护区的干旱频率和强度正在增加并说明季节性
干旱对亚热带森林碳积累的影响。这是为了应对全球气候变化导致的干旱加剧所带来的威胁开展的一项
研究。我们使干旱指数(标准化降水指数、标准降水蒸散发指数、降水距平百分率及自校准帕尔默干旱
指数)准确确定干旱期和降水量增加期。此后将2003至2014年(12年)监测采集的实测涡动通量和土壤
含水量数据在干旱期和湿润期之间进行比较以确定干旱对生态系统碳积累的影响。在本研究所选择的
12年期间干旱的发生时间约占比20%最强干旱事件和严重程度发生于2012至2013年。研究期间的
年平均降水量和气温分别为1404.57 ± 43.2 mm和22.65 ± 0.1 °C与30年记录(1990–2020)相比较年

© The Author(s) 2022. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits
unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

JOURNAL OF PLANT ECOLOGY | https://doi.org/10.1093/jpe/rtac088 1

 降水量减少量可达523 mm而气温则增加了2.55 °C。与全球针对大多数森林生态系统研究所发表的数
据呈相反趋势处于中国南亚热带区域的鼎湖山生物圈保护区在60%的干旱期内所监测的森林生态系统
记录到显著的碳积累趋势说明季节性干旱驱动了森林的碳积累。
关键词干旱气候变化碳积累鼎湖山生物圈保护区涡动通量
Graphical Abstract
INTRODUCTION
Dinghushan Biosphere Reserve plays an important
role in the socioeconomic development of the
Guangdong–Hong Kong–Macao Greater Bay area
(GD–HK–MO) (Zhou et al. 2018). As China’s rst
UNEP-designated nature reserve, it has remained
preserved over time, especially those areas with
special relevance such as around the Buddhist temple,
which has remained undisturbed for more than 400
years. Because of its long history and its geographical
location, the reserve acts as a monitoring forest site
dedicated to the evaluation of the effect of China’s
forestry conservation measures and is sensitive to
increasing instances of drought under a background
of global climate change (Fu et al. 2010; Li et al. 2021).
Drought is dened as a period of shortages in
a region’s water supply, whether as atmospheric
precipitation, surface water or below groundwater
(Barrett and Robertson 2021; Gao et al. 2021; Nikravesh
et al. 2020; Stahl et al. 2020). It can be declared after
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only 15 days of precipitation shortfall and can be
prolonged, lasting for months or years (Bittencourt et
al. 2020; Dikshit et al. 2021). Drought can be caused by
several factors such as extremely low precipitation and
high atmospheric temperatures, leading to increased
evaporation (Aadhar and Mishra 2020; Mishra et
al. 2021). Droughts can have devastating effects on
natural forest ecosystems, agroecosystems, local
economies and the general human wellbeing (Haile
et al. 2020; Lu et al. 2020; Mata-Gonzalez et al. 2021;
Waseem et al. 2021; Yang et al. 2020; Zhang et al. 2022).
The process where carbon is extracted from the
atmosphere and xed into plants is referred to as
‘carbon gain’. It is an integral indicator of a plant’s
tness in its natural environment (Krna and Rapson
2013). Carbon gain is calculated by subtracting
carbon losses due to respiration (Re) and tissue loss
(e.g. consumption by herbivores) from a plant’s
primary production (GPP) (Arehart et al. 2020; Ward
2020).
 Subtropical forests, account for approximately
one-third of global terrestrial gross primary
productivity and sequester one-half of global carbon
i.e. directly stored in terrestrial vegetation as carbon
gain (Hofhansl et al. 2020; Qiu et al. 2020; Zhang et al.
2020). The question of how droughts affect tropical
forests’ carbon gain has been studied in long-term
experimental drought studies where various forest
dynamics were tracked after exposure to drought
conditions (da Costa et al. 2010; Rennenberg et
al. 2006). Drought was found to reduce carbon
gain and even alter forest composition in the long
term (Engelbrecht et al. 2007; Xiao et al. 2021).
Increased frequency of droughts globally has been
predicted using climate models and has been shown
to negatively affect carbon gain and other forest
ecosystem services (Bottero et al. 2017). How tropical
forest ecosystems respond to increasing drought,
especially in the context of climate change, is of great
signicance to the eld of forest ecology (Konings et
al. 2021). It remains uncertain whether subtropical
forests will increase carbon gain as the frequency
of droughts increases (Jehanzaib et al. 2020; Li et
al. 2020; Zhang et al. 2020) thus necessitating our
study.
Dinghushan Biosphere Reserve is a subtropical
monsoon broadleaf forest that has recorded instances
of droughts in the past (Li et al. 2021). Recent climate
simulations show increased drought frequencies and
intensities associated with global climate change,
with unknown consequences on the subtropical
regions (Chen et al. 2020; Omer et al. 2020). This
calls for the need to investigate how the Dinghushan
Biosphere Reserve will respond to changing climate
and how droughts will affect carbon gain. The
objective of this study, therefore, aimed to (i) identify
periods of drought using the four different drought
indices, (ii) examine the effects of seasonal droughts
on carbon gain in the Dinghushan Biosphere Reserve
and (iii) identify the link between droughts and
carbon gain in the Dinghushan Biosphere Reserve.
Guided by previous research done in the Dinghushan
Biosphere Reserve (Li et al. 2012), we hypothesize
that droughts increase carbon gain in the Dinghushan
Biosphere Reserve.
MATERIALS AND METHODS
Site description
The study site was Dinghushan Biosphere Reserve,
a subtropical monsoon evergreen forest located
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
between 23°09ʹ21″ and 23°11ʹ30″ N and 112°30ʹ39″
and 112°33ʹ41″ E in Dinghu District, Zhaoqing City,
Guangdong Province, at the northwest of the Pearl
River Delta (Liu et al. 2022). The reserve has an area
of 1150 ha and is among the rare subtropical forest
ecosystems located near the Tropic of Cancer (Liu et
al. 2021). Dinghushan Biosphere Reserve spreads
out along a vertical spectrum of 14 m up to 1000 m
above sea level (Li et al. 2020). The climate is a humid
subtropical monsoon with an annual sunshine rate of
32.8% and a 30-year average (1990–2020) sunshine
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duration of 1432.7 h annually (Ren et al. 2021). This
region has rainy and drought periods with an annual
temperature average of 20.1 °C and precipitation of
1927 mm (Li et al. 2021). Maximum precipitation and
warm temperatures span from April to September
(the rainy season) and minimum precipitation and
cold temperatures span from October to March (the
dry season) (Li et al. 2012). The total short-wave
solar radiation is 104.8–116.6 kcal cm−1 yr−1 (Liu et
al. 2021). Below 700 m altitude, the soil is mainly
latosol with a soil pH range of 4.5–6.0 (Liu et al.
2021). The vegetation types are mainly subtropical
monsoon evergreen forest, coniferous broadleaved
broadleaved forest, shrub grass, bamboo, etc. (Liu et
al. 2020). The vegetation community structure can
be categorized into two sublayers of trees, a shrub
layer, an herb layer and the lowest is the seedling
layer (Zou et al. 2020). The leaf area index ranges
between 3.7 and 4.2 m2 m−2 at a 95% canopy density
(Li et al. 2012). The data we present were from the
ux tower set at a sampling plot called ‘Wukesong’
Dinghushan Biosphere Reserve ecosystem station
Zhaoqing is located in a coniferous broad-leaved
mixed forest plot (23°10ʹ24″ N, 112°32ʹ10″ E);
Fluxnet Site Code: CN-Din at an altitude of 300 m
and a southeast-facing slope at about 10 °C (Zhang
et al. 2017a). The most widespread species was Pinus
massoniana planted over 20 years from 1930 to 1950
and has now formed a semi-natural forest after
secondary succession; it was planted because of the
invasion by Castanopsis chinensis, Lindera metcalana
and Cryptocarya concinna (Li et al. 2021; Ren et al.
2021). Flora is rich, comprising of greater than 1740
plant species (Wei et al. 2020).
Meteorological data collection
CNR1 net radiometer (Kipp & Zonen’s CM3 ISO-
class, thermopile pyranometer, CG3 pyrgeometer,
PT100 RTD, Campbell Scientic, USA) and
Kipp & Zonen CM 11 pyranometer (Hydromet,
3
Netherlands) were used to measure solar radiation
reaching the top of the tower. Rainfall was
measured with a tipping bucket rain gauge (52203,
R. M. Young Company, MI, USA). Wind velocity
and wind direction were measured with a cup
anemometer (A100R and W200P, respectively,
Vector Instruments, UK). Photosynthetically active
radiation was measured using two sensors namely,
the Li190SB (LI-COR Inc., USA) and LQS70-
10 (Apogee, Logan, UT, USA). Temperature and
humidity were measured at heights of 4, 9, 15, 21,
27, 31 and 36 m using the IRTS-P (Apogee, Logan,
UT, USA) and the HMP45C (Campbell Inc., USA)
sensors. At a depth of 5, 20, 40, 80 and 100 cm the
CS616 (Campbell Inc., USA) and the 105-T and
107-L (Campbell Inc., USA) probes measured soil
temperature and soil moisture. Meteorological data
were recorded at 30-min intervals using the CR23X
(1) and the CR10X (3) (Campbell Inc., USA) data
loggers.
CO2 ux measurements using the eddy
covariance method
The CSAT3 sonic anemometer (Campbell Scientic,
Inc., USA) and the LI-7500 (LI-COR Inc., USA)
open-path CO2 analyzer mounted at a height of
38 m on an 80 cm × 80 cm walkup tower were
used to measure the CO2 exchange, latent heat
and energy in the period between 2003 and 2014.
With adherence to the procedures suggested by (Li
et al. 2008), air temperature, CO2 concentration
and water vapor pressure were recorded at a 10 Hz
frequency. CO2 concentration and vertical velocity
covariances were calculated at every 30-min
interval after which, data screening was done to
remove periods without sufciently developed
turbulence as indicated by friction velocities (u*)
below 0.2 ms−1. Planar t rotations and quality tests
were also done to remove errors in the data (Foken
and Wichura 1996). The EUROFLUX method was
applied in the calculation of net ecosystem exchange
(NEE) using the collected ux data (Aubinet et al.
1999; Lee et al. 2004; Mauder and Foken 2006), and
the carbon gains by the ecosystem were indicated
using negative NEE values. Using the marginal
distribution method, a gap-lling procedure was
performed on the ux data (Owen et al. 2007).
Gross primary production (GPP) and RE (ecosystem
respiration) were computed from NEE using a short-
term temperature-dependent method and the ux
data were recorded as g C m−2 (Owen et al. 2007;
Reichstein et al. 2005).
4 JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
Drought indices
This study considered four drought indices
to identify drought periods and make proper
comparisons and analyses. The indices considered
were SPI (standardized precipitation index), SPEI
(standardized precipitation evaporation index), PA
(precipitation anomaly percentage) and scPDSI (self-
calibrated Palmer drought severity index). The choice
of drought indices to use was based on data collected
and available for analysis.
Standardized precipitation index
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This index is useful in quantifying precipitation
decits as anomaly percentiles based on multiple
timescales observed. Commonly available
precipitation data are used in its calculation and it
is therefore an easy method to implement (McKee
et al. 1993). By tting a Gamma probability density
function into a standardized normal distribution, this
index can be successfully computed (Lloyd-Hughes
and Saunders 2002). This method has been found
suitable for quantifying agricultural, hydrological
and meteorological droughts by dening drought
severity by the probability of anomaly occurrence
(Lloyd-Hughes and Saunders 2002; McKee et al.
1993; Wang et al. 2020).
Å ã
c0 + c1 t + c2 t 2
SPI = S t −
1 + d 1 t + d 2 t 2 + d3 t 3 (1)
t = average temperature [°C]
S = −1, if H(x) ≤ 0.5 [H(x) is the cumulative
probability of distribution]
S = 1 and H(x) = 1 − H(x), if H(x) > 0.5; H(x) = q
+ (1 − q)G(x) [G(x) is the gamma distribution
undened for x = 0]
q = P(x = 0) > 0 [P(x = 0) is the probability of zero
precipitation, x is precipitation in mm] (McKee et
al. 1993)
Standardized precipitation evaporation index
This is a derived index from SPI. By standardizing
the difference between water supply from
precipitation and water demand from potential
evapotranspiration, a climatic water balance analysis
can be implemented on a log-logistic probability
distribution (Thornthwaite and Mather 1955; Vicente-
Serrano et al. 2012). The potential evapotranspiration
is estimated using the Thornthwaite method which
uses the monthly air temperature and the annual heat
index for its estimation (Thornthwaite and Mather
1955; Vicente-Serrano et al. 2012).
 Di = Pi − PETi (2)
Di are values obtained from the SPI procedure
Pi: precipitation (mm)
PETi: potential evapotranspiration for the month
i (mm) based on the Thornthwaite method
(Thornthwaite and Mather 1955)
Precipitation anomaly percentage
This index shows droughts that are a result of
precipitation anomalies. It is derived by dividing the
difference between the observed precipitation and a
30-year mean precipitation ‘normal’ (Yao et al. 2015).
This index is simple to calculate and dry events can be
seen on monthly and annual scales (Yao et al. 2015).
P − p̂
Pa = × 100%
p̂ (3)
P is the period of precipitation
p̂ is the 30-year mean precipitation ‘normal’
Self-calibrated Palmer drought severity index
This index is based on the sum of the current soil
moisture anomaly and a fraction of the previous index
value (Palmer 1965). The soil moisture variability is
calculated based on water supply and demand as a
result of precipitation, runoff, soil water holding
capacity, temperature and evaporation (Benjamin
2002; Zargar et al. 2011). This method results in
the classication of droughts into 11 categories of
increasing severity. These results are revised further
to provide the scPDSI which accounts for extreme
wet and dry events by accounting for the frequencies
of rare events (Benjamin 2002; Wells et al. 2004).
1
scPDSIi = 0.755scPDSIi−1 + Z1
1.63 (4)
Z = Kd
Z is the Palmer moisture anomaly index
K is the climate coefcient dependent on
geographical location and time of the year
d = P − p̂
P is the sum of monthly precipitation
p̂ is an ‘appropriate’ amount of precipitation in the
prevailing climatic condition
Statistical analysis
From the data collected at the research station in
Dinghushan Biosphere Reserve, we calculated the
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
daily, monthly, annual and interannual precipitation,
NEE, temperature, soil moisture, GPP and Re. Carbon
uxes were calculated as shown in Equation (5)
(Owen et al. 2007; Reichstein et al. 2005):
FGPP = FNEE + FRe (5)
A drought index software from the world meteorological
organization was applied in determining periods of
drought and periods of increased precipitation using
30 years of precipitation data collected from the data
collecting station at Dinghushan Biosphere Reserve.
After identifying periods of droughts using each of
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the four drought indices, we proceeded to merge all
drought events into a single list and thereafter, rened
our list to identify the main drought events during
our study period. Statistical correlation, descriptive
statistics and preparation of graphs were done using
SigmaPlot® 14.5 Build 14.5.0.101.
RESULTS
Trends in climatic conditions in Dinghushan
Biosphere Reserve
Precipitation
Fig. 1 shows the total monthly precipitation recorded
during the 12-year study period. Seasonal variations
were visible i.e. the wet season occurred between
April and September and the dry season occurred
between October and March. The year with the
lowest total annual precipitation was 2012, with
a total of 936.50 mm whereas the year with the
highest annual precipitation was 2008 with a total
of 1988.90 mm. The average annual precipitation for
the 12-year study period was 1404.57 ± 43.2 mm,
which was lower than the 30-year average of
1927.00 ± 62.5 mm (1990–2020).
Temperature
Fig. 2a shows monthly averages of air temperature
measured in the Dinghushan Biosphere Reserve. The
annual temperature trends over the 12-year study
period indicated an upward trajectory (Fig. 2b). There
was no clear relationship between the mean annual
temperature and total annual rainfall. Seasonal
temperature variations were consistent throughout
the study period, with higher temperatures being
recorded in summer (April to September) compared
with winter (October to March) as shown in Fig. 2a.
The average annual temperature during the 12-year
study period was 22.65 ± 0.1 °C which is higher than
the 30-year average (1990–2020) of 20.1 ± 0.3 °C.
5
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Figure 1: Monthly total precipitation (mm) recorded in the Dinghushan Biosphere Reserve from 2003 to 2014.

Figure 2: (a) Average monthly temperature trends (°C) from 2003 to 2014; (b) average annual temperature trends (°C)
from 2003 to 2014.

The warmest (23.1 °C) and coldest (22.1 °C) years
were 2006 and 2008, respectively.
Precipitation indices
To identify periods of drought, we used four different
precipitation indices that use long-term precipitation
data to identify periods of drought and periods of
increased precipitation by applying a probability
algorithm and then expressing the results as an easily
interpretable index. A drought was identied once
the precipitation index was below −1.0 as shown in
Table 1.

6 JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088

Standardized precipitation index
After performing the SPI procedure, results were
obtained that showed the predicted months of
drought and the months of high precipitation
alongside the SPI value representing the intensity
of the predicted precipitation event (Table 1). Out of
the 144 months studied, the SPI analysis predicted
14 months of moderate drought, 9 months of severe
drought and 5 months of extreme drought. The
predicted drought period accounted for about 20%
of the total 12-year study period in Dinghushan
was shown to have experienced higher than normal
precipitation having an SPI value higher than 1.5.
The proportions of the droughts, normal and wet
periods are shown in Fig. 3a. As shown in Fig. 3a, the
months of drought and months of high precipitation
did not have a clearly dened seasonal distribution
pattern. Fig. 3a also shows that the latter half of the
study period experienced more drought as compared
with the rst half. The years 2012 and 2013 showed
the greatest number of drought events, with greater
severity (Fig. 3a). The SPI peak showed the highest

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Biosphere Reserve. Only 16% of the study period possible level of drought that occurred during the
period.
Table 1: The drought index and the corresponding
precipitation condition Precipitation anomaly percentage index
Drought index value Precipitation condition The PA predicted 12 months of moderate drought, 10
months of severe drought and 8 months of extreme
2.0+ Extremely wet
drought in the 144 months study period (Fig. 3b;
1.5 to 1.99 Very wet Table 1). Nineteen percent of the study period was
1.0 to 1.49 Moderately wet shown to have experienced higher than normal
precipitation. The proportions of the droughts,
−0.99 to.99 Near normal
normal and wet periods are shown in Fig. 3b. The
−1.0 to −1.49 Moderately dry predicted drought period accounted for about 17%
−1.5 to −1.99 Severely dry of the total 12-year study. The analysis showed
that the months of drought and months of high
−2 and less Extremely dry precipitation did not have a dened seasonality. Fig.

Figure 3: Months of drought and months of high precipitation and their corresponding (a) SPI value and (b) PA from
2003 to 2014.

JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088 7


Figure 4: Months of drought and months of high precipitation and their corresponding (a) scPDSI and (b) SPEI from 2003
to 2014.
3b also shows that the latter half of the study period
experienced more drought as compared with the
rst half. The years 2012 and 2013 had the greatest
number of drought events and the greatest severity
(Fig. 3b).
Standardized precipitation evaporation index
The SPEI predicted 15 months of moderate drought,
12 months of severe drought and 5 months of
extreme drought in the 144 months study period
(Fig. 4b; Table 1). Twenty percent of the study
period was shown to have experienced higher than
average precipitation. The predicted drought period
accounted for about 13% of the total 12-year study
period. The indices of the droughts, normal and wet
periods are shown in Fig. 4b. Fig. 4b also shows
that the latter half of the study period experienced
more drought as compared with the rst half with
the years 2012 and 2013 having the greatest number
of drought events and the greatest severity. The
analysis showed that the months of drought and
months of high precipitation did not have a seasonal
distribution.
Self-calibrated Palmer drought severity index
The scPDSI predicted 10 months of moderate
drought, 11 months of severe drought and 3 months
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of extreme drought in the 144 months study period
(Fig. 4a; Table 1). The predicted drought period
accounted for about 10% of the total 12-year study
period. Fifteen percent of the study period was
shown to have experienced higher than average
precipitation. The indices of the droughts, normal
and wet periods are shown in Fig. 4a. The scPDSI
analysis showed that the months of drought and
months of high precipitation did not have a clearly
dened seasonal distribution. Fig. 4a also shows that
the rst half of the study period experienced less
drought as compared with the latter half with the
years 2012 and 2013 having the greatest number of
drought events and the greatest severity.
Comparison between the different drought
indices
SPEI predicted 15 moderate droughts which was
the highest number; SPEI also predicted 12 severe
drought months which was the highest number; PA
had 8 extreme drought months which was the highest
among the drought indices used in this analysis.
Overall, scPDSI predicted the lowest number of
drought events with a total of 24 months of drought
throughout the study period while SPEI predicted
the highest number of drought events at 32 months
of drought throughout the 144 months drought
period (Fig. 5). All the drought indices used showed
that the latter half of the study period had a higher
frequency of droughts as compared with the rst half.
The average number of predicted drought months
among all the drought indices was 28.5 months. The
pattern of drought distribution was similar among
the drought indices. Table 2 shows the total number
of periods predicted to have experienced droughts
with the duration and the intensity of the drought
accurately shown.
Relationship between drought indices and soil
moisture
Between 2003 and 2008, SPI and soil moisture
trends did not show a strong relationship but
between 2009 and 2014, SPI and soil moisture
trends were in tandem at r2 = 0.49, P < 0.001
(Fig. 6a); Soil moisture and PA had a clear trend
of correlation throughout the study period at r2 =
0.54, P < 0.001 (Fig. 6b) meaning PA could predict
reductions in soil moisture content in response to
drought.
SPEI had the strongest correlation to soil moisture,
with the peaks and troughs matching throughout the
study period at r2 = 0.46, P < 0.001 (Fig. 7a). From
2003 to 2010, the scPDSI did not accurately match
the soil moisture trend at an r2 = 0.57, P < 0.001;
however, between 2012 and 2014, the scPDSI and
soil moisture trend closely matched (Fig. 7b).
Relationship between drought indices
predictions, soil moisture and measured carbon
uxes
After averaging the data from the four drought
indices used in our analysis, the main periods
of drought were identied. The average drought
indices predictions of drought and increased
Figure 5: Comparison of the different drought indices used in the study, SPI, PA, SPEI and scPDSI between 2003 and 2014.
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
precipitation were compared against measured
carbon uxes NEE, RE and GPP to reveal the effects
of drought on carbon gain. First, soil moisture
showed a positive correlation with NEE (r2 =
0.9023, P < 0.0001) as shown in Fig. 8. The indices
showed 16 months of increased precipitation that
had a drought index value of >1, and 16 months
of drought that had a drought index value of <−1,
and these were chosen to make comparisons. It
was found that 9 out of the 16 months compared
showed a higher value of NEE (more negative)
Downloaded from https://academic.oup.com/jpe/article/16/1/rtac088/6693849 by guest on 28 February 2023
during drought than during the period of high
precipitation as shown in Fig. 9a. This showed
that in 60% of the study time, drought increased
NEE by up to 50% in the Dinghushan Biosphere
Reserve. In Fig. 9b on the other hand, RE was
higher during the period of high precipitation in
9 out of the 16 months compared. This showed
that 60% of the time, increased precipitation led
to an increase in RE by up to 40%. GPP is shown
in Fig. 9c and gave a clear picture of how drought
affected primary production. Ten out of the 16
months in the comparison had a higher GPP
during the drought period than during the period
of high precipitation. This meant that 63% of the
time, drought caused an increase in GPP.
DISCUSSION
Effect of drought on ecosystem carbon uxes
By comparing four drought indices we were able
to determine periods of drought and periods
of increased precipitation and compared these
against the measured ecosystem carbon uxes.
Our current ndings support our hypothesis that
droughts increase carbon gain in the Dinghushan
Biosphere Reserve. Interestingly, we recorded an
9
Table 2: Start date, end date, duration, drought index peak and intensity of droughts in Dinghushan Biosphere Reserve

Start date End date Duration (months) Drought index Intensity

August 2012 November 2012 3 −2.85 Extreme drought

June 2012 July 2012 1 −2.26 Extreme drought

May 2013 June 2013 1 −2.17 Extreme drought

March 2005 May 2005 2 −1.99 Severe drought

November 2010 December 2010 1 −1.97 Severe drought

September 2004 January 2005 4 −1.94 Severe drought

Downloaded from https://academic.oup.com/jpe/article/16/1/rtac088/6693849 by guest on 28 February 2023

February 2013 March 2013 1 −1.69 Severe drought

May 2003 June 2003 1 −1.63 Severe drought

April 2011 June 2011 2 −1.54 Severe drought

September 2011 October 2011 1 −1.51 Severe drought

November 2003 January 2004 2 −1.48 Moderate drought

June 2004 July 2004 1 −1.45 Moderate drought

February 2009 March 2009 1 −1.44 Moderate drought

October 2013 November 2013 1 −1.42 Moderate drought

December 2011 March 2012 3 −1.4 Moderate drought

January 2014 February 2014 1 −1.38 Moderate drought

July 2008 August 2008 1 −1.33 Moderate drought

March 2010 April 2010 1 −1.32 Moderate drought

July 2003 August 2003 1 −1.21 Moderate drought

November 2007 December 2007 1 −1.1 Moderate drought

increase in total ecosystem carbon gain in periods
that were drought stricken as compared with
periods of increased precipitation. Indeed, the
ecosystem was a carbon sink for 60% of the period
under drought (Fig. 9a–c). This is counterintuitive
and different from what has been recorded in
other subtropical forest ecosystems in Asia (Xie
et al. 2016; Zhou et al. 2015). Li et al. (2012) and
Njoroge et al. (2021) recorded a strong carbon
sink phenomenon in the Dinghushan Biosphere
Reserve during the dry winter time as compared
with the wet summer time and attributed this
to the increased cloud cover during the rainy
summer season that blocked most light from
reaching the forest canopy thus reducing carbon
uptake by the forest. Their ndings show that
during conditions of low precipitation, the forest
is exposed to more light and therefore can have
more carbon gain. Doughty and Goulden (2008)
reported that dryer conditions trigger leaf ushing
that causes older leaves higher in the canopy to
drop off thus exposing younger leaves lower in the
canopy which have a higher carbon uptake rate.
Observations into the seasonal changes of forest
reectance in the near-infrared (NIR) showed that
forests in regions under the inuence of the Asian
monsoons appear comparably darker during the
dry season illustrating an increased uptake of light
for photosynthesis; thus, increased carbon uptake;
compared with other forests that absorb less light
and appear brighter in NIR (Tanaka et al. 2003).
Our analysis focused mainly on precipitation as
the main limiting factor on carbon gain, however, in
addition to precipitation, other micrometeorological
factors like photosynthetically active radiation affect
forest ecosystems’ carbon gain by directly affecting
the photosynthetic activity of plants (Guttières et al.
2021; Li et al. 2021) and thus carbon ux and carbon
gain are affected by these factors even though our
study did not track their effect.

10 JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088


Figure 6: The relationship between (a) SPI and soil moisture (m3 m−3) and (b) PA and soil moisture (m3 m−3) between
2003 and 2014.
Trends in precipitation and temperature
Both precipitation and temperature showed a strong
seasonal variation, with distinct cool and dry seasons
between October and March and warm and wet
seasons between April and September (Figs 1 and
2a, b). Tropical ecosystems such as the Dinghushan
Biosphere Reserve are particularly susceptible to
changes in climatic conditions and therefore require
more ecologists’ attention because of climate change
(Smith et al. 2020; Stan et al. 2020). Trends in local
climatic conditions are predicted to be inuenced by
global climate change currently taking place making
them harder to predict for purposes of conservation
policy formulation (Diodato et al. 2020; Swarna et
al. 2021). The annual precipitation average for the
12-year study period was 1404.57 mm which is
lower than the 30-year average (1990–2020) of
1927.00 mm, which could mean that the Dinghushan
Biosphere Reserve is increasingly becoming more
drought prone. The average annual temperature
during the 12-year study period was 22.65 °C which
is higher than the 30-year average (1990–2020) of
20.1 °C thus indicating an increasing trend in air
temperature. Subtropical forests and other forests
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
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in China have been identied to be particularly
susceptible to the effects of climate change (Xu et
al. 2018; Zhang et al. 2017b). Researchers have
shown that studying precipitation trends to identify
instances of extreme drought is important in
making predictions that will inform the protection,
preparation and rehabilitation of affected forest
ecosystems (Nepstad et al. 2008).
Effects of drought on soil moisture
We compared soil moisture content in the period
predicted to be in drought and the wet period
using four drought indices. From our ndings, soil
moisture trends can be accurately correlated to
drought indices (Figs 6a, b and 7a, b). We found
that SPEI was the best drought index to be applied
in predicting soil moisture in the Dinghushan
Biosphere Reserve (Fig. 7b). Researchers have
recorded that apart from precipitation, multiple
factors can affect soil moisture such as the wetness
index; the contributing area; the local slope; the soil
depth; the composition of sand, silt and clay; the
scaling parameter and the hydraulic conductivity
(Cheng et al. 2020; Zhu et al. 2020).
11

Figure 7: The relationship between (a) SPEI and soil moisture (m3 m−3) and (b) scPDSI and soil moisture (m3 m−3)
between 2003 and 2014.
Figure 8: A statistical correlation between average soil
moisture (m3 m−3) and average NEE (g C m−2 mon−1) from
2003 to 2014.
We calculated a signicant positive correlation
between soil moisture and ecosystem carbon ux as
shown in Fig. 8. This means that in the Dinghushan
Biosphere Reserve, soil moisture affects carbon gain.
The soil moisture variation over time is shown in
Fig. 10. Soil has been shown to play a big role in
12
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the carbon balances of ecosystems around the world
(Humphrey et al. 2021). Soil moisture content
affects plant photosynthesis thereby affecting
carbon sequestration (Tong et al. 2020) meaning that
soil moisture is an important metric to study and
quantify when determining an ecosystem’s carbon
cycle.
CONCLUSIONS
The current ndings support the hypothesis that
droughts increase carbon gain in the Dinghushan
Biosphere Reserve. By comparing four drought
indices we were able to accurately identify periods
of drought in a much better way than just using
one drought index, enabling us to compare the
periods of drought against the measured ecosystem
carbon uxes to test our hypothesis. Our analysis
uncovered a counterintuitive phenomenon that
60% of the time during drought, the Dinghushan
Biosphere Reserve experienced considerable and
measurable carbon gain, which is contrary to what
has been recorded in other ecosystems around the
world. We acknowledge that by comparing only
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088

Figure 9: (a) NEE (g C m−2 mon−1) during months of drought and months of high precipitation; (b) RE (g C m−2 mon−1)
during months of drought and months of high precipitation; (c) GPP (g C m−2 mon−1) during months of drought and
months of high precipitation.
Figure 10: Monthly average soil moisture (m3 m−3) variation in the Dinghushan Biosphere Reserve between 2003 and
2014.
water availability and carbon uxes, our ndings
may have overlooked perhaps other important
factors at play in this phenomenon. Therefore, we
invite future research work to lean into this area
using our ndings as a foundation. More research is
also needed to nd out the effects droughts will have
on tree mortality, growth, recruitment and other
forest services. The effects of decreased precipitation
on other organisms in the Dinghushan Biosphere
Reserve have also not been clearly documented
and therefore further research is needed to give
wholistic scientic predictions for the future. Long-
term temperature trends need to be studied and
reported for future comparisons. We propose that
our contribution to the knowledge gap be used in
the formulation of conservation policy to protect the
Dinghushan Biosphere Reserve by safeguarding it
against the harsh effects of drought and improving
its resilience to the expected climate change-induced
changes.
JOURNAL OF PLANT ECOLOGY | 2022, 16:rtac088
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Funding
This work was supported by the National Natural
Science Foundation of China (31961143023,
31670453), the Strategic Priority Research Program
of the Chinese Academy of Sciences (XDA23080302),
the National Key Research and Development Program
of China (2021YFF0703905); the Chinese Ecosystem
Research Network (CERN); the Dinghushan Forest
Ecosystem Positioning Research Station of the
National Science and Technology Infrastructure
Platform and the Operation Service Project of the
National Scientic Observation and Research Field
Station of the Dinghushan Forest Ecosystem of
Guangdong, the Ministry of Science and Technology
of the People’s Republic of China.
Acknowledgements
We would like to thank the ANSO Scholarship for
Young Talents for its generous support to students
pursuing scientic research.
13
Conict of interest statement. The authors declare that
they have no conict of interest.
Authors’ Contributions
Brian Njoroge and Yuelin Li: data processing and
writing; Dennis Otieno and Fasih Ullah Haider:
writing; Simin Wei, Qianmei Zhang and Guowei
Chu: data collection; Shizhong Liu: site maintenance;
Ze Meng: instrument maintenance; Deqiang Zhang
and Juxiu Liu: experimental design; John Tenhunen:
methods guide.
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