Journal of
Plant Ecology
Volume 6, Number 1,
Pages 36–47
March 2013
doi:10.1093/jpe/rts030
Advance Access publication
21 September 2012
available online at
www.jpe.oxfordjournals.org
Regeneration dynamics of
subalpine fir (Abies fargesii)
forest across the altitudinal range
in the Shennongjia Mountains,
central China
Haishan Dang, Kerong Zhang, Yanjun Zhang, Xunzhang Tong
and Quanfa Zhang*
Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences,
Wuhan 430074, People’s Republic of China
*Correspondence address. Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical
Garden, Chinese Academy of Sciences, Wuhan 430074, People’s Republic of China. Tel: +86-27-87510702;
Fax: +86-27-87510251; E-mail: [email protected]
Abstract
Aims
Age structure and regeneration dynamics have been used to infer
population response to environmental events and reconstruct forest development history. The aim of this study was to characterize
and examine the differences of the age structure and regeneration
dynamics of subalpine fir (Abies fargesii) forest across the altitudinal
range in the north and south aspects in the Shennongjia Mountains,
central China.
Methods
Ten plots (20 × 20 m) at each altitudinal zone (i.e. the low elevation,
the middle elevation and the high elevation) were established in
both the north and south aspects of the Shennongjia Mountains,
central China. Dendroecological techniques were applied to obtain
information about ages of the trees in the plots. The population age
structure was analyzed to investigate the regeneration dynamics
across the altitudinal range.
Important findings
Fir regeneration dynamics and age structure were similar in both
aspects, and a unimodal population age structure was found at
Introduction
Environmental factors could affect the processes of
establishment and regeneration of plants, and population
dynamics of plant species, especially those with long lifespan,
could be considered as an indicator of vegetation succession
different altitudinal sites of both aspects, indicating that environmental factors might play an important role in shaping the regeneration dynamics and age structure of A. fargesii across its altitudinal
range. There was a sustained recruitment during the 19th century,
but the regeneration was rarer in the last century at low and midelevations. A significant greater number of fir seedlings and saplings
recruited at high elevations in the last century, and fir tree density at
high elevations was significantly higher than that at low elevations.
Thus, the fir population at the high elevations showed a significant
increase in recruitment and stem density in the last century, and
we propose that the gradual infilling of fir seedlings might result in
changes in regeneration dynamics and stand structure of the subalpine fir forest at high elevations in the Shennongjia Mountains,
central China.
Keywords: regeneration dynamics • age structure • Abies
fargesii • the Shennongjia Mountains
Received: 11 June 2012 Revised: 31 July 2012 Accepted: 12
August 2012
as well as environmental changes across their distributional
range (Brubaker 1986; Camarero et al. 2005; Wang et al.
2004). The long lifespan of trees makes it infeasible to trace
their whole life history, so a static investigation on age
structure and regeneration of populations is often accepted in
examining population dynamics and in inferring population
© The Author 2012. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
All rights reserved. For permissions, please email: [email protected]
Dang et al. | Regeneration dynamics of subalpine fir forest37
response to known environmental events (Brubaker 1986;
Svensson and Jeglum 2001; Wang et al. 2004). Investigations
on age structure and regeneration dynamics could not only
give insights into the processes that determined population
structure and pattern over time (Lv and Zhang 2011; Svensson
and Jeglum 2001; Veblen 1989) but also serve as a basic point
of reference central to restoration and management of forest
ecosystems (Covington et al. 1997; Fulé et al. 1997; Mast
et al. 1999; Wang et al. 2004). Assessing and analyzing age
structure and regeneration dynamics are therefore essential
to understand the ecological processes of natural forests,
and studies on regeneration dynamics in many forests have
typically dealt with the analysis of age and size structures and
seedling density (Antos and Parish 2002; Fyllas et al. 2008;
Peñuelas et al. 2007; Taylor and Qin 1988; Taylor et al. 1996;
Wang et al. 2004; Wangda and Ohsawa 2006).
Plant could generally grow and survive in a certain range
of environmental conditions. Within the geographical range
of a species, environmental conditions vary along physiographic and ecological gradients, creating the potential for
spatial heterogeneity in growth-limiting factors associated
with tree establishment and regeneration (Block and Treter
2001; Carrer et al. 2007; Peñuelas et al. 2007; Peterson et al.
2002). Across the distributional range, optimal environmental conditions could enable a well-developed population with
an expected reversed-J shape of the size class distribution
and age structure, while some environmental factors often
become limiting factors and result in poor establishment of
plant individuals and insufficient recruitment of the local
population (Block and Treter 2001; Holz et al. 2006; Taylor
and Qin 1988; Wang et al. 2004). As a result, age structure and
regeneration dynamics of plant populations, especially those
with long-lived species, could act as an indicator of environmental changes across the distributional range.
Some tree species occur across a wide altitudinal range and
play an important role in local ecosystems. In the subalpine
region, the environmental conditions trees are experiencing
differ greatly with altitude; thus, the limiting factors related
to seedling establishment and tree recruitment might vary
with changes in altitude (Block and Treter 2001; Peñuelas
et al. 2007; Wangda and Ohsawa 2006). The understanding of
environmental influences on population structure and regeneration dynamics of the natural forests could be improved by
studies that sample across the altitudinal distributional range
from harsh to mild environmental conditions (Dang et al.
2010; Lingua et al. 2008; Peñuelas et al. 2007; Veblen 1989;
Wang et al. 2004; Wangda and Ohsawa 2006).
The forest of subalpine fir, Abies fargesii, is one of the most
important vegetation in the Qinba Mountains (including the
Daba Mountains and the Shennongjia Mountains), a biodiversity hotspot in China. The subalpine fir (A. fargesii) forest occurs over a wide range above 2300 m, and the conifers
dominated by subalpine fir (A. fargesii) occupy the area above
2500 m in elevation in the Shennongjia Mountains, central China. Although some of the subalpine fir forests in the
Shennongjia Mountains were clearly cut in the 1970s (Jiang
et al. 2009), many remaining intact forests occur in the region
due to the relatively difficult accessibility in the subalpine
forest areas. However, very little is known about the regeneration dynamics of the subalpine fir forest across its altitudinal range due to insufficient research. An understanding of
age structure and regeneration patterns over the past 200–
300 years could provide a context within which to interpret
recent changes as inferred from the present patterns of tree
establishment, and this type of ecological knowledge is fundamental for conservation and sustainable utilization of the
mountain ecosystems (Antos and Parish 2002; Cullen et al.
2001; Wangda and Ohsawa 2006).
In this study, the subalpine fir (A. fargesii) forest was investigated, and its regeneration pattern and age structure were
examined by ageing trees and dating periods of past tree
establishment across its altitudinal distribution range, i.e. the
deciduous to conifer forest transitional zone at low elevations,
the interior forest dominated by A. fargesii at midelevations
and the treeline environment at the high elevations of the
subalpine fir forest, in both the north and south aspects of
the Shennongjia Mountains. The specific goal of this study is
to examine the differences of age structure and regeneration
dynamics of the subalpine fir trees based on their population
structure, seedling/sapling density and regeneration status
along an altitudinal gradient in the north and south aspects.
METHODS
Study area
The study was conducted in the Shennongjia National
Nature Reserve (31°22′–31°37′N, 110°03′–110°34′E) in the
Shenongjia Mountains, an eastern extension of the Daba
Mountains in Hubei Province, central China (Fig. 1). The
Daba Mountains run east–west and are a biologically rich area
of China. The study area is situated in the transitional zone
from plateau in the west to plain in the east in terms of topography (Zhang et al. 2007). Elevation in the study area ranges
from 900 to 3105 m. The highest summit of the Shennongjia
Mountains, Shennongding with an elevation of 3105 m a.s.l.,
is the highest peak in central China.
The Shennongjia Mountains are deeply affected by southeast subtropical monsoon, characterized by abundant precipitation and a moderate mean air temperature, with high
temperatures (monthly mean temperature >25°C) and much
rain (monthly precipitation >250 mm) in summer and a
cold (monthly mean temperature <−4°C) and dry (monthly
precipitation <10 mm) climate in winter (Zhao et al. 2005).
Annual precipitation ranges from 800 to 2500 mm, most of
which falls between June and August. Snowfall usually lasts
5 months (from November to March), and annual temperature ranges from −19.5°C in January to 29.4°C in July (Zhang
et al. 2007). The soil of the study site was classified as a mountain gray-brown forest soil type. Vegetation of the study area
comprises of deciduous broad-leaved forests, mixed conifer
38
Journal of Plant Ecology
Figure 1: locations of the study sites (filled circle) in the Shennongjia Mountains, central China. NL, low elevation in the north aspect; NM,
midelevation in the north aspect; NH, high elevation in the north aspect; SL, low elevation in the south aspect; SM, midelevation in the south
aspect; SH, high elevation in the south aspect. (filled triangle 1) Peak Shennongding (3105 m); (filled triangle 2) peak Xiaoshennongjia (3005 m).
and deciduous forests, conifer forests and subalpine meadow
along the elevational gradient. Fargesia murielae is a common
understory species. The deciduous broad-leaved forests grow
between the elevation of 900–1800 m, and the mixed conifer
and deciduous forests grow between the elevation of 1800–
2500 m. Conifers dominated by subalpine fir (A. fargesii)
occupy the area above 2500 m in elevation, and A. fargesii
usually forms single-species stands or develops into mixed forests with birch (Betula albo-sinensis) above 2500 m. Subalpine
meadow occurs above 2700 m a.s.l.
The present research focuses on the conifer forests
dominated by A. fargesii, i.e. above the elevation of 2500
m. Besides A. fargesii, the subalpine fir forests in the
Shennongjia Mountains are composed of other nine species
(Table 1), each of which only has a low importance value in
the stands (Yu et al. 2008). Although some of the subalpine
fir forests in the Shennongjia Mountains were clear cut in
the 1970s (Jiang et al. 2009), many remaining intact forests
occur in the region due to the relatively difficult accessibility
in the subalpine forest areas. Disturbance agent such as fire
that has played an important role in tree regeneration (Elliott
and Baker 2004) is absent in the area above the elevation
of 2000 m in the Shennongjia region (Chen et al. 1992). No
evidence of previous logging is found in the subalpine fir
stands and they might be similar to those observed more than
half a century ago (Wang 1940; Zhang et al. 2007). Thus,
this study only examines regeneration dynamics of A. fargesii
based on its population structure and seedling/sapling density
Table 1: species composition of the subalpine fir (A. fargesii) forest in the Shennongjia Mountains, central China
Density
(stems/ha)
Dominance
(m2/ha)
Abies fargesii
368.33
35.22
28.57
67.53
76.58
57.56
Betula albo-sinensis
101.17
5.25
20.95
18.55
11.42
16.97
Rhododendron oreodoxa var. fargesii
28.33
3.42
13.33
5.19
7.44
8.65
Sorbus hupehensis
21.67
1.31
16.19
3.97
2.85
7.67
Acer oliverianum
6.67
0.1
5.71
1.22
0.22
2.38
Prunus tomentosa
3.33
0.43
4.76
0.61
0.93
2.10
Acer davidii
5
0.15
4.76
0.92
0.33
2.00
Buxus sinica
6.67
0.08
2.86
1.22
0.17
1.42
Euonymus oblongifolius
1.67
0.02
1.90
0.31
0.04
0.75
Crataegus wilsonii
2.56
0.01
0.95
0.47
0.02
Species
Total
545.4
45.99
Relative
frequency
100
Relative
density
100
Relative
dominance
100
Importance
value
0.48
100
Dang et al. | Regeneration dynamics of subalpine fir forest39
across its altitudinal range in the Shennongjia Mountains,
central China.
RESULTS
Field sampling
Main characteristics of A. fargesii population, such as mean
dbh, tree density, basal area and canopy coverage, varied at the three different altitudinal sites in both the north
and south aspects (Table 2). The dbh of the fir population
declined with the increase in elevation, and the dbh at the
low and midelevations was significantly greater than that at
the high elevations in both aspects (P ≤ 0.05). The fir population at midelevations in both aspects had the largest basal
area, which was significantly larger than that at the low and
high elevations (P ≤ 0.05). The fir tree density increased with
increasing elevation, and the fir population at high elevations
had significantly higher density than that at the low elevations in both the north and south aspects (P ≤ 0.05). A fargesii
population at the midelevations had the largest canopy coverage, but the canopy coverage showed no significant differences among the three different altitudinal sites in both
aspects (Table 2).
In the summer of 2006, we measured age structure and
regeneration dynamics at the low elevations (the deciduous
to conifer forest transitional zone), the middle elevations (the
interior forest dominated by A. fargesii) and the high elevations
(the treeline environment) by sampling 10 plots (20 × 20 m) at
each altitudinal zone in both the north and south aspects of the
Shennongjia Mountains (Fig. 1 and Table 2). These plots were
selected based on the criteria that there were similar habitats
and that the stands should represent the fir forest structure
at each elevational site. Within each plot, the diameter at
breast height (dbh, 1.3 m above the ground level) of each fir
tree was measured, and the fir trees more than 2 m in height
were cored at breast height. One sound core per fir tree was
extracted in the direction parallel to the slope contour using
increment borer. Within each plot, five 3 × 3 m subplots were
established to determine fir sapling (0.5–2 m in height) and
seedling (<0.5 m in height) density. At each altitudinal site, at
least 20 fir saplings and seedlings with normal growth form
were destructively sampled to create an age-height regression
to estimate the time to reach breast height.
Fir population structure
Data analyses
The increment cores were air-dried in the laboratory and
mounted on grooved wooden boards. Mounted increment
cores were sanded with progressively finer grades of sandpaper to produce a flat and polished surface on which treering boundaries were clearly visible. The ages of cores were
read using the Windendro image-analysis system (Regent
Instruments Inc., Quebec, Canada). For the increment cores
missing the pith, the number of rings required to reach the
pith was estimated geometrically (Duncan 1989; Szeicz and
Macdonald 1995).
The correlations between age (y, year) and height (x, cm)
of the fir seedlings/saplings at different altitudinal sites were
all statistically significant (Fig. 2), and it took the fir trees at
the low, middle and high elevation about 26, 28 and 32 years
to reach breast height, respectively. Thus, the ages of individual fir trees were determined by adding the number of
26, 28 and 32 rings on each core at the low, middle and high
elevations, respectively. The age distribution was presented
at 10-year intervals to eliminate the possible errors in the
age determination process, and all the fir trees were also
grouped into size classes at 5 cm intervals according to dbh at
each altitudinal site. The cross-sectional area at breast height
(cm2) was computed using the dbh data. Normal distribution and homoscedasticity of tests of the data (including basal
area, tree density, canopy coverage, age structure, etc.) were
confirmed, and ANOVAs and post hoc Tukey HSD tests were
applied to test differences in the characteristics of A. fargesii
population at the different altitudinal sites in both the north
and south aspects.
Figure 2: correlations between age and height of fir sapling/seedling (<2 m in height) at different altitudinal sites in the Shennongjia
Mountains, central China.
40
Journal of Plant Ecology
Table 2: main characteristics of A. fargesii population at the different altitudinal sites in the north and south aspects of the Shennongjia
Mountains, central China
Elevation (m)
Number of plots
dbh (cm)
Basal area (m2/ha)
Density (stems/ha) Canopy coverage (%)
Low elevation
2450–2650
10
45.3 ± 8.2 (73.3)a
31.92 ± 6.5a
360 ± 169.19a
53.2 ± 6.38a
Midelevation
2650–2850
10
36.3 ± 6.3 (68.3)a
47.77 ± 7.13b
495 ± 180.62b
68.4 ± 6.07a
High elevation
2850–2950
10
23.1 ± 4.6 (42.1)b
23.10 ± 19.58a
560 ± 132.99b
57.8 ± 1.92a
Low elevation
2300–2450
10
47.3 ± 2.9 (74.1)a
34.85 ± 8.99a
365 ± 170.17a
56.2 ± 2.59a
Midelevation
2450–2800
10
38.8 ± 5.0 (63.2)a
49.43 ± 7.43b
450 ± 83.67ab
65.2 ± 4.92a
High elevation
2800–2900
10
24.4 ± 1.1 (45.5)b
25.32 ± 4.42a
520 ± 105.48b
54.8 ± 7.29a
Altitudinal sites
North aspect
South aspect
Data are presented in mean ± SE. The values of maximum dbh are given in the parentheses. The different letters indicate the significance at P
≤ 0.05 level.
Distribution of size classes
In general, the fir population showed a bell-shaped size distribution pattern (5 cm dbh intervals) at the three different
elevations in both the north and south aspects (Fig. 3). At
the high elevations of both aspects, small fir trees with dbh
< 15 cm accounted, respectively, for more than 24 and 19%
Figure 3: size class distribution of the fir trees at different altitudinal sites in the north and south aspects of the Shennongjia Mountains, central
China. Different letters within each size class indicate the difference at P ≤ 0.05 level.
Dang et al. | Regeneration dynamics of subalpine fir forest41
Figure 4: line regressions between age and dbh of fir trees at different elevations in both the north and south aspects of the Shennongjia
Mountains, central China.
in the north and south aspect, while no fir trees occurred in
the large dbh classes more than 45 and 50 cm in the north
and south aspect, respectively. At the midelevations of both
aspects, the subalpine fir trees mainly appeared in the middle
dbh classes from 25 to 50 cm. The smaller dbh class (<25 cm)
and the larger dbh classes (>50 cm) had a relatively small fraction of the total individuals. At the low elevations, however,
large fir trees with dbh > 40 cm, respectively, accounted for
more than 73 and 71% of the total fir trees in both aspects,
while the small fir trees with dbh < 15 cm were very sparse in
the north aspect (3.8%) and in the south aspect (2.4%). The
size class distribution also indicated that the percentage of the
large fir trees with dbh > 40 cm gradually decreased, and the
percentage of the small fir trees with dbh < 40 cm gradually
increased with the increase in elevation in both aspects. At
each of the dbh classes less than 30 cm, fir individuals at the
high elevations were significantly more than at the middle
and low elevations. At each of the dbh classes greater than
40 cm, however, fir individuals at the low elevations were significantly more than at the high elevations in both the north
and south aspects (Fig. 3).
The correlation between age and dbh of the fir trees at different elevations was weak, and the correlation showed an
increased trend with the decrease in elevation in both the
north and south aspects (Fig. 4). In addition, at the same distributional area along the elevational gradient, the correlation
between age and dbh in the north aspect was stronger than
that in the south aspect (Fig. 4).
Age structure
In total, 1005 fir cores were used to count the tree rings at
each altitudinal site in both the north and south aspect. Age
structure analysis indicated that fir trees’ mean age decreased
with the increase in elevation in both the north and south
aspects (Table 3). Statistical analysis indicated that the subalpine fir trees at the high elevations were significantly younger
than those at the low elevations (ANOVA, P ≤ 0.05), and the
quantity of fir seedling and sapling remarkably increased with
increasing altitude in both aspects.
Age structure distribution was similar to that for the size
class distribution of the fir population, displaying a decrease
in the number of large fir trees and an increase in the number
42
Journal of Plant Ecology
Table 3: age statistics and number of seedling/sapling of the subalpine fir (A. fargesii) population at different altitudinal sites in the north
and south aspects of the Shennongjia Mountains, central China
Altitudinal sites
Elevation (m)
Mean age (year)
SD
Range (year)
Density of seedlings and
saplings (no./ha)
North aspect
Low elevation
2500–2650
150.64a
46.02
82–276
400a
Midelevation
2650–2850
125.16a
49.78
41–237
1300b
High elevation
2850–2950
83.05b
29.57
20–174
2000c
South aspect
Low elevation
2500–2600
155.64a
42.26
85–267
200a
Midelevation
2600–2800
109.19b
20.28
50–152
600b
High elevation
2800–2900
98.21b
16.17
38–146
2300c
The different letters in each column indicate the significance at P ≤ 0.05 level.
of young fir trees along the altitudinal gradient in both
aspects (Figs 3 and 5). At the high elevations of both aspects,
the majority of the fir trees were between 50 and 120 years
old, and only 10.9 and 10.8% of the fir trees were older than
120 years in the north and south aspects, respectively (Fig. 5).
At the midelevations, most of the fir trees’ age ranged from 80
to 200 years in the north aspect and from 90 to 170 years in
the south aspect. Those individuals that exceeded 200 years
old were rare, and only a relatively small fraction of the fir
trees were younger than 100 years old in both aspects. At
the low elevations, however, most of the fir trees were over
100 years old, and the oldest individual was over 280 years
old in both aspects (Fig. 5).
Regeneration dynamics
At high elevations of both the north and south aspects, the
fir populations showed a unimodal regeneration pattern, and
there was a sustained regeneration of the fir trees during the
last 140 years with the highest regeneration in the 1910s in
the north aspect and in the 1900s in the south aspect, but no
fir trees established in the 18th century (Fig. 5). At the midelevations, the fir population in the south aspect demonstrated
a unimodal recruitment type and most of the fir individuals recruited from the 1860s to the 1920s, while there was a
long period of stem recruitment with two peaks during the
1810s–1870s and 1900s–1950s in the north aspect. At the low
elevations of both aspects, there had been continuous establishments of the subalpine fir trees during the 19th century
and intermittent establishments from the 1720s to the 1800s,
while no recruitment of the fir trees occurred after the 1920s.
In addition, at each decade after the 1890s, the amount of
fir trees established at the high elevations was significantly
greater than that at the low and midelevations. At each decade before the 1850s, however, the amount of fir trees established at the low and midelevations was significantly greater
than that at the high elevations in both the north and the
south aspects (Fig. 5).
The age structure distribution indicated that the occurrence
of the fir recruitment pulse became progressively later with
the increase in elevation in both aspects (Fig. 5). The regeneration dynamics reconstruction at each altitudinal site in both
aspects, however, did not include the past two to four decades
because the breast height cores were taken and the fir seedling and sapling were not cored. In addition, the density of
fir seedling and sapling (no./ha) significantly increased with
the increase in elevation, from 400 and 200 stems/ha at low
elevation to 1300 and 600 stems/ha at midelevation to 2000
and 2300 stems/ha at high elevation in the north and south
aspects, respectively (Table 3).
Discussion
Regeneration processes that shape population dynamics and
spatial patterns of plant species are highly dependent on local
environmental conditions. Interpretation of tree population
dynamics requires information on the temporal patterns of
tree establishment, often inferred from static age distributions
(Brubaker 1986; Cullen et al. 2001; Wangda and Ohsawa
2006). The age and size studies along an altitudinal gradient
would be helpful in understanding the relationship between
environmental factors and population dynamics. For example, an upsurge in tree recruitment and establishment coupled
with increase in tree density is often an indication of regeneration in response to changes in environmental and/or climatic conditions (Motta and Nola 2001; Peñuelas et al. 2007).
In this study, the survey of distribution patterns of individuals
over the range of tree sizes might represent the change in the
rate of fir tree regeneration over time across the altitudinal
range in the Shennongjia Mountains. However, care must
be taken when explaining static age structure data because
of the differences in species mortality with various age and
canopy classes and stand-history events (Johnson et al. 1994).
The lack of fir trees established before 1800 at each altitudinal site is not necessarily indicative of low recruitment during that period, but might be attributable to their maximum
life expectancy and a high tree turnover rate (the rate with
which trees die and recruit into a population) at these stands
(Phillips 1996; Phillips and Gentry 1994).
Dang et al. | Regeneration dynamics of subalpine fir forest43
Figure 5: age structures at 10-year intervals for the subalpine fir trees at different elevations in the north and south aspects of the Shennongjia
Mountains, central China. Different letters within each 10-year interval indicate the difference at P ≤ 0.05 level.
Modifications of age structure and regeneration dynamics
on various slope aspects and along steep altitudinal
gradients may result from many factors such as climatic and
environmental conditions and anthropogenic disturbance
(Brubaker 1986; Lieberman et al. 1996; Lingua et al. 2008;
Wang et al. 2004). In this study, regeneration dynamics of
the subalpine fir trees showed no significantly differences
between the north and south aspects (Fig. 5). Climatic
conditions show large spatial variation in mountainous
areas, while the microclimatology of montane landscapes is
dependent on latitude, continentality and topography (Barry
1992). In this study, the sampling location in the north aspect
44
is just adjacent to that in the south aspect within a relatively
small geographical region (Fig. 1), which might be responsible
for the similar fir regeneration dynamics in both the north
and south aspects. In addition, the relationship between size
and age was not very strong at different altitudinal sites in
both aspects (Fig. 4), as it is frequently observed in shadetolerant species (Motta and Edouard 2005), suggesting that
diameter of the A. fargesii could not be used as an appropriate
proxy of tree age.
Environmental factors such as temperature and
precipitation generally change along the altitudinal gradient
in the subalpine regions. Low temperature at high elevations
(such as upper treeline ecotones) could inhibit tree growth
and development, while low precipitation and low soil
moisture at low elevations might also restrict tree growth and
development (Block and Treter 2001). At the midelevations,
where the environmental conditions are relatively more
suitable for a tree population, the intrinsic biological traits
of the tree species rather than environmental factors would
be primarily responsible for age structure and regeneration
dynamics of the population (Hörnberg et al. 1995; Wang
et al. 2004). The expected age structure and size distribution
of long-lived tree populations growing under optimum
conditions usually demonstrate a reversed-J shape due to
the initially high mortality of juvenile trees in the smallest
size class (Peñuelas et al. 2007; Svensson and Jeglum 2001),
but limiting factors may cause variation in tree establishment
and mortality rate over time, resulting in deviation of size
and age structure from the reversed-J pattern (Block and
Treter 2001; Wang et al. 2004). In this study, fir population
at midelevations displayed a unimodal regeneration pattern
in the south aspect and a bimodal one in the north aspect,
and fir populations at low and high elevations of both
aspects showed a unimodal age distribution (Fig. 5). This age
structure is probably indicative of the strong effects of past
disturbances across the altitudinal distribution range (such
as unfavorable climate, intensive understory cover, pest and
pathogen outbreak), which caused pulses of stem recruitment
presumably corresponding to periods of high recruitment
after disturbance (Cullen et al. 2001; Peñuelas et al. 2007;
Taylor et al. 1996).
Regeneration dynamics and age structure of a plant
population could be influenced by many factors such as seed
productivity and dispersal, climatic shifts, microenvironmental
factors and man-induced disturbances (Brubaker 1986;
Davis 1986; Firm et al. 2009; Sapkota and Odén 2009). In
the Shennongjia Mountains, a great amount of fir seeds is
produced every several years (Zou et al. 2007), suggesting
that seed production has not produced important impacts
on regeneration dynamics and age structure distribution of
the subalpine fir trees. Tree establishment in the subalpine fir
forest might be controlled mainly by local microenvironmental
factors and climatic conditions, leading to years of either low
or high tree mortality (Szeicz and Macdonald 1995). In most
subalpine forests, disturbances are common and they affect
Journal of Plant Ecology
age structure and regeneration dynamics of plant population
(Firm et al. 2009; Taylor et al. 1996). Natural disturbances
drive the regeneration dynamics of most closed-canopy
forests by creating opportunities for the establishment of new
individuals through canopy opening, and a distinct pulse of
tree establishment evident in an age distribution is often an
indication of regeneration in response to canopy-opening
disturbance (Cullen et al. 2001; Parish and Antos 2004; Peng
et al. 2012; Veblen 1989). Previous study reported that in its
development history, the A. fargesii forest experienced frequent
small-scale disturbances and few large-scale disturbances
during the 19th century (Dang et al. 2009a), which might
probably lead to the sustained stem recruitment in the 19th
century at low and midelevations of both aspects (Fig. 5).
In the study region, fir tree density increased along the altitudinal gradient, and the tree density at high elevations was
significantly higher than that at low elevations (Table 2). The
mean age of the fir population decreased with the increase in
elevation in both aspects, and the fir trees at high elevations
were significantly younger than those at the low elevations
(ANOVA, P ≤ 0.05) (Table 3). A large number of stem recruitment occurred and a significant greater number of fir seedlings and saplings were also recorded during the last century at
high elevations in both aspects (Table 3 and Fig. 5). Upsurges
in tree establishment in high-elevation regions, especially
within the altitudinal treeline ecotones, have been detected in
many parts of the Northern Hemisphere with seedling invasion of subalpine meadows and recent establishment above
the current treeline (Cullen et al. 2001; Daniels and Veblen
2004; Elliott and Baker 2004; Kullman 2007). The rapid
increase in recruitment of subalpine trees in high elevations
might be attributable to climate warming over the last century
(Batllori et al. 2010; Camarero and Gutierrez 1999; Daniels
and Veblen 2004), and numerous studies have reported the
increases in recruitment and tree density in treeline environment in response to recent climate warming (Grabherr et al.
1994; Kullman 2003, 2007; Meshinev et al. 2000; Peñuelas
and Boada 2003; Peñuelas et al. 2007; Szeicz and Macdonald
1995). Temperatures in the study region tended to increase in
the past century, and the mean annual temperature and mean
annual minimum temperature showed an average increase at
a rate of 0.0275 and 0.0276°C per year during the past decades, respectively (Dang et al. 2009b). Previous study had
proved that seedling establishment of A. fargesii was primarily
controlled by temperatures in early growth season at the subalpine treeline environment in the Shennongjia Mountains
(Dang et al. 2009b). The warmer current climate might translate into better conditions for recruitment and growing of subalpine fir at its high elevations, and the positive relationship
between spring temperature and tree recruitment was widely
observed at altitudinal treelines (Camarero and Gutierrez
1999; Camarero et al. 2005; Szeicz and Macdonald 1995).
Besides the environmental conditions, biotic conditions
such as tree turnover (i.e. mortality and recruitment rates)
could have an strong effect on the regeneration patterns
Dang et al. | Regeneration dynamics of subalpine fir forest45
(Cascante-Marín et al. 2011). Some studies have illustrated
that in the tropical forests trees recruit and die twice as fast
on the richer soils than on the poorer soils and the turnover
rates have increased over the past two decades (Phillips 1996;
Phillips and Gentry 1994; Phillips et al. 2004). In this study,
although the turnover rates remain unclear due to the lack of
long-term monitoring data in the study plots, the smaller age
and dbh range of the high elevation stands might be related
to a higher stem turnover rate driven by harsher environmental conditions at the high elevations, which caused an
increased mortality and/or recruitment at the higher altitudinal stands.
The significantly smaller amount of fir seedling and sapling and relatively low recruitment of fir tree during the last
century at the low and midelevations of both aspects might
be linked to the influences of understory bamboo on successful tree seedling establishment and survival as well as recruitment into the main canopy (Campanello et al. 2007; Holz et al.
2006; Taylor and Qin 1988). Bamboos have been considered
to be one of the important factors impeding tree regeneration due to their rapid growth rate and high culm density,
as is shown by numerous studies in temperate and subtropical subalpine forests (Holz et al. 2006; Nakashizuka 1991;
Narukawa and Yamamoto 2002; Taylor et al. 1996; Wang
et al. 2006). In the Shennongjia Mountains, umbrella bamboo
(F. murielae) occurs above the elevation of 2400 m. Previous
study revealed that F. murielae dominated the understory of
the fir forest at low and midelevations (2400–2800 m) with a
coverage of 70–90% of the forest floor, and its dense coverage
negatively affected plant diversity of the subalpine fir forest in
the Shennongjia Mountains (Li et al. 2004). The small amount
of fir recruitment at the low and midelevations is likely attributable to the intensive cover of the umbrella bamboo, which
limited seedling survival and development in the last century
in the Shennongjia Mountains, and such similar findings were
reported in other subalpine forests in subtropical and temperate latitudes (Dang et al. 2010; Holz et al. 2006; Narukawa and
Yamamoto 2002; Taylor and Qin 1988). In addition, in the
context of climate warming, the potential replacement of fir
trees with more warm-loving beech trees at low elevations
(Peñuelas and Boada 2003; Peñuelas et al. 2007) might also
be related to the relatively small amount of fir regeneration in
the last century in the Shennongjia Mountains.
At high elevations, the lack of stems that recruited after
1980 in the north aspect and after 1960 in the south aspect is
partly an artifact of not coring young stems <2 m in height that
would likely occurred at the <40-year age classes (Fig. 5). As
a result, it displayed that there was an upsurge in fir recruitment in the period from 1880 to 1960 that had not sustained
in recent decades at the high altitudinal sites in both aspects.
In addition, the sustained establishment of fir seedling at
the high elevations in both aspects might promote changes
in stand structure and regeneration dynamics of the subalpine fir forest along the altitudinal gradient in the Shenongjia
Mountains, central China.
Funding
National Natural Science Foundation of China (31270011,
31130010); the Chinese Academy of Sciences (KSCX2EW-Q-16, XDA05090305); National Key Technology Research
and Development Program (2011BAD31B02).
ACKNOWLEDGEMENTS
We thank Mr Xuanbing Yuan and Shijun Li for the assistance in field
work, and Mr Xu Pang and Ms Xiuxia Chen for assistance with tree
core processing. We thank the Shennongjia National Nature Reserve
for the logistical support during the field work. We also thank the two
anonymous reviewers for their comments and suggestions.
References
Antos JA, Parish R (2002) Structure and dynamics of a nearly steadystate subalpine forest in south-central British Columbia, Canada.
Oecologia 130:126–35.
Barry RG (1992) Mountain Weather and Climate, 2nd edn. London:
Routledge.
Batllori C, Camarero JJ, Gutiérrez E (2010) Current regeneration patterns
at the tree line in the Pyrenees indicate similar recruitment processes
irrespective of the past disturbance regime. J Biogeogr 37:1938–50.
Block J, Treter U (2001) The limiting factors at the upper and lower
forest limits in the mountain-woodland steppe of Northwest
Mongolia Joachim Block and Uwe Treter. In: Kaennel Dobbertin
M, Bräker OU (eds). Proceedings of the International Conference on Tree
Rings and People. Davos, 22–6.
Brubaker LB (1986) Responses of tree populations to climatic change.
Plant Ecol 67:119–30.
Camarero JJ, Gutierrez E (1999) Structure and recent recruitment
at alpine forest-pasture ecotones in the Spanish central Pyrenees.
Ecoscience 6:451–64.
Camarero JJ, Gutiérrez E, Fortin MJ, et al. (2005) Spatial patterns
of tree recruitment in a relict population of Pinus uncinata: forest
expansion through stratified diffusion. J Biogeogr 32:1979–92.
Campanello PI, Genoveva Gatti M, Ares A, et al. (2007) Tree regeneration and microclimate in a liana and bamboo-dominated semideciduous Atlantic forest. For Ecol Manage 252:108–17.
Carrer M, Nola P, Eduard JL, et al. (2007) Regional variability of climate-growth relationships in Pinus cembra high elevation forests in
the Alps. J Ecol 95:1072–83.
Cascante-Marín A, Meza-Picado V, Estrada-Chavarría A (2011) Tree
turnover in a premontane neotropical forest (1998–2009) in Costa
Rica. Plant Ecol 212:1101–8.
Chen ZH, Wei J, Ma NF, et al. (1992) Variation characteristics of forest
fir along elevation in the Shennongjia region. Forest Fir Prevent 1:3–5.
Covington WW, Fulé PZ, Moore MM, et al. (1997) Restoration of ecosystem health in southwestern ponderosa pine forests. J Forest 95:23–9.
Cullen LE, Stewart GH, Duncan RP, et al. (2001) Disturbance and
climate warming influences on New Zealand Nothofagus tree-line
population dynamics. J Ecol 89:1061–71.
Dang H, Jiang M, Zhang Y, et al. (2009a) Dendroecological study of a
subalpine fir (Abies fargesii) forest in the Qinling Mountains, China.
Plant Ecol 201:67–75.
46
Journal of Plant Ecology
Dang H, Zhang K, Zhang Y, et al. (2009b) Tree-line dynamics in relation to climate variability in the Shennongjia Mountains, central
China. Can J For Res 39:1848–58.
Lv LX, Zhang QB (2011) Asynchronous recruitment history of Abies
spectabilis along an altitudinal gradient in the Mt. Everest region. J
Plant Ecol 5:147–56.
Dang H, Zhang Y, Zhang K, et al. (2010) Age structure and regeneration of subalpine fir (Abies fargesii) forests across an altitudinal range
in the Qinling Mountains, China. For Ecol Manage 259:547–54.
Mast JN, Fule PZ, Moore MM, et al. (1999) Restoration of presettlement age structure of an Arizona ponderosa pine forest. Ecol Appl
9:228–39.
Daniels LD, Veblen TT (2004) Spatiotemporal influences of climate on altitudinal treeline in northern Patagonia. Ecology
85:1284–96.
Meshinev T, Apostolova I, Koleva E (2000) Influence of warming on
timberline rising: a case study on Pinus peuce Griseb. in Bulgaria.
Phytocoenologia 30:431–8.
Davis MB (1986) Climatic instability, time lags and community disequilibrium. In: Diamond J, Case TJ (eds). Community Ecology. New
York: Harper & Row, 269–84.
Motta R, Edouard JL (2005) Stand structure and dynamics in a mixed
and multilayered forest in the upper Susa Valley, Piedmont, Italy.
Can J For Res 35:21–36.
Duncan R (1989) An evaluation of errors in tree age estimates based
on increment cores in Kahikatea (Dacrycarpus dacrydioides). N Z Nat
Sci 16:1–37.
Motta R, Nola P (2001) Growth trends and dynamics in sub-apine forest stands in the Varaita Valley (Piedmont, Italy) and their relationships with human activities and global change. J Veg Sci 12:219–30.
Elliott GP, Baker WL (2004) Quaking aspen (Populus tremuloides
michx.) at treeline: a century of change in the San Juan Mountains,
Colorado, USA. J Biogeogr 31:733–45.
Nakashizuka T (1991) Population dynamics of coniferous and
broad-leaved trees in a Japanese temperate mixed forest. J Veg
Sci 2:413–8.
Firm D, Nagel TA, Diaci J (2009) Disturbance history and dynamics
of an old-growth mixed species mountain forest in the Slovenian
Alps. For Ecol Manage 257:1893–901.
Narukawa Y, Yamamoto S (2002) Effects of dwarf bamboo (sasa sp.)
and forest floor microsites on conifer seedling recruitment in a
subalpine forest, Japan. For Ecol Manage 163:61–70.
Fulé PZ, Covington WW, Moore MM (1997) Determining reference
conditions for ecosystem management of southwestern ponderosa
pine forests. Ecol Appl 7:895–908.
Parish R, Antos JA. (2004) Structure and dynamics of an ancient
montane forest in coastal British Columbia. Oecologia 141:562–76.
Fyllas NM, Dimitrakopoulos PG, Troumbis AY (2008) Regeneration
dynamics of a mixed Mediterranean pine forest in the absence of
fire. For Ecol Manage 256:1552–9.
Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain
plants. Nature 369:448.
Peng Z, Zhou S, Zhang DY (2012) Dispersal and recruitment limitation contribute differently to community assembly. J Plant Ecol
5:89–96.
Peñuelas J, Boada M (2003) A global change-induced biome shift in
the Montseny Mountains (NE Spain). Global Change Biol 9:131–40.
Holz CA, Veblen TT, Franklin J (2006) Tree regeneration responses to
chusquea montana bamboo die-off in a subalpine nothofagus forest in
the southern Andes. J Veg Sci 17:19–28.
Peñuelas J, Ogaya R, Boada M, et al. (2007) Migration, invasion and
decline: changes in recruitment and forest structure in a warming-linked shift of European beech forest in Catalonia (NE Spain).
Ecography 30:829–37.
Hörnberg G, Ohlson M, Zackrisson O (1995) Stand dynamics, regeneration patterns and long-term continuity in boreal old-growth
Picea abies swamp-forests. J Veg Sci 6:291–8.
Peterson DW, Peterson DL, Ettl GJ, et al. (2002) Growth responses of
subalpine fir to climatic variability in the Pacific Northwest. Can J
For Res 32:1503–17.
Jiang XQ, Liu YH, Zhao BY (2009) Structure characteristics and spatial distribution of Abies fargesii population in Shennongjia National
Nature Reserve, China. Acta Ecol Sin 29:2211–8.
Phillips OL (1996) Long-term environmental change in tropical forests: increasing tree turnover. Environ Conserv 23:235–48.
Johnson E, Miyanishi K, Kleb H (1994) The hazards of interpretation
of static age structures as shown by stand reconstructions in a Pinus
contorta-Picea engelmannii forest. J Ecol 82:923–31.
Kullman L (2003) Recent reversal of neoglacial climate cooling trend
in the Swedish Scandes as evidenced by mountain birch tree-limit
rise. Global Planet Change 36:77–8.
Kullman L (2007) Tree line population monitoring of Pinus sylvestris in
the Swedish Scandes, 1973–2005: implications for tree line theory
and climate change ecology. J Ecol 95:41–52.
Li Z, Manfred D, Thomas B (2004) Effects of bamboo Fargesia murielae
on plant diversity in fir forest on Mountain Shennongjia. Forestry
Stud China 6:17–22.
Lieberman D, Lieberman M, Peralta R, et al. (1996) Tropical forest
structure and composition on a large-scale altitudinal gradient in
Costa Rica. J Ecol 84:137–52.
Lingua E, Cherubini P, Motta R, et al. (2008) Spatial structure
along an altitudinal gradient in the Italian central Alps suggests
competition and facilitation among coniferous species. J Veg Sci
19:425–36.
Phillips OL, Baker TR, Arroyo L, et al. (2004) Pattern and process
in Amazon tree turnover, 1976–2001. Philos Trans R Soc Lond B
359:381–407.
Phillips OL, Gentry AH (1994) Increasing turnover through time in
tropical forests. Science 263:954–8.
Sapkota IP, Odén PC (2009) Gap characteristics and their effects on
regeneration, dominance and early growth of woody species. J
Plant Ecol 2:21–9.
Svensson JS, Jeglum JK (2001) Structure and dynamics of an undisturbed old-growth norway spruce forest on the rising Bothnian
coastline. For Ecol Manage 151:67–79.
Szeicz JM, Macdonald GM (1995) Recent white spruce dynamics
at the subarctic alpine treeline of north-western Canada. J Ecol
83:873–85.
Taylor AH, Qin ZS (1988) Regeneration patterns in old-growth AbiesBetula forests in the Wolong Natural Reserve, Sichuan, China. J
Ecol 76:1204–18.
Taylor AH, Qin ZS, Jie L (1996) Structure and dynamics of subalpine
forests in the Wolong Natural Reserve, Sichuan, China. Plant Ecol
124:25–38.
Dang et al. | Regeneration dynamics of subalpine fir forest47
Veblen TT (1989) Tree regeneration responses to gaps along a transandean gradient. Ecology 70:541–3.
Wang Z (1940) The Survey Report for Shennongjia—Soil and Vegetation.
Hubei, China: Shennongjia People’s Government.
Yu Q, Xie ZQ, Xiong GM, et al. (2008) Community characteristics
and population structure of dominant species of Abies fargesii
forests in Shennongjia National Nature Reserve. Acta Ecol Sin
28:1932–41.
Wang W, Franklin SB, Ren Y, et al. (2006) Growth of bamboo Fargesia
qinlingensis and regeneration of trees in a mixed hardwood-conifer
forest in the Qinling Mountains, China. For Ecol Manage 234:107–15.
Zhang Q, Jiang M, Chen F (2007) Canopy recruitment in the beech
(Fagus engleriana) forest of Mt. Shennongjia, central China. J For
Res 12:63–7.
Wang T, Liang Y, Ren H, et al. (2004) Age structure of Picea schrenkiana forest along an altitudinal gradient in the central Tianshan
Mountains, northwestern China. For Ecol Manage 196:267–74.
Zhao CM, Chen WL, Tian ZQ, et al. (2005) Altitudinal pattern of plant
species diversity in Shennongjia Mountains, central China. J Integr
Plant Biol 47:1431–49.
Wangda P, Ohsawa M (2006) Structure and regeneration dynamics
of dominant tree species along altitudinal gradient in a dry valley
slopes of the Bhutan Himalaya. For Ecol Manage 230:136–50.
Zou L, Xie ZQ, Li QM, et al. (2007) Spatial and temporal pattern
of seed rain of Abies fargesii in Shennongjia Nature Reserve,
Hubei. Biodiversity Sci 15:500–9.