Article

Effect of Altitude and Topography on Vegetation Phenological

Changes in the Niubeiliang Nature Reserve of Qinling
Mountains, China
Chenhui Deng 1,2, *, Xinping Ma 1 , Meilin Xie 1 and Hongying Bai 3

1 College of Geography and Environment, Xianyang Normal University, Xianyang 712000, China;
[email protected] (X.M.); [email protected] (M.X.)
2 College of Geography and Tourism, Shaanxi Normal University, Xi’an 710119, China
3 College of Urban and Environmental Sciences, Northwest University, Xi’an 710127, China;
[email protected]
* Correspondence: [email protected]

Abstract: Due to the fragility of the habitats in mountain nature reserves, the vegetation is extremely
sensitive to climate change, and its phenological changes are more specific. Therefore, it is of great
significance to study the effects of topography and climate on the vegetation phenology in mountain
nature reserves. Based on the vegetation phenology data retrieved from MODIS EVI2 during 2000
to 2017, combined with temperature data, spatial trend analysis and correlation analysis methods
were used to study the effects of topographic and climatic factors on vegetation phenology in the
Niubeiliang Nature Reserve of the Qinling Mountains. The results showed that the GSS (growing
season start) was advanced with a rate of 4.24 days/10a, and the rates in the northern and southern
slopes were almost the same; the GSE (growing season end) was delayed with a rate of 3.29 days/10a,
and the rate in the northern slope was faster; and the GSL (growing season length) was prolonged.
There were seasonal differences and north–south differences in the effects of topography on the
Citation: Deng, C.; Ma, X.; Xie, M.;
phenophase. The phenophase changed regularly with the increase in altitude. The higher the altitude,
Bai, H. Effect of Altitude and
the more significant the effect. The steeper the slope, the later the GSS, the earlier the GSE, and the
Topography on Vegetation
more significant its effect on the GSE. The aspect had little effect on GSS but a more significant effect on
Phenological Changes in the
Niubeiliang Nature Reserve of
GSE, which was the latest on the sunny slope and the earliest on the zero slope. Temperature affected
Qinling Mountains, China. Forests both the GSS advance and the GSE delay, and both had a time-lag effect of approximately 2–3 months.
2022, 13, 1229. https://doi.org/ Its effect was more significant in the GSE, in the southern slopes, and in the high-altitude areas.
10.3390/f13081229
Keywords: vegetation remote sensing phenology; topographic differentiation; climate warming;
Academic Editor: Romà Ogaya
north–south differences; Niubeiliang Nature Reserve
Received: 2 June 2022
Accepted: 26 July 2022
Published: 3 August 2022

Publisher’s Note: MDPI stays neutral

1. Introduction
with regard to jurisdictional claims in For the past hundred years, the global climate has been undergoing a significant
published maps and institutional affil- change characterized by warming [1]. Climate change exhibits significant regional differ-
iations. ences, and ecologically sensitive areas, especially the geographical transition zones and
mountains at mid- and high-latitudes, are considered to be amplifiers of global warming
signals [2–6]. Vegetation phenology is considered to be the most objective and sensitive
biological indicator reflecting environmental conditions and climate change [7], and is
Copyright: © 2022 by the authors.
regarded as the “language” of nature [8] and the “fingerprint” for diagnosing global
Licensee MDPI, Basel, Switzerland.
change [9,10]. The vegetation phenology in many regions of the world has been signifi-
This article is an open access article
cantly affected by climate change [11], and regions such as Europe [12,13], Asia [14,15],
distributed under the terms and
Australia [16], and North America [17,18] all have the phenomenon of a GSS (growing
conditions of the Creative Commons
season start) in advance and a GSL (growing season length) in prolongation. However, due
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
to the limitation of natural environment conditions such as terrain and traffic, phenological
4.0/).
observation data in mountainous areas are extremely scarce.

Forests 2022, 13, 1229. https://doi.org/10.3390/f13081229 https://www.mdpi.com/journal/forests

Forests 2022, 13, 1229 2 of 21

The development of remote-sensing technology provides a new method for vegetation

phenology monitoring, and has become an important means of phenological monitoring
at present. Compared with traditional plant phenology observation technology, remote-
sensing phenology has the advantages of a multi-temporal phase, wide spatial coverage,
strong temporal continuity, etc. It can realize the expansion of the research scale from
individual vegetation to a community or ecosystem, and from point to surface, which is
convenient for carrying out research on phenological changes at the regional and global
scales [19]. Scholars have used the vegetation index monitored by remote sensing in the
tropical rain forests [20] and the transitional zone of desert-steppe in the northern hemi-
sphere [21], as well as in China, the Qinghai-Tibet Plateau [22–26], the Loess Plateau [27–29],
the Inner Mongolia [30,31], the Qaidam Basin [32], the southern subtropical monsoon re-
gion [33], the southwest karst rift basin [34], and other ecologically sensitive areas, where
extensive research on vegetation phenology has been carried out. At the same time, remote-
sensing technology also has unique advantages in monitoring mountain phenology. At
present, it has been applied to mountain vegetation phenology research [35,36]. Vegetation
phenology in the Qinling Mountains is also a hotspot area of concern to scholars [7,37–44].
Some scholars have pointed out that 15% of the earth’s terrestrial carbon sinks (about
312 Gt) are stored in reserves around the world. Nature reserves are also natural buffers for
climate change impacts and other disasters, which have an important value in responding
to climate change adaptation and mitigation, and are known as effective solutions to the
climate change crisis [45]. Niubeiliang National Nature Reserve is typical and representative
of the Qinling Mountains; it is considered as the epitome of the Qinling Mountains [46].
Its ecological status is extremely important and it is the core area of the Qinling ecological
space, but the ecological environment is extremely fragile. In addition, the geomorphic
type of the Qinling Mountains is the most special in the Niubeiliang Reserve. Its terrain of
“gentle in the northern slope and steep in the southern slope” forms a clear contrast with
the “gentle in the southern slope and steep in the northern slope” in the central and western
sections of the Qinling Mountains. Therefore, it is of great significance to study the effects
of topographic and climatic factors on vegetation phenology in the Niubeiliang Nature
Reserve. However, the current research on vegetation phenology in mountain nature
reserves is relatively weak, and research on the vegetation phenology in the Niubeiliang
reserve has not been reported in detail. Therefore, MODIS EVI2 time-series images from
2000 to 2017 were reconstructed by the double logistic curve fitting algorithm to extract the
phenological parameters, and combined with the spatial temperature data interpolated by
ANUSPLIN; we studied the temporal and spatial change laws of the vegetation phenology
in the Niubeiliang Nature Reserve over the past 18 years, and explored the effects of
topographic differentiation and climate change on the vegetation phenology. The purpose
of this study was to reveal the laws of vegetation phenology change and its influence in
mountain nature reserves in the context of climate change, to provide decision support for
the adaptive management and protection of the vegetation ecosystems in mountain nature
reserves against climate change, and also to provide a scientific reference for improving the
carbon sink function of forests in mountain nature reserves.

2. Materials and Methods

2.1. Study Area
The Niubeiliang National Nature Reserve is an important part of the “Qinling nature
reserve group” and is known as “the epitome of the Qinling Mountains”. It was identi-
fied as 1 of the 40 top-priority biodiversity conservation areas in the “China biological
diversity protection action plan”, and is also listed as an A-level protected area with global
significance, mainly to protect the national I-level protected animal takin and its habitat.
Its geographical range is 33◦ 440 –33◦ 470 N and 108◦ 450 –109◦ 030 E, which spans the
north–south slope and the main ridge of the Qinling Mountains, with a long narrow
distribution in the east–west orientation, about 28 km long from east to west and 15 km
wide from north to south, with a total area of 164.18 km2 . The Niubeiliang is the main peak
Forests 2022, 13, 1229 3 of 21

with an altitude of 2802 m, which is the highest peak in the eastern Qinling Mountains.
The reserve is located in the relatively intact natural forest region in the eastern Qinling
Mountains, and the forest coverage rate is more than 96% [47]; it is known as the “green
pearl”. The reserve belongs to the mountain forest system of a coniferous and broad-leaved
mixed type in the warm temperate zone, showing obvious vertical structure characteristics.
From the bottom to the top of the reserve, there are the mixed coniferous and broad-leaved
forest zone with the deciduous broad-leaved forest and the pine-oak forest, the mixed
coniferous and broad-leaved forest zone with the mid-alpine pine-birch forest, and the
subalpine coniferous forest zone. The vertical vegetation zones of the reserve are obviously
different between the northern and the southern slope, there is the Quercus acuteserrata
forest on the bottom of the northern slope, while there is the Quercus variabilis forest on the
bottom of the southern slope. In addition, there is a Picea asperata forest in the northern
slope but not in the southern slope. The geographical location of the reserve and the spatial
distribution of the vertical vegetation zones are shown in Figure 1.

Figure 1. Geographical location of the study area and spatial distribution of its vertical vegetation zone.

The reserve is located at the meeting place of the northern and southern climates in
China. It belongs to the warm temperate semi-humid monsoon climate, which is cool and
humid in the summer then cold and dry in the winter. The annual average temperature is
2–10 ◦ C, the annual precipitation is 850–950 mm, and the frost-free period is approximately
130 days. It has the characteristics of a mountain climate with obvious vertical differences.
From the top to the bottom of the reserve, there are five different climatic zones including
the alpine frigid zone, cold temperate zone, temperate zone, warm temperate zone, and
north subtropical zone.

2.2. Data Source and Preprocessing

2.2.1. Data Sources
The phenological data derived from the established vegetation remote-sensing phenol-
ogy dataset of the Qinling Mountains [37] and the vegetation phenology data of the research
area from 2000 to 2017 were extracted according to the boundary range of the Niubeiliang
Nature Reserve. The data were derived from the MOD09Q1 surface reflectance dataset
Forests 2022, 13, 1229 4 of 21

in the MODIS data products provided by the NASA (https://ladsweb.nascom.nasa.gov)

(accessed on 1 November 2018), which retrieved the MODIS EVI2 vegetation index from
2000 to 2017 as a data source for monitoring remote-sensing phenological changes, with a
temporal resolution of 8 days and a spatial resolution of 250 m × 250 m.
The meteorological data were derived from the established temperature raster dataset
of the Qinling Mountains [48]. The data were obtained by the spatial interpolation of the
monthly temperature data of 32 meteorological stations in the Qinling area from 2000 to
2017. The data came from the Shaanxi Provincial Meteorological Information Center.
The DEM data came from the Shaanxi Provincial Bureau of Surveying and Mapping
Geographic Information, with a resolution of 25 m × 25 m.

2.2.2. Data Processing

(1) Pre-Processing of Remote-Sensing Data
Firstly, the maximum value composite (MVC) method was used to process the data,
and the enhanced vegetation index 2 (EVI2) in the region was calculated by the band
calculation tool of the ENVI software. The formula is detailed in [37]. Secondly, the
harmonic analysis of time series (HANTS) method was used to further denoise and smooth
the filtering of the EVI2 time-series data to remove residual clouds and long-time hazes
or other negative effects in the sub-pixels. Then, the three parameters of the GSS, GSE
(growing season end), and GSL were used as the identification indexes of the vegetation
phenology in the study area, and the day of year (DOY), which is the actual number of
days since 1 January of the same year, was used to represent the time when the phenophase
appeared. The parameters GSS and GSE for the identification of plant phenophase were
both determined according to their multi-year time evolution laws, and were extracted by
a combination of the threshold method and the maximum ratio method in the software
TIMESAT. Afterwards, a 1% confidence interval was set to eliminate outliers of the GSS
and GSE. Finally, the annual GSL was calculated (the difference between GSS minus GSE).
The detailed mechanism of data processing can be found in [37].
(2) Processing of Topographic Data
In order to perform overlay analysis with the vegetation phenology data, the DEM data
were resampled to 250 m × 250 m, and the slope and aspect of the study area were extracted
from the DEM using ArcGIS software. According to the gradient classification standard
in the “Main Technical Provisions of Forest Resources Planning and Design Survey”, the
slope was divided into the flat slope (below < 5◦ ), gentle slope (5◦ –15◦ ), sloping slope
(15◦ –25◦ ), steep slope (25◦ –35◦ ), and sharp slope (>35◦ ); the aspect was divided into the
zero slope (0◦ ), shady slope (0◦ –45◦ and 315◦ –360◦ ), semi-shade slope (45◦ –135◦ ), sunny
slope (135◦ –225◦ ), and semi-sunny slope (225◦ –315◦ ). The grades of the slope and aspect in
the study area are shown in Figure 2.
(3) Processing of Temperature Data
The spatial interpolation of temperature data adopted the latest international profes-
sional meteorological data interpolation software ANUSPLIN. Some scholars have found
through comparison that the ANUSPLIN is more suitable for the spatial interpolation of
climatic elements in complex mountain environments [49]. At the same time, the DEM
was used as a covariate in the interpolation process, so the raster data of the monthly aver-
age temperature with topographic features in the Qinling Mountains in the past 18 years
(spatial resolution 250 m × 250 m, projection WGS–1984–UTM–Zone–48) were obtained.
Forests 2022, 13, 1229 5 of 21

Figure 2. Spatial distribution of the slope and aspect classification in the study area. (a) Slope;
(b) aspect.

2.3. Research Methods

2.3.1. Spatial Unary Linear Regression Trend Analysis and Its Significance Test
This method used the least squares method to fit the slope of the vegetation phenology
parameters, which can simulate the change trends of the vegetation phenology parameters
in each grid, and comprehensively reflect the evolution process of the temporal and spatial
pattern of the vegetation phenology in the region. The calculation formula is:
n n n
n ∑ ixi − ∑ i ∑ xi
slope = i=1 i =1 i =1
 2
n n
n ∑ i2 − ∑ i
i =1 i =1

In the formula: the slope represents the inter-annual change rate, n is the annual
sequence, and xi represents the vegetation phenology parameters of the ith year. When the
slope > 0, it indicates that x is advancing or shortening, and when the slope < 0, it indicates
that x is delaying or prolonging. The t-test is used to reflect the significance of the change
trend, and the results are divided into extremely significant changes (p ≤ 0.01), significant
changes (0.01 < p ≤ 0.05), weakly significant changes (0.05 < p ≤ 0.1), and insignificant
changes (p > 0.1).

2.3.2. Spatial Correlation Analysis and Its Significance Test

In order to investigate the effect of temperature on vegetation phenology, the Pearson
correlation coefficient at the pixel scale was used to calculate the correlation between the
GSS and the monthly average temperature of the same period (April, April and May,
May) and previous period (January, January and February, February, February and March,
March, March and April), as well as the correlation between the GSE and the monthly
average temperature of the same period (September, September and October, October)
and previous period (June, June and July, July, July and August, August, August and
September), which analyzed the spatial correlation between the vegetation phenophase
and the temperature. At the same time, the significance of the correlation coefficient
was tested, and the results were divided into highly significant correlations (p ≤ 0.01),
significant correlations (0.01 < p ≤ 0.05), weakly significant correlations (0.05 < p ≤ 0.1) and
insignificant correlations (p > 0.1).
Forests 2022, 13, 1229 6 of 21

3. Results
3.1. Temporal and Spatial Variation Characteristics of Vegetation Phenology
3.1.1. Spatial Distribution of Vegetation Phenology
Figure 3 shows the spatial distribution of the multi-year mean values of the vegetation
phenology parameters in the Niubeiliang reserve from 2000 to 2017. It can be seen from
Figure 3 that the vegetation phenology changes in the reserve exhibited obvious topo-
graphic differentiation in the past 18 years, especially in the GSS. The GSS in the reserve
mainly occurred at 115–140 DOY (92.68%), that is, from late April to mid-May, with an
average of 126.54 DOY. The GSSs in the northern and southern slopes were not much
different, with an average of 126.77 DOY in the northern slope and 126.46 DOY in the
southern slope. Spatially, the GSS was earlier in the low-altitude regions in the northern
and southern slopes, while it was relatively later in the high-altitude regions on both sides
of the ridge. The GSE in the reserve mainly occurred at 260–300 DOY (93.65%), that is,
from late September to late October, with an average of 282.18 DOY. The average GSE
was 275.44 DOY in the northern slope and 284.48 DOY in the southern slope, and the
GSE in the southern slope was approximately 9.04 days later than that in the northern
slope. Spatially, the GSE ended earlier in the northern slope, especially in the high-altitude
areas in the east of the ridge, while it was relatively later in the low-altitude areas in the
southern slope. The GSL in the reserve was mainly concentrated in 130–190 days (96.64%),
that is, approximately 4–6 months, with an average of 155.64 days. The average GSL was
148.66 days in the northern slope and 158.03 days in the southern slope, and the GSL in the
southern slope was approximately 9.36 days longer than that in the northern slope.

Figure 3. Spatial distribution of the multi-year average of vegetation phenological parameters in

Niubeiliang Nature Reserve from 2000 to 2017. (a) GSS; (b) GSE; (c) GSL.
Forests 2022, 13, 1229 7 of 21

3.1.2. Inter-Annual Variability of Vegetation Phenology

Figure 4 shows the interannual change trends of the vegetation phenological parame-
ters and their significances in the Niubeiliang Nature Reserve from 2000 to 2017. It can be
seen from Figure 4 that there were obvious spatial differences in the interannual changes
of the vegetation phenology in the reserve in the past 18 years. The GSS was dominated
by an advancing trend, and 99.53% of the whole area showed an advanced trend. The
average rate in the whole area was −4.24 days/10a, which was mainly 2–4 days/10a in
advance (39.77%), followed by 4–6 days/10a (36.82%), while 6–8 days/10a was relatively
less common (9.93%). The change rates in the northern and southern slopes were relatively
consistent, with an average of −4.41 days/10a in the northern slope and −4.40 days/10a in
the southern slope. The t-test results showed that only 11.53% of the whole area displayed a
significant advancing trend (p ≤ 0.05, the same below) in the GSS, and these areas were mainly
located in the high-altitude areas of the reserve. The areas where the advance trend reached a
significant level were 8.02% and 12.74% in the northern and southern slopes, respectively.

Figure 4. Spatial distribution of interannual change trends of the vegetation phenological parameters
in Niubeiliang Reserve from 2000 to 2017 and their significances. (a) Slope of the GSS; (b) significance
of the GSS; (c) slope of the GSE; (d) significance of the GSE; (e) slope of the GSL; (f) significance of the GSL.
Forests 2022, 13, 1229 8 of 21

The GSE was mainly delayed, and 75.62% of the whole area showed a delayed trend.
The average rate in the whole area was 3.29 days/10a, which was mainly delayed by
4–6 days/10a (16.46%), followed by 2–4 days/10a (16.31%), 6–8 days/10a (15.24%), and
then >8 days/10a (15.05%). This showed that the distribution of the change rate at all levels
was relatively balanced, and the differences in regional proportion were small. The change
rate in the northern slope was faster than that in the southern slope, with an average of
4.12 days/10a in the northern slope and 3.01 days/10a in the southern slope. The t-test
results showed that only 1.63% of the whole area displayed a significant delay trend in the
GSE, and these areas were mainly located in the low-altitude areas of the northern slope.
The areas where the delay trend reached a significant level were 3.58% and 0.97% in the
northern and southern slopes, respectively.
The GSL was mainly prolonged, and 91.64% of the whole area showed a prolonged
trend. The average rate in the whole area was 7.54 days/10a, which was mainly prolonged
by 4–8 days/10a (26.70%), followed by 10–14 days/10a (22.97%), while 0–4 days/10a was
relatively less common (16.93%). The change rates were not much different between the
northern and southern slopes, with an average of 7.91 days/10a in the northern slope and
7.42 days/10a in the southern slope. The results of the t-test showed that only 4.78% of
the whole area displayed a significant prolonged trend in the GSL, which were 8.15% and
3.62% in the northern and southern slopes, respectively.

3.2. Effect of Topography on Vegetation Phenology

3.2.1. Effects of Altitude
Figure 5 shows the changes of the vegetation phenology parameters at different
altitudes in the entire Niubeiliang Nature Reserve and its northern and southern slopes
from 2000 to 2017. It can be seen from Figure 5 that the vegetation phenological changes in
the Niubeiliang Reserve had a significant altitude sensitivity. With the increase in altitude,
the GSS in the whole area showed a significant delay trend, with a rate of 1.84 days/100 m,
and the delay rate in the southern slope was faster than that of the northern slope. The
difference in the GSS between the northern and southern slopes gradually increased with
the increase in altitude, and the difference was the largest in the summit area, approximately
8.51 days. The GSE presented a significant advance trend, with a rate of 1.66 days/100 m,
and the change rates in the southern slope and the northern slope were not much different.
At the same altitude, the GSE was later in the southern slope than the northern slope, and
the difference between the southern slope and the northern slope was the largest at 2700 m,
approximately 10.55 days. It can be seen that the north–south difference in the GSE with the
change in altitude was more obvious than that of the GSS. The GSL exhibited a significant
shortening trend, with a rate of 3.50 days/100 m, and the change rates in the northern slope
and the southern slope were also not much different. The difference in the GSL between
the northern and southern slopes gradually narrowed with the increase in altitude, and the
difference was the smallest in the area of ≥2300 m.
Based on the distribution of the vertical vegetation zones in the Niubeiliang Re-
serve [47], the multi-year mean changes of the phenological parameters in the vegetation
zones in the northern and southern slopes from 2000 to 2017 were analyzed, as shown in
Table 1. The GSS in the northern slope was the earliest in the Quercus acuteserrata forest zone
and the latest in the Abies fargesii forest zone, with a difference of approximately 15.37 days,
while in the southern slope, it was the earliest in the Quercus variabilis forest zone and the
latest in the Abies fargesii forest zone, with a difference of approximately 26.25 days. In
the same type of vegetation zone, the GSS occurred earlier in the northern slope than in
the southern slope, with a difference of approximately 8.55 days for the Birch forest zone,
approximately 7.47 days for the Abies fargesii forest zone, and approximately 4.54 days for
the Quercus acuteserrata forest zone.
Forests 2022, 13, 1229 9 of 21

Figure 5. Changes of vegetation phenological parameters at the different altitudes in Niubeiliang

Reserve from 2000 to 2017. (a) GSS of the whole area with the altitude; (b) GSS of the northern and
southern slopes with the altitude; (c) GSE of the whole area with the altitude; (d) GSE of the northern
and southern slopes with the altitude; (e) GSL of the whole area with the altitude; (f) GSL of the
northern and southern slopes with the altitude.

The GSE in the northern slope was the latest in the Quercus acuteserrata forest zone and
the earliest in the Abies fargesii forest zone, with a difference of approximately 12.13 days,
while in the southern slope, it was the latest in the Quercus variabilis forest zone and the
earliest in the Abies fargesii forest zone, with a difference of approximately 20.53 days. In
the same type of vegetation zone, the GSE occurred later in the southern slope than in the
northern slope, with a difference of approximately 4.76 days for the Quercus acuteserrata

3
Forests 2022, 13, 1229 10 of 21

forest zone, approximately 4.16 days for the Abies fargesii forest zone, and approximately
2.22 days for the Birch forest zone.

Table 1. Multi-year mean of vegetation phenological parameters on the different vegetation vertical
zones in Niubeiliang Reserve from 2000 to 2017.

Northern Slope Southern Slope

Altitude GSS GSE GSL Altitude GSS GSE GSL
Vegetation Zones Vegetation Zones
Range/m /DOY /DOY /Days Range/m /DOY /DOY /Days
Quercus
1200~1800 117.44 284.50 167.06 Quercus variabilis 750~1300 113.63 296.60 182.97
acuteserrata
Quercus
Birch 1800~2100 124.47 275.14 150.67 1300~2050 121.98 289.26 167.29
acuteserrata
Picea asperata 2100~2300 129.61 272.65 143.04 Birch 2050~2600 133.02 277.36 144.34
Abies fargesii >2300 132.81 272.37 139.51 Abies fargesii >2600 140.28 276.53 136.25

The GSL in the northern slope was the longest in the Quercus acuteserrata forest
zone and the shortest in the Abies fargesii forest zone, with a difference of approximately
27.55 days, while in the southern slope, it was the longest in the Quercus variabilis forest
zone and the shortest in the Abies fargesii forest zone, with a difference of approximately
46.72 days. In the same type of vegetation zone, except that the GSL of the Quercus acuteser-
rata zone was basically the same in the northern and southern slopes, the other vegetation
zones were longer in the northern slope than in the southern slope. The difference was ap-
proximately 6.33 days in the Birch forest zone and 3.26 days in the Abies fargesii forest zone.
Figure 6 shows the change trends of the phenology in the vertical vegetation zones in
the Niubeiliang Reserve from 2000 to 2017. It can be seen from Figure 6 that the advance
rate of the GSS in the vertical vegetation zone was relatively the largest in the Abies fargesii
forest zone in the northern slope, and it was relatively small and not much different in other
zones. In the southern slope, all vegetation zones except the Quercus variabilis forest zone
tended to increase with the increase in altitude. For the same type of the vertical vegetation
zone, the advance rate of the GSS was faster in the southern slope than in the northern
slope, and the difference between the northern and the southern slopes gradually increased
with the increase in altitude. Among them, the change rate of the Abies fargesii forest zone
was the largest difference between the northern and the southern slopes (3.20 days/10a). In
the whole area, the advance rate of the GSS was the largest in the Abies fargesii forest zone
in the southern slope, followed by Quercus variabilis forest zone in the southern slope.

Figure 6. Change trends of vegetation phenological parameters on the different vegetation vertical
zones in Niubeiliang Reserve from 2000 to 2017. (a) GSS slope of vegetation vertical zones; (b) GSE
slope of vegetation vertical zones; (c) GSL slope of vegetation vertical zones.

The delay rate of the GSE in the vertical vegetation zone showed a decreasing trend
with the increase in altitude in the northern slope, and the rates in the Picea asperata forest
zone and the Abies fargesii forest zone in the high-altitude area were the smallest and
Forests 2022, 13, 1229 11 of 21

showed little difference. In the southern slope, all vegetation zones except the Quercus
variabilis forest zone showed an increasing trend with the increase in altitude. For the same
type of the vertical vegetation zone, the delay rates of the GSE in the Quercus acuteserrata
forest zone and the Birch forest zone were faster in the northern slope than in the southern
slope, while that in the Abies fargesii forest zone was faster in the southern slope than in the
northern slope. Among them, the change rate of the Quercus acuteserrata forest zone was the
largest difference between the northern and the southern slopes (4.29 days/10a), followed
by the Quercus variabilis forest (2.52 days/10a). In the whole area, the delay rate of the GSE
was the largest in the Quercus acuteserrata forest zone in the northern slope, followed by the
Quercus variabilis forest zone in the southern slope.
The prolongation rate of the GSL in the vertical vegetation zone also presented a
decreasing trend with the increase in altitude in the northern slope, and the rate of the Abies
fargesii forest zone was second only to that of the Quercus acuteserrata forest zone. In the
southern slope, all vegetation zones except the Quercus variabilis forest zone showed an
increasing trend with the increase in altitude. For the same type of the vertical vegetation
zone, the prolongation rate of the GSL in the Quercus acuteserrata forest zone was faster in
the northern slope than in the southern slope, while that in the Birch forest zone and in
the Abies fargesii forest zone were faster in the southern slope than in the northern slope.
Among them, the change rate of the Abies fargesii forest zone was the largest difference
between the northern and the southern slopes (5.73 days/10a), followed by the Quercus
variabilis forest zone (2.52 days/10a). In the whole area, the prolongation rate of the GSL
was the largest in the Abies fargesii forest zone in the southern slope, followed by the Quercus
variabilis forest zone in the southern slope.

3.2.2. Effects of Slope

Figure 7 shows the changes of the vegetation phenological parameters on the different
slopes in the entire Niubeiliang Reserve and its northern and southern slopes from 2000 to
2017. It can be seen from Figure 7a,b that the GSS displayed a significantly delayed trend
with the increase in the slope, which was the earliest on the flat slope and the latest on
the sharp slope, with a difference of approximately 3.19 days. In the northern slope, the
GSS change fluctuated greatly with the increase in the slope, and the delay trend was not
significant. The various slopes were in the order of the flat slope < steep slope < sloping
slope < sharp slope < gentle slope; that is, the GSS was the earliest on the flat slope and the
latest on the gentle slope, with a difference of approximately 7.09 days. In the southern
slope, the GSS gradually delayed with the increase in the slope, showing a significant
delaying trend. The various slopes were in the order of the flat slope < gentle slope <
sloping slope < steep slope < sharp slope; that is, the GSS was the earliest on the flat
slope and the latest on the sharp slope, with a difference of approximately 2.53 days. For
the same type of slope, the GSSs on the flat slope and the steep slope were earlier in the
northern slope than the southern slope, while the GSSs on the other slopes were earlier in
the southern slope than the northern slope, but the difference between the northern and
the southern was not large. The difference was the largest on the flat slope, but it was only
approximately 2.83 days.
It can be seen from Figure 7c,d that the GSE displayed an extremely significant advance
trend with the increase in the slope, which was the latest on the flat slope and the earliest on
the sharp slope, with a difference of approximately 7.42 days. In the northern and southern
slopes, the GSE showed a significant advance trend with the increase in the slope, and it
was more significant in the northern slope than the southern slope. The various slopes
were in the order of the flat slope > gentle slope > sloping slope > steep slope > sharp
slope; that is, the GSE was the latest on the flat slope and the earliest on the sharp slope.
The difference between the two was approximately 16.07 days in the northern slope, and
approximately 7.90 days in the southern slope. For the same type of slope, the GSEs on
the various slopes were all later in the southern slope than in the northern slope, and the
Forests 2022, 13, 1229 12 of 21

difference between the northern and the southern slopes increased with the increase in the
slope. The difference between the sharp slopes was the largest, approximately 12.05 days.

Figure 7. Changes of vegetation phenological parameters on the different slopes in Niubeiliang

Reserve from 2000 to 2017. The horizontal coordinate was specifically the flat slope (below < 5◦ ),
gentle slope (5◦ –15◦ ), sloping slope (15◦ –25◦ ), steep slope (25◦ –35◦ ), and sharp slope (>35◦ ). (a) GSS
of the whole area with the slope; (b) GSS of the northern and southern slopes with the slope; (c) GSE
of the whole area with the slope; (d) GSE of the northern and southern slopes with the slope; (e) GSL
of the whole area with the slope; (f) GSL of the northern and southern slopes with the slope.

It can be seen from Figure 7e,f that the GSL displayed an extremely significant short-
ening trend with the increase in the slope, which was the longest on the flat slope and the
shortest on the sharp slope, with a difference of approximately 10.61 days. In the northern
and southern slopes, the GSL showed a significant shortening trend with the increase in
the slope, and it was more significant in the northern slope than the southern slope. The
various slopes were in the order of the flat slope > gentle slope > sloping slope > steep
Forests 2022, 13, 1229 13 of 21

slope > sharp slope; that is, the GSL was the longest on the flat slope and the shortest
on the sharp slope. The difference between the two was approximately 23.16 days in the
northern slope, and approximately 10.43 days in the southern slope. For the same type
of slope, the GSLs on the various slopes were all longer in the southern slope than in the
northern slope, and the difference between the northern and the southern slopes increased
with the increase in the slope. The difference between the sharp slopes was the largest,
approximately 13.78 days.

3.2.3. Effects of Aspect

Figure 8 shows the changes of the vegetation phenological parameters on different
aspects in the entire Niubeiliang Reserve and its northern and southern slopes from 2000
to 2017. It can be seen from Figure 8a,b that the GSS was the earliest on the shady slope
and the latest on the zero slope, with a difference of approximately 3.14 days. The various
aspects in the northern slope were in the order of the zero slope < shady slope < semi-shady
slope < semi-sunny < sunny slope; that is, the GSS was the earliest on the zero slope and the
latest on the sunny slope, with a difference of approximately 5.06 days, while the various
aspects in the southern slope were in the order of the shady slope < zero slope < semi-sunny
slope < sunny slope < semi-shady slope; that is, the GSS was the earliest on the shady slope
and the latest on the semi-shady slope, with a difference of approximately 5.38 days. It
follows that the GSS in the northern slope was the earliest on the zero slope, while in the
southern slope it was the earliest on the shady slope, which was attributed to the fact that
the aspect not only caused the temperature difference between the different slopes, but also
affected the difference in the water evaporation, revealing that water was also an important
factor affecting the advancement of the beginning of the phenophase. For the same type of
aspect, the GSS in the southern slope was later than the northern slope on all other aspects
except the semi-shady slope, and the difference between the sunny slope was the largest
at approximately 3.81 days, which indicated that the effect of the aspect on the GSS was
relatively small, and there was little difference between the northern and southern slopes.
It can be seen from Figure 8c,d that the GSE was the latest on the sunny slope and
the earliest on the zero slope, with a difference of approximately 13.03 days. The various
aspects in the northern and southern slopes were in the order of the sunny slope > semi-
shady slope > zero slope > semi-sunny slope > shady slope; that is, the GSE was the latest
on the sunny slope and the earliest on the shady slope, with a difference of approximately
6.57 days in the northern slope and 9.03 days in the southern slope. It follows that the GSE
in both the northern and southern slopes was the latest on the sunny slopes, indicating that
the sunny slope was beneficial to the delay of the ending of the phenophase, especially the
sunny slope in the southern slope. For the same type of aspect, the GSEs on all aspects were
later in the northern slope than the southern slope, the difference between the northern and
southern slopes was relatively large at all levels except the shady slope (0–45◦ ) (3.73 days),
and the difference between the sunny slopes was relatively large, with a difference of
approximately 7.89 days. The results revealed that the aspect had a great influence on the
GSE, and there was a great difference between the northern and southern slopes.
It can be seen from Figure 8e,f that the GSL was the longest on the sunny slope and
the shortest on the zero slope, with a difference of approximately 14.56 days. The various
aspects in the northern slope were in the order of the zero slope > semi-shady slope >
sunny slope > shady slope (0–45◦ ) > semi-sunny slope > shady slope (135–225◦ ); that is,
the GSL was the longest on the zero slope and the shortest on the shady slope (135–225◦ ),
with a difference of approximately 3.47 days, while the various aspects in the southern
slope were in the order of the sunny slope > zero slope > semi-sunny slope > shady slope >
semi-shady slope; that is, the GSL was the longest on the sunny slope and the shortest
on the semi-shady slope, with a difference of approximately 6.19 days. For the same type
of aspect, the GSLs on all aspects were longer in the southern slope than the northern
slope, and the difference between the sunny slopes was relatively large, with a difference
of approximately 11.69 days.
Forests 2022, 13, 1229 14 of 21

Figure 8. Changes of vegetation phenological parameters on the different aspects in Niubeiliang

Reserve from 2000 to 2017. (a) GSS of the whole area with the aspect; (b) GSS of the northern and
southern slopes with the aspect; (c) GSE of the whole area with the aspect; (d) GSE of the northern
and southern slopes with the aspect; (e) GSL of the whole area with the aspect; (f) GSL of the northern
and southern slopes with the aspect.
Forests 2022, 13, 1229 15 of 21

3.3. Effect of Temperature on Vegetation Phenology

Figure 9 shows the correlation analysis results of the GSS, GSE, and the monthly
average temperature in the Niubeiliang Reserve. It can be seen from Figure 9 that the
correlation coefficients between the GSS and the temperature were mainly negative, that is,
as the temperature rose, the beginning of the phenophase was advanced. The areas with a
negative correlation between the GSS and the average temperature in February were the
most common (84.39%), and the areas with a negative correlation reaching a significant
level were the average temperature in May, but only represented 1.23% of the whole area
(p < 0.05). The correlation coefficients between the GSE and the temperature were mainly
positive, that is, as the temperature rose, the ending of the phenophase was delayed. The
areas with a positive correlation between the GSE and the average temperature in July
were the most represented (74.70%), and the areas that reached the significant level were
4.17% of the whole area (p < 0.05). The areas with a positive correlation between the GSE
and the average temperature from July to August were the second most common (70.65%),
and the areas that reached the significant level were 2.68% of the whole area (p < 0.05),
indicating that the temperature had an effect on both the advance of the beginning of the
phenophase and the delay of the ending of the phenophase, and the effect on the ending of
the phenophase was more significant than on the beginning of the phenophase.

Figure 9. Spatial correlations between the GSS/GSE and temperature in Niubeiliang Reserve from
2000 to 2017. (a) Correlation between the GSS and temperature in February; (b) correlation be-
tween the GSS and temperature in May; (c) correlation between the GSE and temperature in July;
(d) correlation between the GSE and temperature in July and August.

The effect of the temperature on the GSS and the GSE exhibited obvious time-lag
effects, in which the time-lag effect on the GSS was approximately 2–3 months, and the lag
time effect on the GSE was also approximately 2–3 months. Spatially, there were significant
north–south differences and altitude differences in the effects of temperature on the GSS
Forests 2022, 13, 1229 16 of 21

and the GSE, which presented that the effect in the southern slope was more significant
than that in the northern slope. The effects of the temperature on the GSS and the GSE in
high-altitude areas were more significant than that in low-altitude areas, indicating that the
effect of the temperature change on the vegetation phenology in high-altitude areas was
more significant.

4. Discussion
4.1. Influence of Altitude, Slope, and Aspect on Phenology
In mountainous terrain, there are complex spatial changes in vegetation phenology
due to the effects of topography on microclimate, soil moisture, and community composi-
tion [50]. Altitude, aspect, and slope are the three main topographic factors that indirectly
affect the vegetation patterns of mountains [51]. The research results of the influence of
the three topographic factors on the change in vegetation phenology in the Niubeiliang
Reserve showed that the vegetation phenology changed regularly with the increase in
altitude; the beginning of phenophase was significantly delayed, with an average rate of
1.84 days/100 m; the end of phenophase was significantly advanced, with an average rate
of 1.66 days/100 m; and the length of growing season was significantly shortened, with an
average rate of 3.50 days/100 m. The higher the altitude, the more significant its impact
on the phenological changes, which are closely related to the mountain climate, especially
the temperature change decreases with the increase in altitude. The effects of the slope
and the aspect on the end of phenophase were more significant than at the beginning of
phenophase. With the increase in the slope, the beginning of phenophase was significantly
delayed, it was earliest on flat slopes and latest on sharp slopes; the end of phenophase
was significantly advanced, it was the latest on the flat slope and the earliest on the sharp
slope; and the length of growing season was significantly shortened, it was the longest on
the flat slope and the shortest on the sharp slope. The steeper the slope, the earlier the end
of phenophase, which may be related to the amount of the solar radiation received. The
steeper the slope, the lower the amount of solar radiation received at the end of phenophase,
leading to the advance of the end of phenophase. The aspect had a more significant effect
on the end of phenophase, it was the latest on the sunny slope and the earliest on the zero
slope, which may be related to the accepted sunshine duration. The sunny slope had a long
sunshine duration, which was conducive to the delay of the phenological end. The influ-
ence of the topographic factors on the phenophy not only displayed seasonal differences,
but also north–south differences. The effect of altitude on the beginning of phenophase
was smaller in the northern slope than in the southern slope, while the effect on the end of
phenophase was greater in the northern slope than in the southern slope. The effects of
slope on the beginning and end of phenology were greater in the northern slope than the
southern slope, and the effect of aspect on the beginning of phenology had little difference
between the northern and the southern slopes, while its effect on the end of phenology
was greater in the southern slope than in the northern slope, which was attributed to the
difference in the impact of the terrain on climate factors in the reserve. Topography is an
important influencing factor for the existence of spatial differences in phenology, and the
altitude is the most important factor among the three factors, because it can be served as a
proxy for temperature and precipitation [52]. The results of a phenological study on the
humid temperate forests in the southern Appalachian Mountains of the USA showed that
there was a strong linear relationship between altitude and the beginning of phenophase,
and altitude factor had the strongest explanatory power for all phenological parameters,
followed by temperature lapse rate [50]. The spatial distributions of forest community
types in the region were closely related to elevation, aspect, and moisture gradient. In
the forest-steppe of Mongolia, as a result of topographically induced differences of solar
radiation and evapotranspiration, the landscape difference of “grass on the southern slope
and trees on the northern slope” was formed [53]. Such a landscape pattern also exists
on both sides of the ridge of the Qinling Mountains. Phenological studies in Mongolia
have shown that there are obvious differences in the response of vegetation phenology to
Forests 2022, 13, 1229 17 of 21

altitude. The beginning of phenophase was hardly affected by the altitude changes, while
the end of phenophase and the length of the growing season changed greatly with the
increase in altitude [54], which were obviously different from the research conclusion of
the Niubeiliang Reserve. With regard to the effect of slope on vegetation phenology in the
Qinghai-Tibet Plateau, the beginning of phenophase in the meadow area was significantly
delayed but the end of phenophase significantly advanced with the increase in slope on
both northern and southern slopes [55], which were also significantly different from the
research conclusions of the Niubeiliang Reserve. In addition, the influence pattern of slope
on vegetation phenology was the opposite in the steppe zone and in the meadow zone of
the Qinghai-Tibet Plateau [55]. With regards to the effect of aspect on vegetation phenology,
the beginning of phenophase was later but the end of phenophase was earlier on shaded
slopes than on sunlit slopes in the meadow area, and the beginning of phenophase did not
significantly depend on aspect in the steppe area, while the end of phenophase indicated a
similar response to aspect in the steppe area to that in the meadow area [55]. In conclusion,
the influence mechanism of topography on vegetation phenology is complex and needs to
be further explored.

4.2. Influence of Temperature on Phenology

The vegetation phenology in the mid- and high-latitudes region is primarily controlled
by temperature and photoperiod, while in tropical and semi-arid regions it is mainly con-
trolled by seasonal rainfall [55]. The related research results of the topographic effects on
vegetation phenological changes in the Qinghai-Tibet Plateau showed that temperature
and moisture combinations were the main controlling factors [56]. The spatio-temporal
variations of the beginning of phenophase in the mountains of northwest Mongolia were
mainly influenced by both spring temperature and winter precipitation, with increasing
precipitation in winter tending to delay the beginning of phenophase, while increasing tem-
perature in spring tended to advance the beginning of phenophase [57]. The extension of
the growing season in the steppes, shrubs, and savannahs of Australia, Africa, and southern
South America is entirely dependent on changes in precipitation conditions [58]. Numerous
studies have also shown that precipitation strongly affects spring phenology [59,60]. How-
ever, due to the high altitude of the reserve, there was a lack of meteorological observation
data. The temperature data can be easily retrieved, while other meteorological data such
as precipitation and sunshine were more easily affected by factors such as terrain and
microhabitat, making them difficult to obtain. Therefore, the study only analyzed the
relationship between the temperature in the meteorological factors and the phenological
changes in the reserve. Temperature has been regarded as a driving factor for the change
in beginning of phenophase in most high-latitude and high-altitude ecosystems [61]. The
results in Niubeiliang Reserve displayed that the temperature had an effect on both the
advance of the beginning of phenology and delay of the end of phenology, but the areas
where the effect reached a significant level were relatively small, which indicated that the
temperature was only one of the main factors affecting the phenological changes in the
reserves. However, a single climate factor is not always sufficient to explain vegetation
phenology at a given location. Rather, multiple factors act on phenology simultaneously
or at different phases of vegetation development [62,63]. Especially in mountainous ar-
eas, the phenological changes of vegetation are more complex, which is the result of the
comprehensive effect of multiple factors. In addition, the beginning of phenophase has
different sensitivities to the temperature change compared to the end of phenophase, and
the response to the temperature change in the beginning of phenophase is greater than that
in the end of phenophase [64]. Our research found that the advance rate in the beginning of
phenology was faster than the delay rate in the end of phenology, but the effect of tempera-
ture in the end of phenology was more significant than that in the beginning of phenology,
and the effect was more significant in the high-altitude area than that in the low-altitude
area, and the relevant influence mechanisms still need to be further considered—more
factors, especially climate factors, need to be further studied.
Forests 2022, 13, 1229 18 of 21

4.3. Significance of the Results in the Context of Climate Change

In high-altitude areas, the vulnerability of vegetation ecosystems and hydrological
systems leads to their phenology being more sensitive and their response to climate change
more intense [65]. The Qinling Mountains are the boundary of physical geography and
climate between the north and south of China, and the Niubeiliang Nature Reserve belongs
to the mid-mountain or sub-alpine mountain in the Qinling Mountains, with a great height
difference, all-over canyons, and a special geomorphic type. In the past 18 years, the
beginning of phenophase in the reserve has advanced, the end of phenophase has been
delayed, and the growing season has been prolonged. This research conclusion is consistent
with the change trends of phenophase in the Qinling Mountains [37], but the change rates
of phenophase were significantly faster than those in the Qinling Mountains, indicating that
the climate changes in the high-altitude areas of the mountains were more severe and had a
greater impact on the vegetation phenology. In the Qinling Mountains, the average annual
temperature has increased by about 0.2 ◦ C per decade in the past 50 years, and the rate of
change in the northern slope was faster than that in the southern slope [48]. The temperature
in the Qinling Mountains has increased significantly since 1985. The spatial distributions of
the temperature change rate in spring and autumn in Niubeiliang Reserve from 1985 to
2017 are shown in Figure 10. In the Mongolian Plateau, the average annual temperature
has increased by about 0.36 ◦ C per decade in the past 50 years, and has risen rapidly since
1985, reaching 0.51 ◦ C per decade [66]. In the Qinghai-Tibet Plateau, the average annual
temperature has increased by about 0.4 ◦ C per decade in the past 50 years [67], which is
more than twice the rate of global temperature rise [68]. The temperature increases have
displayed spatiotemporal heterogeneity, being greater in the winter and autumn than in
spring and summer, at nighttime than in daytime, and in the western parts than in the
eastern parts [69,70]. In short, high-altitude areas are sensitive areas for climate change,
and the temperature in these areas increases significantly and at an extremely fast rate,
with significant differences in different regions due to latitude and topography. The related
impact mechanism is still a hot topic of research by scholars. In the context of climate
change, warming has promoted longer plant growing seasons, which may contribute
to an increase in the vegetation net primary productivity and cause negative feedback
on the current global warming caused by elevated atmospheric CO2 concentrations [71].
Vegetation phenology changes affect the carbon budget of terrestrial ecosystems, and the
carbon budget of forest ecosystems determines the intensity of the increase in atmospheric
CO2 concentration, so it also affects the process of global warming [72].

Figure 10. Spatial distribution of interannual change trends of temperature in Niubeiliang Reserve
from 1985 to 2017. (a) Slope of temperature in spring. (b) Slope of temperature in autumn.

5. Conclusions
The GSS of the reserve mainly occurred from late April to mid-May, showing an early
trend, and the change rates in the northern and southern slopes were basically the same.
Forests 2022, 13, 1229 19 of 21

The GSE mainly occurred from late September to late October, showing a delaying trend,
and the rate in the northern slope was slightly faster than that in the southern slope. The
GSL was approximately 4 to 6 months, showing a prolonged trend, and the change rates in
the northern and southern slopes were not much different.
With the increase in altitude, the phenophase showed regular changes. The higher the
altitude, the more significant its effect on the phenological changes. The effect of altitude
on the GSS was smaller in the northern slope than that in the southern slope, while its
effect on the GSE was larger in the northern slope than that in the southern slope. With
the increase in the slope, the GSS was significantly delayed; the GSE was significantly
advanced; and the GSL was significantly shortened. The influence of slope on the GSE
was more significant than that of the GSS, and its influences on the GSS and the GSE were
greater in the northern slope than in the southern slope. The aspect had little effect on
the GSS, while it had a more significant effect on the GSE, its effect on the GSS exhibited
less difference between the northern and southern slopes, while the effect on the GSE was
greater in the southern slope than in the northern slope.
The GSS was mainly negatively correlated with the temperature, while the GSE was
mainly positively correlated with the temperature. The effects of temperature on the GSS
and the GSE had a lag of approximately 2 to 3 months; its effect on the GSE was more
significant than that on the GSS, its effect in the southern slope was more significant than
that in the northern slope, and its effect in the high-altitude area was more significant than
in the lower-altitude area.

Author Contributions: Methodology and software C.D. and M.X.; formal analysis, C.D. and X.M.;
writing—original draft preparation, C.D.; writing—review and editing, H.B., X.M. and C.D. All
authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Special Scientific Research Program from the Education
Department of China’s Shaanxi Provincial Government (Grant number 19JK0930), as well as the
China Postdoctoral Science Foundation (Grant number 2019M663922XB).
Conflicts of Interest: The authors declare no conflict of interest.

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