Download Nitrogen deposition but not climate warming promotes Deyeuxia

Science of the Total Environment 544 (2016) 85–93
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
Nitrogen deposition but not climate warming promotes Deyeuxia
angustifolia encroachment in alpine tundra of the Changbai Mountains,
Northeast China
Shengwei Zong a, Yinghua Jin a, Jiawei Xu a,⁎, Zhengfang Wu a, Hongshi He a,b, Haibo Du a, Lei Wang a
a
b
School of Geographical Sciences, Northeast Normal University, 130024 Changchun, China
School of Natural Resources, University of Missouri, Columbia, MO, USA
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Treatments consisting of increased temperature and addition of nitrogen were
applied.
• Elevated temperature had a negative effect on encroaching species, D.
angustifolia.
• The native alpine shrub, R. chrysanthum,
showed negligible responses to treatments.
• Nutrient perturbation promoted D.
angustifolia encroachment to alpine
tundra.
a r t i c l e
i n f o
Article history:
Received 17 August 2015
Received in revised form 26 November 2015
Accepted 26 November 2015
Available online xxxx
Editor: J. P. Bennett
Keywords:
Climate warming
Nitrogen deposition
Upward expansion
Alpine tundra
Encroaching plant species
a b s t r a c t
Vegetation in the alpine tundra area of the Changbai Mountains, one of two alpine tundra areas in China, has undergone great changes in recent decades. The aggressive herb species Deyeuxia angustifolia (Komarov) Y. L.
Chang, a narrow-leaf small reed, was currently encroaching upon the alpine landscape and threatening tundra
biota. The alpine tundra of the Changbai Mountains has been experiencing a warmer climate and receiving a
high load of atmospheric nitrogen deposition. In this study, we aimed to assess the respective roles of climate
warming and atmospheric nitrogen deposition in promoting the upward encroachment of D. angustifolia. We
conducted experiments for three years to examine the response of D. angustifolia and a native alpine shrub, Rhododendron chrysanthum, to the conditions in which temperature and nitrogen were increased. Treatments
consisting of temperature increase, nitrogen addition, temperature increase combined with nitrogen addition,
and controls were conducted on the D. angustifolia communities with three encroachment levels (low, medium,
and high levels). Results showed that 1) D. angustifolia grew in response to added nutrients but did not grow well
when temperature increased. R. chrysanthum showed negligible responses to the simulated environmental
changes. 2) Compared to R. chrysanthum, D. angustifolia could effectively occupy the above-ground space by
⁎ Corresponding author at: School of Geographical Sciences, Northeast Normal University, No. 5268, Renmin Street, Changchun 130024, China.
E-mail address: [email protected] (J. Xu).
http://dx.doi.org/10.1016/j.scitotenv.2015.11.144
0048-9697/© 2015 Elsevier B.V. All rights reserved.
86
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
increasing tillers and growing rapidly by efficiently using nitrogen. The difference in nitrogen uptake abilities between the two species contributed to expansion of D. angustifolia. 3) D. angustifolia encroachment could deeply
change the biodiversity of tundra vegetation and may eventually result in the replacement of native biota, especially with nitrogen addition. Our research indicated that nutrient perturbation may be more important than
temperature perturbation in promoting D. angustifolia encroachment upon the nutrient- and species-poor alpine
tundra ecosystem in the Changbai Mountains.
© 2015 Elsevier B.V. All rights reserved.
1. Introduction
Alpine ecosystems are characterized by strong winds, short growing
seasons, high solar radiation, and low temperatures (Körner, 2003). Due
to the harsh environment, these systems are commonly considered to
be at low risk of plant encroachments that originate from low elevations
(Humphries et al., 1991). However, upward expansion of plant species
to higher elevations has occurred in many mountainous areas in the
last decade (Beckage et al., 2008; Gaur et al., 2003; Kelly and Goulden,
2008; Klanderud and Birks, 2003; McDougall et al., 2005; Parolo and
Rossi, 2008; Pauli et al., 2007; Walther et al., 2005). The upward trend
is found to be accelerating and the expansion is greater for herbaceous
species (Pauli et al., 2007; Walther et al., 2005), which are fastgrowing, often with broad altitudinal and ecological niches. They present a great threat to slow-growing, competition-intolerant alpine
plant species (Körner, 1995; Sætersdal and Birks, 1997). Herbaceous
plant encroachment into alpine ecosystems can potentially lead to extirpation of local biota because of their special functional traits (Pauli
et al., 2007). Thus far, the upward expansion of plant species from
low elevations has been attributed to three main causes: climate change
induced by elevated greenhouse gases (Thuiller et al., 2007), increased
nitrogen deposition (Heer and Körner, 2002), and increased human activities (McDougall et al., 2011). Among these causes, human activities
are readily tied to herbaceous plant encroachment through rapidly
growing tourism and other uses of mountain areas, but evidence of climate warming and nutrient deposition has also been reported.
Studies suggest that warmer climates make it possible for plant species to move from low to high elevations (Klanderud and Birks, 2003).
Rising temperatures have caused an amelioration of environmental
conditions (longer vegetative season length, increased energy supply
and reduction of some other ecological constraints), opening alpine terrain for “invaders” from lower elevations (Parolo and Rossi, 2008;
Huang et al., 2011; Thuiller et al., 2007). For upward encroaching species, positive responses to climate warming have included a higher germination rate, a high survival rate, expanding their habitats, and so on
(Walther, 2004). However, until now, few studies have been conducted
to assess the effect of climate warming on the upward expansion of
plant species and the interaction between encroaching plants and native plants in alpine regions (Harte and Shaw, 1995). The main finding
has been that climate warming drives changes in vegetation structure,
based on analysis of climate data and a comparison of historical and current vegetation (Parolo and Rossi, 2008). Most experimental studies
used simulated warming experiments to focus on the response of alpine
plant species to warmer conditions (Marion et al., 1997). They generally
found that warmer conditions promote the replacement of typical alpine shrubs by other plants, especially herbaceous plants. For example,
researchers in an alpine area of southern Norway who simulated
warming using an open-top chamber found that Dryas octopetala, the
typical and dominant alpine shrub in that area, could be replaced by
herbaceous plants (Klanderud and Totland, 2005). Thus, we wanted to
determine whether climate warming is indeed the factor that initiates
plant expansion from low to high elevations.
Besides climate warming, another explanation for plants expanding
to high elevations is an increase in available nutrients, especially nitrogen resources. It has been proven that global terrestrial ecosystems
have experienced increased atmospheric nitrogen deposition over the
past decades (Phoenix et al., 2006). Alpine regions commonly received
particularly high nitrogen deposition because they have higher rainfall
than surrounding areas at lower elevations (Fowler et al., 1988). Because alpine vegetation has developed under poor nutrient conditions,
its sensitivity to increased nitrogen may result in changes to species
composition (Curtis et al., 2005; Pearce et al., 2003). If increased nitrogen deposition enhances plant species' upward range shifts, then
nitrogen-demanding species would probably shift their range more
than other species (Körner, 2003). Undoubtedly, fast-growing herbaceous plants could take advantage of the increased nitrogen deposition.
Simulated nitrogen deposition experiments have demonstrated that
with sufficient nitrogen supply, perennial herbaceous plants would
gradually take the place of evergreen shrubs in alpine areas (Aerts and
de Caluwe, 1994). Thus, an increase in nitrogen resources may create
the opportunity for herbaceous species to expand through competition
with native alpine plant species.
However, until now, it has been difficult to distinguish between the
effect of climate warming and the effect of nitrogen deposition on the
upward expansion of plant species. We still do not know which one is
more important in driving plants to higher elevations. If the increase
in species richness on mountain summits does not require climate
warming (Kammer et al., 2007), then changes in competitive interactions under conditions of enhanced resource availability could explain
the successful upward expansion of plant species. It has been demonstrated that alleviation of stress in alpine ecosystems is frequently associated with a corresponding reduction in diversity. This is because
stress-tolerant species are excluded due to competition from other species, such as herbaceous plants, which grow most rapidly under favorable conditions (Nilsson et al., 2002). We sought to learn whether the
increase in nitrogen supply, in addition to or rather than elevated temperature, was a determining influence in alpine vegetation changes.
This information would help us to better understand the mechanism
that was aiding the expansion of an herbaceous plant that was
encroaching upon an alpine ecosystem.
Alpine tundra of the Changbai Mountains is one of the two alpine
tundra areas in China. Comparing current conditions with historical
data, we found that Deyeuxia angustifolia (Komarov) Y. L. Chang in
birch forests on an adjacent mountain area had crossed the tree line
and expanded into the alpine tundra. The widely distributed
D. angustifolia patches have severe impacts on the alpine tundra ecosystem and lead to extirpation of typical tundra plants such as Rhododendron chrysanthum (Zong et al., 2013b). D. angustifolia, a narrow-leaf
small reed, is characterized as a hydro-mescophyte perennial herb,
with life traits that include fast growth, clonal and sexual reproduction,
a short juvenile period, high seed production and anemochory
(Williamson and Fitter, 1996). These traits ensure they can overcome
stressful abiotic conditions and survive in the harsh alpine tundra environment (Quiroz et al., 2009). D. angustifolia is native to the Changbai
Mountains but is not recorded in alpine tundra areas until the 1990s.
In the mountain birch forest at lower elevations surrounding the alpine
tundra, D. angustifolia is commonly distributed in moist habitats. The
earliest record of the plants of the alpine tundra indicated that
D. angustifolia belonged to the mountain birch forest zone, not the alpine tundra zone (Qian, 1979). Plant surveys in the 1980s showed
that D. angustifolia was not found in any alpine tundra plant communities (Huang and Li, 1984). However, in the 1990s, the first recording of
D. angustifolia was reported in moist habitats in alpine tundra, where
the cover of D. angustifolia was about 10% (Qian, 1992). Our field survey
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
work in 2010 showed that D. angustifolia was widespread in alpine tundra, which altered the landscape. Records showed that D. angustifolia
was not a tundra plant species. However, we cannot fully prove that it
is not a native species. Thus, we refer to it as an encroaching species.
At present, the driving mechanisms of D. angustifolia expansion are
not well studied. Never-the-less, we have found unassailable evidence
that the alpine tundra environment in the Changbai Mountains has
changed in two ways. First, the mean temperature of the growing season rose by 0.239 °C/10 a during the period between 1959 and 2010
(Zong et al., 2013a). Second, atmospheric nitrogen deposition reached
23 kg N ha−1 yr−1 (Hu et al., 2009), a rate in excess of many critical
loads set (e.g. 20 kg N ha−1 yr−1 in northern Europe) for sensitive ecosystems across globe (Phoenix et al., 2006). It seems that both climate
warming and atmospheric nitrogen deposition could contribute to the
D. angustifolia expansion because synergistic effects of climate warming
and atmospheric nitrogen deposition may co-occur (Klanderud and
Totland, 2005; Robinson et al., 1998). However, research is needed to illustrate the respective effects of climate warming and nitrogen deposition on the D. angustifolia encroachment.
In past decades, both annual temperatures and nitrogen deposition
increased in the alpine tundra, but notable changes in the precipitation
regime were not observed in this region (Zong et al., 2013a). Our previous studies showed that the response of D. angustifolia to increased temperature was negative (Jin et al., 2014). Therefore, we proposed the
hypothesis that nitrogen deposition rather than climate warming promotes D. angustifolia expansion within the alpine tundra. To test this hypothesis, we conducted a multi-year experiment in which we added
warmth and nutrients to D. angustifolia communities. The specific objectives of our study were to determine 1) the different responses to environmental change between D. angustifolia and the native alpine plant
species; 2) the respective effects of elevated temperature and atmospheric nitrogen deposition on D. angustifolia encroachment; and 3) diversity change as a result of environmental change and D. angustifolia
encroachment. Results from this study will help to understand the driving mechanism of herbaceous species' upward expansion and to predict
future changes in vegetation in the alpine tundra of the Changbai
Mountains.
2. Materials and methods
2.1. Study area
Changbai Mountain Nature Reserve, located in Jilin province, northeast China, has been managed for nature conservation purposes for 53
years. It has unique vertical spectra with five vegetation zones: 1) deciduous broad-leaved forest zone (below 500 m asl); 2) mixed deciduous
broad-leaved/conifer forest zone (500–1100 m asl); 3) coniferous forest
zone (1100–1700 m asl); 4) birch forest zone (1700–1950 m asl); and
5) tundra zone (above 1950 m asl). Our study area is located on the
western slope of alpine tundra (41°53′–42°04′N, 127°57′–128°11′E;
2100 m–2200 m), where the D. angustifolia expansion occurred. The climate of alpine tundra is characterized by low temperature, heavy precipitation and a short growing season. Annual mean temperatures
during the growing season (June to September) range from 3.37 to
8.82 °C (mean temperature is 5.87 °C). Annual average precipitation
ranges from 700 to 1400 mm (Zong et al., 2013a). Weather data are
from the Tianchi Meteorological Station, which is located 2623 m asl
and is 6.2 km away from our study area. The vegetation is characterized
as low stature or prostrate shrubs represented by D. octopetala var.
asiatica, evergreen shrubs represented by R. chrysanthum, deciduous
shrubs represented by Vaccinium uliginosum L., and tussocks dominated
by Carex pseudo-longerostrata, etc. The tundra plant community being
encroached upon is primarily the R. chrysanthum community (Zong
et al., 2013b). At present, D. angustifolia communities mainly include
two dominant plants, D. angustifolia and R. chrysanthum. Other associated plant species include Rhodiola cretinii, Sanguisorba tenuifolia var. alba,
87
Ligularia jamesii, and Saussurea triangulata, which are few in number
and with minimal coverage. In this study, we focused on the responses
to environmental changes by the two dominant species, D. angustifolia
and R. chrysanthum, because they determine the plant community
structure and function.
We treated D. angustifolia as an encroaching species in this study and
defined the D. angustifolia communities at three encroachment levels,
which are a high encroachment level (HEL, plant cover of
D. angustifolia ≥ 70%, plant cover of R. chrysanthum ≤ 30%), medium encroachment level (MEL, 40% ≤ plant cover of D. angustifolia ≤ 70%,
30% ≤ plant cover of R. chrysanthum ≤ 60%), and low encroachment
level (LEL, 10% ≤ plant cover of D. angustifolia ≤ 40%, plant cover of
R. chrysanthum ≥ 60%), respectively.
2.2. Design of the experiment
Treatments consisting of temperature increase (T), nitrogen addition (N), temperature increase and nitrogen addition (T + N), and controls (C, no treatment) were conducted on D. angustifolia communities
for the three encroachment levels defined above. Plots (1 m2) were
established in early June 2011 on the western slope of alpine tundra,
with four replicates for each treatment. Buffer zones with distances of
0.5 to 1 m were set around each plot, and no plot had the same treatment as an adjacent plot. In each plot, four 20 cm × 20 cm subplots
were set up for measuring growth and plant harvest.
To simulate atmospheric nitrogen deposition, external nitrogen was
applied in equal monthly doses during the growing season (June to September) with a solution of NH4NO3 (14.3 g/m2 per application) in deionized distilled water, starting in 2011. In each application,
ammonium nitrate solution was sprayed evenly over the experimental
plots at the beginning of each month. The total amount of nitrogen applied yearly was 57.2 g, which is comparable to other nitrogen addition
studies (Boyer and Zedler, 1999; Green and Galatowitsch, 2002).
In our study, we used an open-top chamber (OTC), a passive
warming apparatus, to simulate elevated atmospheric temperature as
a surrogate of climate warming. We used an OTC similar to the hexagonal version of The International Tundra Experiment OTC (Marion et al.,
1997). Each one is a steel frame 60 cm in height with a top diameter
of 150 cm, a basal diameter of 208 cm (base area of approximately
1.86 m2), and with 70° inwardly inclined walls. The large OTC we
made could have an edge effect, such as reducing precipitation inside
the chamber (Aerts et al., 2007). All OTCs were removed at the end of
the growing season and reinstalled in their original locations the following year shortly after snowmelt. Abiotic conditions inside and outside of
OTCs were continuously measured during the growing season. At intervals of 1 h, air temperature (20 cm above ground) and soil temperature
at 0 cm, 5 cm, and 10 cm depth were measured with a data logger
(HOBO, Onset Computer Corporation, Pocasset, Massachusetts, USA).
During the observation period, there was an average increase in mean
air temperature by 2.18 °C. Soil temperatures at depths of 0 cm, 5 cm,
and 10 cm increased by 1.53 °C, 1.00 °C, and 0.59 °C, respectively. In
the central area of each OTC, an area of 1 m2 was regarded as the experimental plot used for growth measurement and harvest.
2.3. Growth measurements
Within all three encroachment levels, the growth parameters measured for D. angustifolia and R. chrysanthum included the proportional
growth, aboveground biomass, and NUE (nitrogen use efficiency). Records were kept for each plot to determine whether the two species'
numbers expanded under experimental treatment. Tiller numbers
were recorded for D. angustifolia and shoot numbers were recorded
for R. chrysanthum. D. angustifolia, the fast growing plant, withered in
late September and produced new tillers in early June of the next year.
Because the original number of tillers was different in each plot, the
growth in tiller numbers was calculated as proportional growth. We
88
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
counted the number of tillers in late September 2011, 2012, and 2013.
We subtracted the original number as of late September 2010 (before
the start of our experiment), and then divided by the original number,
respectively. R. chrysanthum, the evergreen shrub, generated new
shoots every year. The method of calculating proportional growth in
shoot numbers was the same as that of D. angustifolia. To get accurate
results, we marked all the original shoots and new shoots with different
labels.
During the peak growing month (mid-August) in 2013, near the end
of the experiment, we clipped the above-ground parts of the two species to the ground surface on all the four subplots within each treatment
plot. Then, the above-ground biomass was separated into leaves and
stems, dried at 70 °C for 48 h, and then weighed to the nearest 0.01 g.
Below-ground biomass was estimated by empirical equation (Liu
et al., 2009). However, we did not analyze below-ground biomass in
this study.
The usual adaptation strategy of an herbaceous plant in a nitrogenpoor environment is to compete with native plant species for nitrogen
resources (Suding et al., 2004). Thus, we measured NUE of the two
plants, which is defined as the aboveground biomass produced per
unit of aboveground peak season nitrogen (Bowman, 1994; Klanderud
and Totland, 2005). N concentration was estimated for the peak season
standing crops of each plant species, which was determined by the
Kjeldahl method using an automatic intermittent analyzer
(SMARTCHEM 140 from French AMS Group).
To assess the effect of D. angustifolia encroachment and various
treatments on community diversity, we measured the biodiversity of
the plant communities. The Shannon–Wiener diversity index (H) and
the Species evenness Pielou index (E) were applied. The ShannonS
Wiener diversity index is calculated as H ¼ −∑ðPi h Pi Þ, where Pi is
l¼l
the proportional relative abundance of plant species belonging to the
ith species. The Species evenness index is calculated as E = H / lnS.
2.4. Data analyses
All the data acquired were tested to determine if they met the normality assumption of ANOVA. Transformations (log, arcsine-square
root) were necessary for some of the data. The effects of T, N, and
T + N treatments on plant growth for the two plant species were tested
with a multiple-factorial ANOVA. Comparisons among individual means
were made by Fisher's least significant difference (LSD) post hoc test
after ANOVA. All the statistical analyses were done using SPSS (version
16.0, SPSS Inc., Chicago, IL). For each of the statistical analyses, the levels
of significance were P b 0.05.
Fig. 1. Proportional growth per plot (mean ± 1 SE, n = 4) of the encroaching plant,
Deyeuxia angustifolia, and the native plant, R. chrysanthum, in 2011, 2012, and 2013
(n = 4) under treatments of temperature increase (T), nitrogen addition (N), temperature
increase combined with nitrogen addition (T + N), and control (C). LEL represents low encroachment level; MEL represents medium encroachment level; LEL represents high encroachment level. Different lower-case letters indicate a significant difference in results
using different treatments within the same community type at the P b 0.05 level, according to one-way ANOVA with Fisher's least significant difference (LSD) test.
nitrogen supply. In contrast to D. angustifolia, R. chrysanthum showed
negligible response to both T and N treatments.
3.2. Above-ground biomass ratio (ABR)
3. Results
3.1. Changes in proportional growth
The response of D. angustifolia to environmental change was more
significant than that of R. chrysanthum (Fig. 1). The D. angustifolia population reduced under T treatment, suggesting a negative effect from increasing temperature (Fig. 1, Table 1, F = 229.155, P b 0.000). In
contrast, N treatment clearly led to an increase in population, especially
at the low encroachment level (Table 1, F = 48.204, P b 0.000). Under
T + N treatment, the D. angustifolia population also increased, but the
extent of the increase was not as high as those under the N treatment,
which correlated to the negative effect of warming on plant growth.
In contrast, R. chrysanthum was not responsive to the simulated environmental changes (Fig. 1, Table 1). The reduction of population was
obvious at the high encroachment level, especially under N treatment,
but the reduction was not statistically significant. Therefore, it can be inferred that D. angustifolia might gradually occupy the aboveground
space by increasing population, especially under conditions of sufficient
Above-ground biomass is related to the number of tillers and shoots
and the growth of leaf and stem. We calculated the ABR (above-ground
biomass ratio) of D. angustifolia to R. chrysanthum, which made it easier
to understand the relationship between the encroaching plant and the
native plant under environmental changes and to compare the relative
response of each species under various treatments. The ABR increased
gradually with the transition from low encroachment to high encroachment levels (Fig. 2); D. angustifolia increased and R. chrysanthum decreased. At each encroachment level, T treatment reduced the ABR
(Table 1, F = 25.139, P b 0.000), which is probably related to the negative response of D. angustifolia to warmer conditions. Under N treatment, the ABR highly increased (Table 1, F = 53.077, P b 0.000),
which is consistent with the higher sensitivity of D. angustifolia to nitrogen addition as compared with R. chrysanthum (Fig. 2). The ABR under N
treatment was higher than that under T + N treatment, followed by T
treatment, which indicates that growth of D. angustifolia was inhibited
under T treatment. Interaction of T and N treatments was not significant
(Table 1, F = 2.979, P b 0.000).
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
89
Table 1
Results of multi-factorial ANOVA test.
Variable
df
Proportional growth
Deyeuxia angustifolia
Plant community (PC)
Temperature (T)
Nitrogen (N)
PC ∗ T
PC ∗ N
N∗T
2
1
1
2
2
1
ABR
Nitrogen use efficiency
Rhododendron
chrysanthum
Deyeuxia
angustifolia
Rhododendron
chrysanthum
F
P
F
P
F
P
F
P
F
P
1.205
229.155
48.204
4.278
1.363
0.691
0.311
0.000
0.000
0.021
0.268
0.419
259.632
0.781
2.848
0.278
2.261
0.185
0.000
0.382
0.099
0.759
0.141
0.673
304.999
25.139
53.077
5.337
1.779
2.979
0.000
0.000
0.000
0.009
0.183
0.092
23.925
49.189
42.905
0.486
5.668
0.298
0.000
0.000
0.000
0.619
0.007
0.588
18.146
24.298
19.078
1.348
0.015
47.948
0.000
0.000
0.000
0.272
0.985
0.060
ABR = above-ground biomass ratio of D. angustifolia to R. chrysanthum. Results of four treatments were examined: 1) all three encroachment levels of plant communities (PC) combined;
2) treatments of temperature increase (T); 3) nitrogen addition (N); 4) temperature increase and nitrogen addition (N ∗ T). Underlined bold P values are significant at the 0.05 level.
3.3. NUE
D. angustifolia and R. chrysanthum both showed significant response
to simulated environmental changes in their nitrogen use efficiency, as
shown by multi-factoral ANOVA analysis (Table 1). NUEs of
D. angustifolia within all three encroachment levels were generally
higher than that of R. chrysanthum in the control plots (Fig. 3). Under
T treatment, NUE of D. angustifolia decreased greatly within all three encroachment levels (Fig. 3, Table 1, F = 49.189, P b 0.000) and was generally lower than that of R. chrysanthum, which confirmed the negative
effect of temperature increase on the growth of D. angustifolia. Under N
treatment, NUE of D. angustifolia greatly increased and was higher than
that of R. chrysanthum within all encroachment levels. The combined effect of T and N treatment on NUE of D. angustifolia and R. chrysanthum
was not significant (Table 1, P N 0.05). NUE of R. chrysanthum showed
positive responses to T (Table 1, F = 24.298, P b 0.000) and N treatments (Table 1, F = 19.078, P b 0.000). It was notable that within the
high encroachment level, NUE of D. angustifolia was higher than
R. chrysanthum under any treatment.
3.4. Diversity change
Various treatments basically increased the Shannon-Wiener diversity index in the communities of all three encroachment levels (Fig. 4,
a) indicating an increase in the number of species. The increment of
increase in the Shannon-Wiener index under N treatment was higher
than under T treatment, which indicates nitrogen input caused dramatic
diversity changes compared to increased temperature. Before treatments, the Shannon-Wiener index for the medium encroachment
level was higher than those of the low or high encroachment level.
After treatments, the diversity index was even higher, especially with
N treatment. Before treatments, the Pielou index for the low encroachment level was lower than those of the medium and high encroachment
levels (Fig. 4, b), which indicates a simple community structure within
the low encroachment level. After treatments, the community evenness
was generally decreased. The changes in community evenness under N
treatment were greater than under T treatment, which indicates that nitrogen input decreased the community evenness even though diversity
increased. From low to high encroachment levels, the decrement of
community evenness under N treatment was increased. Various treatments generally increased the species richness in the communities
within all three encroachment levels (Fig. 4, c). But N treatment greatly
increased the species richness of the plant community, especially within
the medium and high encroachment levels. According to our field observations, the plant species added were not shrubs, but forbs
(Aquilegia japonica and Saussurea tenerifolia) and Compositae
(Hieracium coreanum) from nearby communities. It can be inferred
that once D. angustifolia expands and dominates a community, it may
consequently change the community diversity of alpine tundra in the
Changbai Mountains.
4. Discussion
4.1. The two species' different responses to environmental change
Fig. 2. The ratio of above-ground biomass (mean ± 1 SE, n = 4) between the encroaching
plant, Deyeuxia angustifolia, and the native plant, R. chrysanthum, under treatments of temperature increase (T), nitrogen addition (N), temperature increase and nitrogen addition
(T + N), and control (C). LEL represents low encroachment level; MEL represents medium
encroachment level; LEL represents high encroachment level. Different lower-case letters
indicate a significant difference in results using different treatments within the same community type at the P b 0.05 level, according to one-way ANOVA with LSD test.
Low temperatures and poor nutrients are two common major constraints to plant growth in alpine habitats (Heer and Körner, 2002). Manipulative experiments conducted in Arctic tundra sites indicated that
shrubs benefited at the expense of herbaceous vegetation from increases in soil nutrients (Shaver et al., 2001; Bret-Harte et al., 2002;
Hobbie et al., 2005), which could occur directly through nitrogen deposition (Chapin et al., 1995; Hobbie et al., 2002). Also, community composition shifted from herbaceous-dominated to woody-dominated
(Formica et al., 2014). In contrast, in our study R. chrysanthum, the typical tundra shrub, showed negligible response to the simulated environmental changes. This may be because evergreen shrubs in alpine tundra
can be affected negatively by nutrient addition (Robinson et al., 1998).
Competition may not explain R. chrysanthum's lack of response to N addition and warming. We did not investigate the response of a pure
R. chrysanthum community to N addition and warming treatments in
this study. However, our another separate research has indicated that
R. chrysanthum showed negligible response to N addition and warming
treatments (Jin et al., 2014). This shows that even without competition,
R. chrysanthum did not respond to environmental changes.
D. angustifolia, the herbaceous plant from low elevations, grew in
90
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
Fig. 3. Nitrogen use efficiency (mean ± 1 SE, n = 4) of the encroaching plant, Deyeuxia
angustifolia, and the native plant, R. chrysanthum, under treatments of temperature increase (T), nitrogen addition (N), temperature increase and nitrogen addition (T + N),
and control (C). LEL represents low encroachment level; MEL represents medium encroachment level; LEL represents high encroachment level. Different lower-case letters indicate a significant difference in results using different treatments within the same
community type at the P b 0.05 level, according to one-way ANOVA with LSD test.
response to added nutrients but did not grow well under warmer conditions. Compared with R. chrysanthum, D. angustifolia could effectively
occupy the above-ground space by increasing tillers and growing rapidly by efficiently using nitrogen. Our results are consistent with two prior
studies. Aerts and de Caluwe (1994) found a difference in the N economy between evergreen and deciduous species, which can lead to deciduous species replacing evergreen species. Klanderud and Totland
(2005) found a shift in dominance hierarchies from shrub to graminoids
and forbs under nutrient addition.
It was unexpected that D. angustifolia responded negatively to
warmer conditions since experiments across Arctic tundra sites worldwide have shown that responses of plant species, especially graminoids,
to simulated increases in temperature and nutrient supply are generally
Fig. 4. The Shannon–Wiener index, Pielou index and species richness index (mean ± 1 SE,
n = 4) before and after treatments of temperature increase (T), nitrogen addition (N),
temperature increase and nitrogen addition (T + N), and control (C). LEL represents
low encroachment level; MEL represents medium encroachment level; LEL represents
high encroachment level.
positive (Bowman, 1994; Huang et al., 2011; Seastedt and Vaccaro,
2001; Elmendorf et al., 2012a; Elmendorf et al., 2012b). In Arctic areas,
the difference in relative humidity inside and outside of OTCs is not a
major issue because temperature is the most important limiting factor
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
for plant growth in high-latitude sites (Havström et al., 1993). However,
in the alpine tundra of the Changbai Mountains, the combined effect of
temperature and moisture is more important for plant growth than
temperature alone. D. angustifolia is a hydro-mesophyte perennial
herb, so water deficiency would limit its establishment and growth.
OTC treatment increased the air temperature while reducing soil moisture due to high evaporation (Bokhorst et al., 2008). Therefore, the negative response of D. angustifolia to OTC treatment was really because of
the coupled effect of higher temperatures and less water. In the mountain birch forest, forest canopy effectively reduces water evaporation
and provides relatively moist conditions for D. angustifolia. Therefore,
our findings do not necessarily demonstrate that increased nitrogen
has enabled the species to expand regardless of its natural climatic
niche within mountain birch forests. D. angustifolia grows well in the
mountain birch forest even as conditions become warmer. In China,
there are only two alpine tundra areas. To our knowledge,
D. angustifolia encroachment has only occurred in the alpine tundra of
the Changbai Mountains. Similarly, herbaceous plant species
encroaching at high elevations in alpine areas have also been found in
the USA (Wolf et al., 2003), Europe (Parolo and Rossi, 2008), and
Australian (McDougall et al., 2005). This signals a possible vegetation
change in Arctic and alpine regions even though the mechanisms of
such a change may differ by region.
In this study, our focus was mainly on the changes in the biomass of
D. angustifolia and R. chrysanthum in response to increased temperature
and nitrogen. We are unable to quantify the effect of competition or to
separate the impacts of competition on vegetation structure change.
None-the-less, we compared our findings with those conducted elsewhere and derived the follow synthesis. Fertilization had a negligible
or negative effect on the aboveground biomass of shrubs in this study,
which is consistent with research conducted by Gerdol et al. (2002)
an alpine area in Italy. However, Gerdol showed that removal of a codominant shrub species had a strong positive effect. This finding was
different from ours, which may be because Gerdol studied plant interactions between two shrubs, but in our study, a grass and a shrub
interacted. Conversely, in a Colorado alpine area in the USA, N fertilization had a negligible or negative effect on the relative abundance of a
forb and a bunchgrass, which was also different from our findings. We
found that the amount of atmospheric nitrogen deposited in alpine Colorado (6 kg N ha−1 yr−1) was much less than in the Changbai Mountains (23 kg N ha− 1 yr− 1), which may cause plant species to have
different responses.
4.2. Respective roles of elevated temperature and nitrogen deposition
Although many studies suggest a high correlation between climate
warming and the upward expansion of plant species (Huang et al.,
2011; Thuiller et al., 2007; McDougall et al., 2011), we consider that climate warming does not explain the expansion of D. angustifolia. We
have demonstrated that elevated temperature does not result in a
high seed germination rate of D. angustifolia within alpine tundra habitats (Zong et al., 2013c). In this study, growth of D. angustifolia showed a
negative response to warmer conditions. Unlike other upwardly
expanding plants (Klanderud and Birks, 2003), the effect of elevated
temperature on D. angustifolia expansion is not decisive. Furthermore,
D. angustifolia is commonly distributed at low elevations on all four
slopes in the alpine tundra of the Changbai Mountains; however, the
upward expansion phenomenon only occurred on the western slope.
If climate warming is promoting the D. angustifolia expansion, the phenomenon could be expected on other slopes, at least on the south slope
with similar habitat conditions, since variations in climatic conditions
on the four slopes were not found (Jin et al., 2013). Therefore, our results indicate that climate warming may not be the dominant factor in
promoting D. angustifolia encroachment to alpine tundra.
Nutrient supply as a driving growth mechanism is a reasonable explanation of D. angustifolia encroachment (Fowler et al., 1988). Alpine
91
tundra of the Changbai Mountains has received an increasingly high
load of atmospheric nitrogen deposition as monitored by the Chinese
Scientific Academy (Hu et al., 2009). Sufficient nitrogen supply is conducive to D. angustifolia encroachment. Additional nitrogen could accumulate on the western slope because it is windward, and westerly winds
prevail during the growing season (Liu and Zhou, 2009), which means
more atmospheric nitrogen deposition has been brought by precipitation. We had previously documented the movement of D. angustifolia
seed resources from the mountain birch forests at lower elevations,
where the plant grew vigorously, to the alpine tundra, following a typhoon disturbance in 1986 (Jin et al., 2013). Our results show that
once it is established, D. angustifolia could effectively spread and expand
by utilizing nitrogen. Moreover, other plant species in the community
that can tolerate lower nutrient levels are unable to compete successfully against this encroaching species. (Brooks, 2003). Our results support
the view of Alatalo et al. (2015) that for some herbaceous plant species
with high nitrogen use efficiency, climate warming may not be the decisive factor in the process of moving upward to high elevations. There
may be many influential factors in explaining D. angustifolia encroachment. Our evidence suggests nitrogen is one of the most important factors (Jin et al., 2015). However, at this stage of study, we are unable to
quantify the contribution of this influential factor. Results from our
study support our hypothesis, showing that nitrogen plays an important
role in promoting the movement of D. angustifolia to higher elevations
in the alpine tundra of the Changbai Mountains.
4.3. Future changes in alpine tundra vegetation in the Changbai Mountains
In general, tall species may expand at the expense of low stature species in the alpine region if temperature and soil nutrients increase
(Suding et al., 2004). In this study, external nitrogen input assisted
D. angustifolia to become dominant at the expense of the slowgrowing ericaceous dwarf shrub R. chrysanthum. Such results are consistent with other research concerning fertilization on alpine vegetation
(Fox, 1992; Nilsson et al., 2002; Robinson et al., 1998; Turkington
et al., 1998). Biodiversity is highly correlated to changes in the abundance of a dominant species because the dominant species may strongly
influence biotic conditions and is often an important driver of ecosystem function and community dynamics (Heer and Körner, 2002;
Hodáňová, 1981). In this study, the native dominant species,
R. chrysanthum, was suppressed as D. angustifolia expanded. Continued
D. angustifolia expansion would deeply change the biodiversity of tundra vegetation and may eventually result in the replacement of native
biota, especially if the increased supply of nitrogen continues. This prediction is consistent with the findings of Wolf et al. (2003) who studied
the invasion of sweet clover (Melilotus) in Montane Grasslands, Rocky
Mountain National Park, USA.
Nitrogen addition led to an increase in species richness and a decline
in evenness in this study. Similar results were found in an alpine tundra
area in Colorado, USA, by Suding et al. (2008), who showed that increased nitrogen led to the decline of a nitrogen conservative species.
The removal of this species in turn increased the abundance of a fastgrowing bunch grass and decreased community evenness by more
than 35% after six years. It can be inferred that as D. angustifolia becomes
dominant in the future, the number of nitrogen conservative species
will increase, but their abundance will be low. Temperature increases
would limit the growth of D. angustifolia while nitrogen addition
would promote its encroachment. We can anticipate that increases in
nitrogen will have a greater effect on long-term vegetation changes
and community biodiversity in the alpine tundra than will increases in
temperature. D. angustifolia encroachment has occurred during past decades, despite increased temperatures. Therefore, we could expect that
when the current nitrogen level (23 kg N ha−1 yr−1) increases to
46 kg N ha− 1 yr−1 in 2050 as projected by Lü et al. (2007), then
D. angustifolia populations would significantly increase (Fig. 5). Richness
would increase correspondingly. Evenness of plant communities would
92
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
at first increase because of the gradual increase of D. angustifolia, then
decrease because D. angustifolia would dominate the plant community
in the future.
5. Conclusion
To assess the respective effects of elevated temperature and atmospheric nitrogen deposition on the D. angustifolia expansion, we conducted experiments for three years to examine the response of an
upward expanding herbaceous plant, D. angustifolia, and a native alpine
shrub, R. chrysanthum, to conditions in which temperature and nitrogen
were increased. Treatments consisting of temperature increase, nitrogen addition, temperature increase combined with nitrogen addition,
and controls were conducted on the D. angustifolia communities within
three encroachment levels (low, medium, and high encroachment
levels). Results showed that temperature increase had a negative effect
on the growth of D. angustifolia but nitrogen addition dramatically stimulated D. angustifolia expansion by increasing the number of tillers.
Compared to R. chrysanthum, D. angustifolia could effectively occupy
the above-ground space by efficiently using nitrogen. The native alpine
shrub, R. chrysanthum, showed negligible responses to the simulated
environmental changes, and its growth was suppressed by
D. angustifolia, especially in the high encroachment community under
N treatment. Our research highlights the fact that nutrient perturbation
may be more important than temperature perturbation in promoting
D. angustifolia encroachment within the nutrient- and species-poor alpine tundra ecosystem in the Changbai Mountains.
Fig. 5. Theoretical prediction of long-term changes in the Shannon–Wiener diversity index
and Pielou index for plant communities in the alpine tundra of the Changbai Mountains,
based on changes in temperature, atmospheric nitrogen deposition, and the corresponding changes in distribution of D. angustifolia (DA).
Acknowledgments
This study was supported by National Natural Science Foundation of
China (No. 41501089), Project Funded by China Postdoctoral Science
Foundation (2015M580241), Open Foundation of Changbai Scientific
Research Academy (201501), and the Doctoral Fund of Ministry of Education of China (No. 20120043110014). I would like to thank Meng
Xiangjun and Liu Lina for their assistance with field work.
References
Aerts, R., Cornelissen, J.H.C., Van Logtestijn, R.S.P., Callaghan, T.V., 2007. Climate change
has only a minor impact on nutrient resorption parameters in a high-latitude
peatland. Oecologia 151, 132–139.
Aerts, R., de Caluwe, H., 1994. Nitrogen use efficiency of Carex species in relation to nitrogen supply. Ecology 75, 2362–2372.
Alatalo, J.M., Little, C.J., Jägerbrand, A.K., Molau, U., 2015. Vascular plant abundance and diversity in an alpine heath under observed and simulated global change. SCI. REP-UK
10197. http://dx.doi.org/10.1038/srep10197.
Beckage, B., Osborne, B., Gavin, D.G., Pucko, C., Siccama, T., Perkins, T., 2008. A rapid upward shift of a forest ecotone during 40 years of warming in the Green Mountains
of Vermont. Proc. Natl. Acad. Sci. U. S. A. 105, 4197–4202.
Bokhorst, S., Huiskes, A., Convey, P., Van Bodegom, P.M., Aerts, R., 2008. Climate change
effects on soil arthropod communities from the Falkland Islands and the Maritime
Antarctic. Soil Biol. Biochem. 40 (7), 1547–1556.
Bowman, W.D., 1994. Accumulation and use of nitrogen and phosphorus following fertilization in two alpine tundra communities. Oikos 70, 261–270.
Boyer, K.E., Zedler, J.B., 1999. Nitrogen addition could shift plant community composition
in a restored California salt marsh. Restor. Ecol. 7, 74–85.
Bret-Harte, M.S., Shaver, G.R., Chapin, F.S., 2002. Primary and secondary stem growth in
Arctic shrubs: implications for community response to environmental change.
J. Ecol. 90, 251–267.
Brooks, M.L., 2003. Effects of increased soil nitrogen on the dominance of alien annual
plants in the Mojave desert. J. Appl. Ecol. 40 (2), 344–353.
Chapin III, F.S., Shaver, G.R., Giblin, A.E., Nadelhoffer, K.J., Laundre, J.A., 1995. Responses of
Arctic tundra to experimental and observed changes in climate. Ecology 76 (3),
694–711.
Curtis, C.J., Emmett, B.A., Grant, H., Kernan, M., Reynolds, B., Shilland, E., 2005. Nitrogen
saturation in UK moorlands: the critical role of bryophytes and lichens in determining retention of atmospheric N deposition. J. Appl. Ecol. 42, 507–517.
Elmendorf, S.C., Henry, G.H., Hollister, R.D., Björk, R.G., Bjorkman, A.D., Callaghan, T.V., et
al., 2012a. Global assessment of experimental climate warming on tundra vegetation:
heterogeneity over space and time. Ecol. Lett. 15 (2), 164–175.
Elmendorf, S.C., Henry, G.H., Hollister, R.D., Björk, R.G., Boulanger-Lapointe, N., Cooper, E.J.,
et al., 2012b. Plot-scale evidence of tundra vegetation change and links to recent
summer warming. Nat. Clim. Chang. 2 (6), 453–457.
Formica, A., Farrer, E.C., Ashton, I.W., Suding, K.N., 2014. Shrub expansion over the past
62 years in Rocky Mountain alpine tundra: possible causes and consequences. Arct.
Antarct. Alp. Res. 46 (3), 616–631.
Fowler, D., Cape, J.N., Leith, I.D., Choularton, T.W., Gay, M.J., Jones, A., 1988. The influence
of altitude on rainfall composition at Great Dun Fell. Atmos. Environ. 22, 1355–1362.
Fox, J.F., 1992. Responses of diversity and growth-form dominance to fertility in Alaskan
tundra fellfield communities. Arct. Antarct. Alp. Res. 24 (3), 233–237.
Gaur, U.N., Raturi, G.P., Bhatt, A.B., 2003. Quantitative response of vegetation in Glacial
Moraine of Central Himalaya. Environmentalist 23, 237–247.
Gerdol, R., Brancaleoni, L., Marchesini, R., Bragazza, L., 2002. Nutrient and carbon relations
in subalpine dwarf shrubs after neighbour removal or fertilization in northern Italy.
Oecologia 130, 476–483.
Green, E.K., Galatowitsch, S.M., 2002. Effects of Phalaris arundinacea and nitrate-N addition on the establishment of wetland plant communities. J. Appl. Ecol. 39, 134–144.
Harte, J., Shaw, R., 1995. Shifting dominance within a montane vegetation community: results of a climate-warming experiment. Science 267, 876–880.
Havström, M., Callaghan, T.V., Jonasson, S., 1993. Differential growth responses of
Cassiope tetragona, an arctic dwarf-shrub, to environmental perturbations among
three contrasting high-and subarctic sites. Oikos 66 (3), 389–402.
Heer, C., Körner, C., 2002. High elevation pioneer plants are sensitive to mineral nutrient
addition. Basic. Appl. Ecol. 3 (1), 39–47.
Hobbie, S.E., Nadelhoffer, K.J., Högberg, P., 2002. A synthesis: the role of nutrients as constraints on carbon balances in boreal and Arctic regions. Plant and Soil 242 (1),
163–170.
Hobbie, S.E., Gough, L., Shaver, G.R., 2005. Species compositional differences on differentaged glacial landscapes drive contrasting responses of tundra to nutrient addition.
J. Ecol. 93 (4), 770–782.
Hodáňová, D., 1981. Plant strategies and vegetation processes. Biol. Plantarum. 23 (4),
254.
Hu, Y.L., Han, S.J., Li, X.F., Zhao, Y.T., Li, D., 2009. Responses of soil available nitrogen of natural forest and secondary forest to simulated N deposition in Changbai Mountain.
Journal of Northeast Forestry University 37 (5), 36–42 (In Chinese).
Huang, D., Haack, R.A., Zhang, R., 2011. Does global warming increase establishment rates
of invasive alien species? A centurial time series analysis. PLoS One 6, e24733.
Huang, X.C., Li, C.H., 1984. An analysis on the ecology of alpine tundra landscape of
Changbai Mountains. Acta Geograph. Sin. 39 (3), 285–297 (In Chinese).
S. Zong et al. / Science of the Total Environment 544 (2016) 85–93
Humphries, S.E., Groves, R.H., Mitchell, D.S., 1991. Plant Invasions of Australian Ecosystems: A Status Review and Management Directions. Australian National Parks and
Wildlife Service.
Jin, Y.H., Xu, J.W., Liang, Y., Zong, S.W., 2013. Effects of volcanic interference on the vegetation distribution of Changbai Mountain. Sci. Geogr. Sin. 33, 203–208 (In Chinese).
Jin, Y.H., Xu, J.W., Zong, S.W., Wang, P., 2014. Experimental study on the effects of nitrogen
deposition on the tundra vegetation of the Changbai Mountains. Scientia Geographica
Sinica. 34 (12), 1526–1532 (In Chinese).
Jin, Y., Xu, J., Wang, Y., Wang, S., Chen, Z., Huang, X., Niu, L., 2015. Effects of nitrogen deposition on tundra vegetation undergoing invasion by Deyeuxia angustifolia in
Changbai Mountains. Chinese. Geogr. Sci. doi: http://dx.doi.org/10.1007/s11769015-0746-1.
Kammer, P.M., Schöb, C., Choler, P., 2007. Increasing species richness on mountain summits: upward migration due to anthropogenic climate change or re-colonisation?
J. Veg. Sci. 18 (2), 301–306.
Körner, C., 1995. Alpine Plant Diversity: A Global Survey and Functional Interpretations.
Arctic and Alpine Biodiversity: Patterns, Causes and Ecosystem Consequences.
Springer, pp. 45–62.
Körner, C., 2003. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems.
Springer.
Kelly, A.E., Goulden, M.L., 2008. Rapid shifts in plant distribution with recent climate
change. Proc. Natl. Acad. Sci. U. S. A. 105, 11823–11826.
Klanderud, K., Birks, H.J.B., 2003. Recent increases in species richness and shifts in altitudinal distributions of Norwegian mountain plants. The Holocene 13 (1), 1–6.
Klanderud, K., Totland, Ø., 2005. Simulated climate change altered dominance hierarchies
and diversity of an alpine biodiversity hotspot. Ecology 86 (8), 2047–2054.
Liu, Q.J., Xu, Q.Q., Zhang, G.C., 2009. Impact of alpine snowpack on primary productivity in
Rhododendron chrysanthum community in Changbai Mountains, China. Acta Ecological Sinica. 29 (8), 4035–4044 (In Chinese).
Liu, X.G., Zhou, H.X., 2009. Analysis on the regional precipitation characteristics of western slope in Changbai Mountain. Jilin meteorology 3, 25–26 (In Chinese).
Lü, C.Q., Tian, H.Q., Huang, Y., 2007. Ecological effects of increased nitrogen deposition in
terrestrial ecosystems. Chinese Journal of Plant Ecology. 31 (2), 205–218 (In Chinese).
Marion, G.M., Henry, G.H.R., Freckman, D.W., Johnstone, J., Jones, G., Jones, M.H., 1997.
Open-top designs for manipulating field temperature in high-latitude ecosystems.
Glob. Chang. Biol. 3 (S1), 20–32.
McDougall, K.L., Khuroo, A.A., Loope, L.L., Parks, C.G., Pauchard, A., Reshi, Z.A., 2011. Plant
invasions in mountains: global lessons for better management. Mt. Res. Dev. 31 (4),
380–387.
McDougall, K.L., Morgan, J.W., Walsh, N.G., Williams, R.J., 2005. Plant invasions in treeless
vegetation of the Australian Alps. Perspect. Plant Ecol. 7 (3), 159–171.
Nilsson, M.C., Wardle, D.A., Zackrisson, O., Jäderlund, A., 2002. Effects of alleviation of ecological stresses on an alpine tundra community over an eight-year period. Oikos 97
(1), 3–17.
Parolo, G., Rossi, G., 2008. Upward migration of vascular plants following a climate
warming trend in the Alps. Basic. Appl. Ecol. 9 (2), 100–107.
Pauli, H., Gottfried, M., Reiter, K., Klettner, C., Grabherr, G., 2007. Signals of range expansions and contractions of vascular plants in the high Alps: observations
(1994–2004) at the GLORIA* master site Schrankogel, Tyrol, Austria. Glob. Chang.
Biol. 13 (1), 147–156.
Pearce, I.S.K., Woodin, S.J., Van der Wal, R., 2003. Physiological and growth responses of
the montane bryophyte Racomitrium lanuginosum to atmospheric nitrogen deposition. New Phytol. 160 (1), 145–155.
93
Phoenix, G.K., Hicks, W.K., Cinderby, S., Kuylenstierna, J.C., Stock, W.D., Dentener, F.J., et al.,
2006. Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a
greater global perspective in assessing N deposition impacts. Glob. Chang. Biol. 12
(3), 470–476.
Qian, H., 1992. Alpine tundra vegetation on the Changbai Mountains. For. Res. Ecosystem
6, 72–96 (In Chinese).
Qian, J.J., 1979. Vertical plant list of the Changbai Mountains. Northeast Normal University
Press, Changchun (In Chinese).
Quiroz, C.L., Choler, P., Baptist, F., Gonzalez-Teuber, M., Molina-Montenegro, M.A.,
Cavieres, L.A., 2009. Alpine dandelions originated in the native and introduced
range differ in their responses to environmental constraints. Ecol. Res. 24 (1),
175–183.
Robinson, C.H., Wookey, P.A., Lee, J.A., Callaghan, T.V., Press, M.C., 1998. Plant community
responses to simulated environmental change at a high Arctic polar semi-desert.
Ecology 79 (3), 856–866.
Sætersdal, M., Birks, H.J.B., 1997. A comparative ecological study of Norwegian mountain
plants in relation to possible future climatic change. J. Biogeogr. 24 (2), 127–152.
Seastedt, T., Vaccaro, L., 2001. Plant species richness, productivity, and nitrogen and phosphorus limitations across a snowpack gradient in alpine tundra, Colorado, USA. Arct.
Antarct. Alp. Res. 33 (1), 100–106.
Shaver, G.R., Bret-Harte, M.S., Jones, M.H., Johnstone, J., Gough, L., Laundre, J., et al., 2001.
Species composition interacts with fertilizer to control long-term change in tundra
productivity. Ecology 82 (11), 3163–3181.
Suding, K.N., LeJeune, K.D., Seastedt, T.R., 2004. Competitive impacts and responses of an
invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141
(3), 526–535.
Suding, K.N., Ashton, I.W., Bechtold, H., Bowman, W.D., Mobley, M.L., Winkleman, R.,
2008. Plant and microbe contribution to community resilience in a directionally
changing environment. Ecol. Monogr. 78 (3), 313–329.
Thuiller, W., Richardson, D.M., Midgley, G.F., 2007. Will climate change promote alien
plant invasions? Biological invasions. Springer, pp. 197-211.
Turkington, R., John, E., Krebs, C.J., Dale, M.R.T., Nams, V.O., Boonstra, R., et al., 1998. The
effects of NPK fertilization for nine years on boreal forest vegetation in northwestern
Canada. J. Veg. Sci. 9 (3), 333–346.
Walther, G.R., Beißner, S., Burga, C.A., 2005. Trends in the upward shift of alpine plants.
J. Veg. Sci. 16 (5), 541–548.
Williamson, M.H., Fitter, A., 1996. The characters of successful invaders. Biol. Conserv. 78
(1), 163–170.
Wolf, J.J., Beatty, S.W., Carey, G., 2003. Invasion by sweet clover (Melilotus) in montane
grasslands, Rocky Mountain National Park. Ann. Assoc. Am. Geogr. 93 (3), 531–543.
Zong, S.W., Wu, Z.F., Du, H.B., 2013a. Study on climate change in Alpine tundra of the
Changbai Mountain in growing season in recent 52 years. Arid Zone Research 30
(1), 41–49 (In Chinese).
Zong, S.W., Xu, J.W., Wu, Z.F., Qiao, L.L., Wang, D.D., Meng, X.J., et al., 2013b. Analysis on
the process and impacts of Deyeuxia angustifolia invasion on the alpine tundra,
Changbai Mountain. Acta Ecol. Sin. 34 (23), 6837–6846 (In Chinese).
Zong, S.W., Xu, J.W., Wu, Z.F., 2013c. Investigation and mechanism analysis on the invasion of Deyeuxia angustifolia to tundra zone in western slope of Changbai Mountain.
J. Mt. Sci. 31 (4), 448–455 (In Chinese).