Journal of Plant Ecology Advance Access published January 23, 2014

Journal of
Plant Ecology Contrasting responses of net
PAGES 1–12

doi:10.1093/jpe/rtt066 primary productivity to inter-annual

variability and changes of climate
available online at
www.jpe.oxfordjournals.org

among three forest types in northern

China
Shuai Ouyang1,2, Xiangping Wang1, Yulian Wu1 and
Osbert Jianxin Sun1,2,*

Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014

1
Ministry of Education, Key Laboratory for Silviculture and Conservation, College of Forest Science, Beijing Forestry
University, 35 Qinghua East Road, Haidian, Beijing 100083, China
2
Institute of Forestry and Climate Change Research, Beijing Forestry University, 35 Qinghua East Road, Haidian, Beijing
100083, China
*Correspondence address. Ministry of Education Key Laboratory for Silviculture and Conservation, College
of Forest Science, Beijing Forestry University, 35 Qinghua East Road, Haidian District, Beijing 100083, China.
Tel: +86-10-6233-7095; E-mail: sunjianx@bjfu.edu.cn

Abstract

Aims inter-annual growth variations reflected by tree-ring width index

A lack of explicit information on differential controls on net primary (RWI) at the study sites.
productivity (NPP) across regions and ecosystem types is largely
Important Findings
responsible for uncertainties in global trajectories of terrestrial
Inter-annual variations in modeled NPP during the period 1960–06
carbon balance with changing environment. The objectives of this
were mostly consistent with the temporal patterns in RWI. There were
study were to determine how NPP of different forest types would
contrasting responses of modeled NPP among the three forest types to
respond to inter-annual variability of climate and to examine the
inter-annual variability of the present climate as well as to predicted
responses of NPP to future climate change scenarios across con-
changes in future climate. The modeled NPP was positively related to
trasting forest types in northern China.
annual mean air temperature in the L. gmelinii forest (P < 0.001), but
negatively in the P. tabulaeformis forest (P = 0.05) and the Q. wutais-
Methods
hanica forest (P  =  0.03), while the relationships of modeled NPP
We investigated inter-annual variations of NPP in relation to climate
with annual precipitation for the three forest types were all positive.
variability across three forest types in northern China, including a
Multiple stepwise regression analyses showed that temperature was a
boreal forest dominated by Larix gmelinii Rupr., and two temper-
more important constraint of NPP than precipitation in the L. gmeli-
ate forests dominated by Pinus tabulaeformis Carr. and Quercus
nii forest, whereas precipitation appeared to be a prominent factor
wutaishanica Mayr., respectively, and studied the responses of NPP
limiting the growth in P. tabulaeformis and Q. wutaishanica. Model
in these forests to predicted changes in climate for the periods
simulations suggest marked, but differential increases in NPP across
2011–40, 2041–70 and 2070–100 under carbon emission scenar-
the three forest types with predicted changes in future climate.
ios A2 and B2 of Intergovernmental Panel on Climate Change. We
simulated the responses of NPP to predicted changes in future cli-
Keywords: biome-BGC, climate change, forest type, NPP,
mate as well as inter-annual variability of the present climate with
simulations, tree-ring width index (RWI)
the Biome-BGC version 4.2 based on site- and species-specific
parameters. The modeled forest NPP data were validated against Received: 25 September 2013, Revised: 13 December 2013,
values in literature for similar types of forests and compared with Accepted: 18 December 2013

© The Author 2014. 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: journals.permissions@oup.com
Page 2 of 12
Introduction
With a continuously rising concentration of atmospheric
greenhouse gases, an increase in mean annual air tempera-
ture of 4–5°C is predicted to occur by the end of the 21st cen-
tury (Christensen et al. 2007; IPCC 2007). In China, the mean
annual air temperature increased at an average rate of 0.6°C/
decade over the past two decades (Piao et al. 2011), which was
far greater than the global average of ~0.27°C/decade (IPCC
2007). Associated with this warming, significant changes in
seasonal precipitation were also observed (Piao et  al. 2005).
Recent changes in climate have been particularly evident in
northern China (Ren et al. 2008, 2012).
Forests are considered to play an important role in global
carbon balance because they account for up to 80% of the total
aboveground carbon and some 40% of belowground carbon
in the entire terrestrial ecosystems (Dixon et al. 1994). A per-
sistent warming and changes in climate can lead to unprec-
edented changes in forest growth and productivity (Myneni
et al. 2001; Nemani et al. 2003; Piao et al. 2007; Tan et al. 2007),
enhancing or weakening the forest carbon sinks. However,
assessment of regional and global forest carbon balance under
changing climate can be complicated by differential responses
of forest productivity to climate variability across stand types
and geographical locations (Law et  al. 2004; Lindner et  al.
2010; Sun et al. 2004). Therefore, a better understanding on
the local controls and constraints of forest response to climate
variability is vital when efforts are made for reducing uncer-
tainties in assessment of the regional carbon budget and forest
feedbacks to global climate change.
Net primary productivity (NPP) is a central component of
ecosystem carbon cycle and a primary indicator of ecosys-
tem functioning. Direct field measurements often provide
most accurate estimate of forest NPP at stand level, but the
operation is more costly and time consuming with increasing
spatial and temporal coverage (Clark et al. 2001; Gower et al.
2001; Houghton 2005). Ground NPP estimates based on forest
growth data from permanent sampling plots or forest inven-
tory analysis typically rely on measurements taken at inter-
vals ranging from 5 to 10 years; the resultant increment data
provide mean values for specified time periods while neglect-
ing the inter-annual variations in NPP due to climate fluctua-
tions (Churkina et al. 2003; Hasenauer et al. 2012; Houghton
2005). For identification of the climatic controls on temporal
dynamics of forest NPP, explicit information on the responses
of tree growth and stand dynamics to inter-annual variabil-
ity of climate and other environmental conditions is critical
(Bousquet et  al. 2003; Cao et  al. 2003; Keenan et  al. 2012).
Process-based modeling provides a mean of integrating data
collected across a spectrum of spatial and temporal scales for
studying the regional carbon balance and assessing potential
changes in ecosystem carbon dynamics with changing envi-
ronment (Law et al. 2003, 2004).
Process-based models have inherent advantages in pre-
dicting how future climate change may influence forest
Journal of Plant Ecology
NPP compared with field-based approaches (Melillo et  al.
1993; Morales et  al. 2005; Scurlock et  al. 2002; Wang et  al.
2012). Several models have been used to assess forest NPP
and responses to climate change in China (Cao et al. 2003;
Fang et  al. 2003; Gao and Zhang 1997; Jiang et  al. 1999;
Peng et al. 2009; Wang et al. 2005; Xiao et al. 1998; Zhu et al.
2007). Most of them use meteorological data and remote-
sensing products of vegetation as model inputs with mini-
mum parameterization of the models and only a few have
examined temporal dynamics of forest NPP on an annual
basis (Cao et al. 2003; Fang et al. 2003; Piao et al. 2005). The
inter-annual variations and long-term trend of NPP have
not been comprehensively assessed or reported for forests in
northern China.
Determination of the accuracy and validation of model
predictions are important steps in modeling ecosystem car-
bon cycle and understanding critical drivers of regional NPP
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
under changing environment. Availability of long-term data
on tree growth and forest productivity is a prerequisite for
model validation (Tao et  al. 2005; Turner et  al. 2005). Tree-
ring chronologies provide long-term records of ad hoc tree
growth under natural conditions and, therefore, can be used
as indicators of NPP for evaluations of the impacts of climate
change and atmospheric CO2 enrichment on forest produc-
tivity (Rathgeber et  al. 2000, 2003). Tree-ring width index
(RWI) has been proven to be an effective indicator of forest
NPP because tree radial increment is proportional to annual
NPP for a wide variety of forest types (Graumlich et al. 1989;
Krakauer and Randerson 2003; Rathgeber et al. 2000, 2003).
RWI provides a robust testing of model simulations of inter-
annual variations in forest NPP.
In this study, by using the ecosystem process model Biome-
BGC (BioGeochemical Cycles) with site- and/or species-
specific parameters, we investigated inter-annual variability
of NPP under present climate, and simulated responses of
NPP to predicted changes of future climate and increasing
atmospheric CO2, in three representative forest types (Larix
gmelinii Rupr., P. tabulaeformis Carr. and Quercus wutaishanica
Mayr. [aka. Q. liaotungensis Koidz.]) across two climate zones
in northern China. The objectives of this study were (i) to
determine how NPP of different forest types would respond to
inter-annual variability of climate and (ii) to examine the dif-
ferential responses of NPP to future climate change scenarios
across the three contrasting forest types in northern China.
Materials And Methods
Study sites
The study was located at two forest sites: one in the Genhe
Nature Reserve on the northwest slope of Daxing’anling moun-
tains (Genhe site), Inner Mongolia (latitude 50°49ʹ–50°51ʹN;
longitude 121°30ʹ–121°31ʹE; elevation 784–1142 m a.s.l.)
and the other in the Mt Linkong of the Taiyue mountains
(Taiyue site), Shanxi province (latitude 36°31ʹ–43ʹN; longi-
tude 121°01ʹ–121°15ʹE; elevation 1542–1734 m a.s.l.).
Ouyang et al.     |     Forest NPP response to variability and change in climate
The Genhe site is situated in the boreal region of north-
eastern China. Annual mean air temperature at the site is
about –5.4°C and annual precipitation fluctuates between
450 and 550 mm, of which 85–90% falls during the grow-
ing season (Gower et  al. 2001). Soils are of dark brown
earth (i.e. Cryumbreps in the US soil classification system or
Humiccambisols in the UN–FAO soil classification system)
developed on bedrocks of granite and basalt. Continuous or
discontinuous permafrost is commonly found in the region,
which reaches down to 3 m below the ground surface and
lasts for 8  months each year. The dominant forest tree spe-
cies in the Genhe area is L. gmelinii, often forming communi-
ties with Ledum palustre or Rhododendron dahuria as dominant
companion shrubs in the understory and thick Sphagnum
layer on forest floor.
The Taiyue site has a warm-temperate and continental
monsoon climate with an annual mean air temperature of
8°C. Annual precipitation varies from 600 to 650 mm, occur-
ring mostly during summer months (Yi et al. 2008). The soil is
identified as Cinnamon, which matches the alfisol type in the
US soil classification system. The dominant tree species are
evergreen needleleaf P.  tabuliformis and deciduous broadleaf
Q.  wutaishanica, which occur widely in northern China (Yu
and Sun 2013). Shrubs are represented by Lespedeza bicolor
Turcz. and Spiraea salicifolia, occurring mostly in the open or
on forest edge.
Establishment of stand chronologies
Tree-ring chronologies were developed for the three forest
types by using increment coring method and used for deter-
mination of inter-annual variations in tree growth.
Increment cores were collected from previously established
plots for the three forest types at the two study sites, includ-
ing three plots for the L. gmelinii forest at the Genhe site, and
four plots for the P. tabulaeformis forest and three plots for the
Q.  wutaishanica forest, respectively, at the Taiyue site. Plots
at the Genhe site, each of the dimension 20 × 50 m, repre-
sented the three most common forest community types of the
region, namely L. gmelinii–R. dahuria community, L. gmelinii–
L.  palustre community and L.  gmelinii–L.  palustre–Sphagnum
community. The plots at the Taiyue site are representatives of
pure P. tabulaeformis and Q. wutaishanica stands, and were laid-
out in the regular dimension of 20 × 20 m each.
On each plot, increment cores were collected from pre-
designated sampling trees at breast height (130 cm above
ground) with a Presler increment borer. Altogether, the trees
sampled for increment cores consisted of 30 individuals for
L. gmelinii, 82 individuals for P. tabulaeformis and 65 individu-
als for Q. wutaishanica, which were randomly selected across
age classes >50  years. The cores were mounted on grooved
boards under a layer of wood glue, air dried and then sanded
with successively finer grades of sandpaper until all rings
became easily identifiable. The ring widths were measured
with a linear digitizing tablet coupled to a computer at a res-
olution of 0.001 mm. Dating and measurement errors were
Page 3 of 12
further checked and identified by using the computer pro-
gram COFECHA of Holmes (1983). Cores with apparent miss-
ing rings or severe distortion were excluded from the analysis.
After standardizing each chronology, all tree-RWI were aver-
aged to generate a standard chronology for each tree species
by using the program ARSTAN (Cook and Holmes 1986).
Several descriptive statistics commonly adopted in dendro-
chronology were used to assess the quality of the standard
chronologies, including the mean sensitivity (MS) and stand-
ard deviation (SD) for assessing the high-frequency varia-
tions (Fritts 1976), and the express population signal (EPS)
for expressing the confidence of the site chronologies (Briffa
and Jones 1990). EPS is a measure to express the common
signal in a time series; a value of 0.85 or higher is commonly
considered as acceptable (Wigley et al. 1984).
Model description and parameterization
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
We used the version 4.2 of Biome-BGC model (http://
www.ntsg.umt.edu/project/Biome–BGC) developed by the
Numerical Terradynamic Simulation Group at the University
of Montana, USA, to simulate the forest NPP under present
climate and predicted changes in future climate of the study
areas. The model simulates the mass-balanced dynamics of
carbon, nitrogen, water and energy in forest and non-forest
terrestrial ecosystem ranging from individual plots to global
scale (Churkina et  al. 2003; Luo et  al. 2010; Running and
Coughlan 1988; Thornton et  al. 2002; White et  al. 2000). It
runs on a daily time-step with the input data of daily mete-
orological records and information on the general environ-
ment and the ecophysiological traits of the vegetation to be
simulated.
The Biome-BGC was provided with default parameter sets
of ecophysiological characteristics for the major biome types,
such as evergreen needleleaf forest, deciduous needleleaf for-
est and deciduous broadleaf forest (White et al. 2000). In this
study, the model was parameterized with site- and/or species-
specific information compiled for this study by conducting
literature survey. Average values were used if multiple data
sources were found for the same attributes. If the species-
specific data on some of the parameters were not found from
literature, the default values of deciduous needleleaf forest
were used as representation of L. gmelinii, the default values
of evergreen needleleaf forest as representation of P. tabulae-
formis and the default values of deciduous broadleaf forest as
representation of Q. wutaishanica, respectively. The ecophysi-
ological parameters for simulations of NPP of the three forest
types are listed in Supplementary Tables A1–A3.
Meteorological data
Daily records of maximum and minimum temperatures
and precipitation for the period 1960–2006 were obtained
from the China Meteorological Data Sharing Service System
(CMDSSS; http://cdc.cma.gov.cn). The missing daily data for
vapor pressure deficit, incident shortwave radiation and day-
time solar irradiance were generated using the microclimate
Page 4 of 12
simulator MT–CLIM version 4.3 (http://www.ntsg.umt.edu/
project/mtclim), corrected for differences in slope, aspect
and elevation between the base meteorological station and
the study site (Thornton and Running 1999; Thornton et al.
2000).
Values of the annual mean air temperature and annual
precipitation were directly derived from the daily meteoro-
logical observations archived in the database of CMDSSS. The
annual evapotranspiration was computed based on mete-
orological and vegetation data using the Penman–Monteith
equation (Monteith 1973).
Modeling procedures
The model simulations were comprised of two phases: the
self-initialization, or spin-up simulation, and the normal
simulation. Biome-BGC is a mechanistic biogeochemical
model; the endpoint of any given simulation depends on
the starting values of state and flux variables, or simply on
initial conditions (Ruelle 1978), as commonly required in
ecosystem models (Thornton and Rosenbloom 2005). In the
absence of information for the initialization of the state vari-
ables, model simulations are required for the spin-up run
based on standard procedures (White et al. 2000). Using pre-
industrial carbon dioxide concentration of 294.842  p.p.m.,
approximating the level at the end of the nineteenth cen-
tury and for the nitrogen deposition levels at 0.0001 kg N
m2 year−1 (Holland et  al. 1999), we performed the spin-up
procedure until reaching a steady state among climate,
vegetation, ecophysiological traits, soil organic matter and
nutrient pools (Thornton et  al. 2002). The endpoint of the
spin-up run was used as the initial conditions for the nor-
mal model simulations performed for a 47-year time period,
from 1960 to 2006, with historical daily metrological data
and the ambient CO2 concentration.
Future climate and CO2 scenarios
Global temperature increase is predicted to be greatest in
the northern mid- and high-latitude regions (IPCC 2007).
This general pattern of climate change also applies to China
(Ding et  al. 2006). To develop future trajectories of global
climate change, the Intergovernmental Panel on Climate
Table 1:  predicted changes in annual mean air temperature and annual precipitation under the climate change scenarios SRES A2 and B2
of IPCC (2000) for the periods 2011–40, 2041–70 and 2071–100 against the reference period 1961–90 and the corresponding atmospheric
CO2 concentrations used in the simulation
A2
Study sites Period Temperature (°C) Precipitation (%) CO2 (p.p.m.)
Genhe 2011–40 +1.7 +1 386–481
2041–70 +3.8 +5
2071–100 +6.1 +13
Taiyue 2011–40 +1.6 –1 386–481
2041–70 +3.2 +2
2071–100 +5.3 +11
Journal of Plant Ecology
Change (IPCC) outlined four carbon emissions scenarios,
designated as A1, A2, B1 and B2, based on distinct direc-
tions for global development through the year 2100 (IPCC
2000). The scenarios A2 and B2 are generally adopted in
the China’s National Assessment Report on Climate Change
(ECNARCC 2007) and were used for evaluation in this
study. A2 describes a world with increased population
growth, slow economic development and slow technologi-
cal change, whereas B2 reflects a scenario with an inter-
mediate population and economic growth, addressing local
solutions to economic, social and environmental sustain-
ability (IPCC 2000).
We used predicted changes in air temperature and precipi-
tation in the China’s National Assessment Report on Climate
Change (ECNARCC 2007) for the periods 2011–40, 2041–70
and 2071–100, against the reference period 1961–90 for the
three forest types (Table  1). The CO2 concentrations of the
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
three time periods were set to values estimated using the Bern
carbon model based on the IPCC carbon emissions scenarios
A2 and B2 (Joos et  al. 2001). We performed simulations to
examine the sensitivity of each forest type to future climate
change and rising CO2 concentrations.
Statistical analysis
Relationships between the modeled NPP and tree-RWI were
examined with linear regression analyses. The relationships
between the modeled NPP and the selective climatic vari-
ables (i.e. temperature and precipitation) were examined with
both the linear regression analyses for single-factor effect and
the multiple stepwise regressions for the interactive effects
between precipitation and temperature. All data analyses were
performed with R3.0.1 software (R Development Core Team
2009).
Results
Historical climate analysis of the study sites
During the period 1960–2006, the annual mean air tem-
perature significantly increased at an average rate of 0.07°C
a−1 (P  <  0.001) with relatively large inter-annual variations
B2
Temperature (°C) Precipitation (%) CO2 (p.p.m.)
+2.1 +3 386–490
~620 +3.4 +8 ~524
~836 +4.5 +12 ~611
+1.8 +2 386–490
~620 +2.9 +4 ~524
~836 +3.8 +10 ~611
Ouyang et al.     |     Forest NPP response to variability and change in climate Page 5 of 12

A Table 2:  general descriptive statistics of the standard tree-ring

10
chronologies for the three forest types
8
Trees Chronology
Annual mean air temperature ( C)

y = -23.44 + 0.02x
6 Forest types sampled time span MS SD EPS
o

R 2 = 0.21
4 P < 0.001
Larix gmelinii forest 30 1743–2009 0.17 0.22 0.95
Genhe site Pinus tabulaeformis forest 69 1895–2010 0.27 0.31 0.98
2
Taiyue site Quercus wutaishanica forest 54 1904–2010 0.25 0.24 0.97
0

-2
Biome-BGC simulations of NPP and comparison
-4
y = -142.47 + 0.07x with RWI
-6 R 2 = 0.60 Among the three forest types, the L.  gmelinii forest had the
P < 0.001
-8 lowest values of modeled NPP with more constrained inter-
B annual variability (CV = 10.8%), ranging from 280 to 496 g
1200 C m−2 a−1, whereas the Q. wutaishanica forest had the highest
values of modeled NPP with intermediate inter-annual vari-
ability (CV  =  17.8%), ranging from 334 to 848 g C m−2 a−1

Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014

1000
Annual precipitation (mm)

(Fig.  2A). The P.  tabulaeformis forest ranked intermediate in

800
600
400
200
1960 1970
Figure  1: temporal variation in (A) annual mean air temperature
and (B) annual precipitation during the period 1960–2006 for the
two study sites in northern China.
(coefficient of variation [CV]  =  30.1%) at the Genhe site
and at 0.02°C a−1 (P = 0.001) with a relatively narrow range
of inter-annual variations (CV  =  5.8%) at the Taiyue site
(Fig. 1A). The annual precipitation was moderately variable
inter-annually (CV  =  17.7%) without displaying apparent
trend of change at the Genhe site, while it declined marginally
(P = 0.06) with large inter-annual variations (CV = 23.6%) at
the Taiyue site (Fig. 1B).
Tree-ring chronologies and associated descriptive
statistics
Among the three forest types, the L.  gmelinii forest had the
longest chronology and was lowest in the MS, SD and EPS,
whereas the P. tabulaeformis forest was highest in the MS, SD
and EPS (Table 2). The values of EPS of the chronologies for
all three forest types exceeded the recommended threshold
of 0.85; hence, the chronologies were judged to be suitable
for use in evaluating the impacts of climate change variability
and rising atmospheric CO2 concentration on forest produc-
tivity (Table 2).
the modeled NPP with the greatest inter-annual variations
(CV = 18.8%), ranging from 235 to 710 g C m−2 a−1 (Fig. 2A).
The mean values of modeled NPP for the period 1960–2006
based on the Biome-BGC simulations are in general agree-
ment with those reported in literature for the same area or
other similar forest types in China and worldwide (Tables
3–5).
The inter-annual variability in modeled NPP closely
matched the inter-annual variability in RWI for the three for-
1980 1990 2000 2010 est types (Fig.  2A; CV  =  10.8% vs. 10.4% in L. gmelinii for-
Year est, 18.8% vs. 19.6% in P. tabulaeformis forest and 17.8% vs.
17.4% in Q. wutaishanica forest, respectively). However, sig-
nificant relationships between modeled NPP and RWI were
only found in the two forest types at the Taiyue site, namely
the P. tabulaeformis forest (P  <  0.05) and the Q. wutaishanica
(P < 0.001) forest (Fig. 2B).
Climatic constraints of NPP under present
conditions
The modeled NPP based on the present climate was signifi-
cantly (P < 0.05) related to both annual mean air tempera-
ture and annual precipitation. However, the relationships
differed among the three forest types as well as between the
two study sites. The modeled NPP was positively and closely
related to annual mean air temperature in the L.  gmelinii
forest, but negatively in the P.  tabulaeformis forest and the
Q.  wutaishanica forest (Fig.  3). The relationships of mod-
eled NPP with annual precipitation for the three forest types
were all positive (Fig. 3). Among the three forest types, the
Q.  wutaishanica forest responded most strongly in modeled
NPP to both annual mean air temperature and annual pre-
cipitation, whereas the L. gmelinii forest responded the least
to both climatic variables (Fig. 3). Multiple stepwise regres-
sion analyses showed that temperature was a more impor-
tant constraint of NPP than precipitation in the L.  gmelinii
forest, whereas precipitation appeared to be a prominent
Page 6 of 12 Journal of Plant Ecology

A B
1000 1.6 1000
Larix gmelini Modeled NPP Larix gmelini
RWI 1.4
800 800
1.2

1.0 600
600
0.8
400 0.6 400

0.4
200 200

1000 1.6 1000

Pinus tabuliformis

Modeled NPP (g C m2 yr-1 )

Modeled NPP (g C m2 yr-1 )

Pinus tabuliformis
1.4 y = 346.2 + 165.55x
800 800 R2 = 0.12
1.2 P = 0.02

RWI
1.0 600
600
0.8

Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014

400 0.6 400

0.4
200 200

1000 1.6 1000

Quercs liaotungensis Quercs liaotungensis
1.4 y = 359.0 +291.55x
800 800 R 2 = 0.21
1.2 P = 0.001
1.0
600 600
0.8
400 0.6 400

0.4
200 200
1960 1970 1980 1990 2000 2010 0.4 0.6 0.8 1.0 1.2 1.4 1.6
Year RWI

Figure 2:  comparison of modeled NPP with RWI in the three forest types of northern China for the period 1960–2006. (A) Time series of mod-
eled NPP and RWI; (B) relationships between modeled NPP and RWI.

factor limiting the growth in P.  tabulaeformis and Q.  wutais-
hanica (Table 6).
Responses of NPP to predicted climate change
Future climate changes were predicted to substantially
increase NPP for all the three forest types (Table 7). The mag-
nitude of changes, however, appeared to vary over different
time periods and with forest types and climate change scenar-
ios. Under the projected climatic and atmospheric CO2 condi-
tions of SRES A2, the two needleleaf forests would increase
NPP by more than 40% over the period 2071–100 against
the reference period 1961–90, whereas only half of the NPP
increase would be expected in the Q.  wutaishanica forest as
compared with the other two forest types. Between the two
needleleaf forest types, the L. gmelinii forest was predicted to
have a much greater initial response in NPP to future changes
in climate than the P. tabulaeformis forest (Table 7). However,
with time the difference in the response of NPP between the
two forest types would diminish. In contrast, the two temper-
ate forest types started with similar responses in NPP to future
changes in climate but continued with much diverged tempo-
ral patterns (Table 7).
The model simulations produced similar values of the
relative change in NPP over the period 2071–100 against
the reference period 1961–90 among the three forest types
under the climatic and atmospheric CO2 conditions of SRES
B2 (Table 7). However, the temporal patterns of the relative
change in NPP are differentiated between the two study sites;
the L. gmelinii forest at the Genhe site was predicted to have
greater initial response to the future climate change under
SRES B2 than other two forest types (Table 7).
Discussion
Forest responses to climate change are determined to a
large extent by the susceptibility of tree growth to temporal
Ouyang et al.     |     Forest NPP response to variability and change in climate Page 7 of 12

Table 3:  summary of NPP values from various studies for boreal or deciduous coniferous forests

Forest type Location NPPa (g C m−2 a−1) Method of estimation Reference

Larix gmelinii Genhe 424b Biome-BGC simulations This study

Larix gmelinii Genhe 425 Field measurements Feng and Yang (1985)
Larix gmelinii Genhe 448 (417–478)c Field measurements Liu et al. (1994)
Larix gmelinii Daxing’anling 437 (389–490) Field measurements Shi et al. (2002)
Larix spp Boreal forest, China 516 (189–868) Field measurements Ni et al. (2001)
Boreal forest China 181–780 Field measurements Jiang et al. (1999)
Deciduous coniferous forest Eastern China 419 Field measurements Li et al. (2011)
Deciduous coniferous forest China 432 CASA simulations Piao et al. (2001)
Deciduous coniferous forest Northeast China 451 GLOPEM–CEVSA simulations Zhao et al. (2011)
Larix gmelinii forest Daxin’anling 510 Remote sensing Jiang et al. (1999)
Larix spp Northern China 447 (152–626) Remote sensing Zhu et al. (2007)
Boreal forest Siberian 314–445 Field measurements Jarvis et al. (2001)
Boreal forest Worldwide 424 Field measurements Gower et al.(2001)
Deciduous coniferous forest Worldwide 400 (200–1000) MIAMI simulations Lieth (1975)

Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014

a
Data on biomass in the original literature were all converted to carbon stock assuming the conversion factor of 0.5 for wood, foliage and roots.
Values in parentheses indicate the range of variation in NPP.
b
The modeled NPP in this study is an average for the period 1960–2006.
c
The study provided only the aboveground NPP, which was converted to the total NPP using the ratio of shoot NPP to root NPP reported in Feng
and Yang (1985).

Table 4:  summary of NPP values from various studies for evergreen coniferous forests

Forest type Location NPPa (g C m−2 a−1) Method of estimation Reference

b
Pinus tabulaeformis forest Taiyue 515 Biome-BGC simulations This study
Pinus tabulaeformis forest Taiyue 490 Field measurements Zhai et al. (1992)
Pinus tabulaeformis forest northern China 589 Field measurements Fang et al. (2006)
Temperate evergreen coniferous forest China 635 Remote sensing Jiang et al. (1999)
Temperate evergreen coniferous forest Northeast China 470 GLOPEM–CEVSA simulations Zhao et al.(2011)
Evergreen coniferous forest China 179–806 Field measurements Zhu et al. (2007)
Temperate evergreen coniferous forest China 625 Field measurements Jiang et al. (1999)

a
Data on biomass in the original literature were all converted to carbon stock assuming the conversion factor of 0.5 for wood, foliage and roots.
Values in parentheses indicate the range of variation in NPP.
b
The modeled NPP in this study is an average for the period 1960–2006.

Table 5:  summary of NPP values from various studies for deciduous broadleaved forests

Forest type Location NPPa (g C m−2 a−1) Method of estimation Reference

Quercus wutaishanica forest Taiyue 645b Biome-BGC simulations This study

Quercus wutaishanica forest Northern China 349–1364 Field measurements Jiang (1997)
Quercus wutaishanica forest Northern China 700 LPJ–GUESS simulations Liu et al. (2009)
Deciduous broadleaved forest Northern China 638 GLOPEM–CEVSA simulations Zhao et al. (2011)
Deciduous broadleaved forest China 663 Remote sensing Zhu et al. (2007)
Temperate deciduous forest China 715 (502–1036) TEM simulations Xiao et al. (1998)
Temperate deciduous forest World 620 (81–978) TEM simulations Melillo et al. (1993)

a
Data on biomass in the original literature were all converted to carbon stock assuming the conversion factor of 0.5 for wood, foliage and roots.
Values in parentheses indicate the range of variation in NPP.
b
The modeled NPP for each forest type is an average for the period 1960–2006.
Page 8 of 12 Journal of Plant Ecology

Larix gmelini Table 6:  summary of multiple stepwise regressions of modeled

1000 NPP with precipitation and temperature
y = 339 + 0.20x y = 501.6 + 19.9x
R 2 = 0.11 R2 = 0.27
800 P = 0.02 Forest type Variable Estimate Standard error t-value P
P < 0.001
Larix gmelinii (Intercept) 420.494 36.88 11.402 0.000
600
Precipitation 0.183 0.07 2.559 0.014
Temperature 18.618 4.43 4.201 0.000
400
R2 0.36

200 F-value 12.57

200 300 400 500 600 700 -8 -6 -4 -2 0 P <0.001
Pinus tabuliformis Pinus tabulaeformis (Intercept) 219.612 43.86 5.007 0.000
1000
Modeled NPP (g C m 2 yr -1 )

y = 219.6 + 0.45x y = 999.1 - 59.4x Precipitation 0.438 0.06 6.905 0.000

2
R = 0.52 R2 = 0.08 R2 0.52
800 P < 0.001 P = 0.05
F-value 12.57
600 P <0.001
Quercus wutaishanica (Intercept) 262.022 43.27 6.055 0.000
400 Precipitation 0.569 0.06 9.09 0.000

Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014

200
200 400 600 800 1000 1200 6
Quercus liaotungensis
1000
y = 262 + 0.57x
R 2 = 0.65
800 P < 0.001
600
400
200
200 400 600 800 1000 1200 6
Annual precipitation (mm)
Figure  3: relationships of modeled NPP with annual precipitation
and annual mean air temperature in the three forest types of north-
ern China for the period 1960–2006.
fluctuations in climatic conditions. Different forest types may
vary in the patterns of inter-annual variability in productiv-
ity owing to differential responses to climatic signals (Law
et al. 2004). Simulations of inter-annual variability of terres-
trial ecosystem carbon cycle has, therefore, imposed a chal-
lenge for most biogeochemical models (Keenan et  al. 2012;
Mahecha et al. 2010). In this study, based on simulations with
the Biome-BGC model parameterized with species- and site-
specific information and validated with tree-ring chronolo-
gies, we found contrasting responses of NPP among three
forest types typical of northern China to inter-annual climate
variations as well as to predicted changes in future climate
under the carbon emission scenarios A2 and B2 of IPCC
(2000). Among the three forest types, the L.  gmelinii forest
represents a typical boreal forest in the northeastern China,
whereas both P. tabulaeformis and Q. wutaishanica forests nat-
urally occur under temperate climate over a large range in
central and northern China (Yu and Sun 2013). Our results
R2 0.65
F-value 82.62
7 8 9 10
P <0.001
y = 1269.07 - 76.45x
R 2 = 0.10
P = 0.03 showed that the modeled NPP was positively related to annual
mean air temperature in the L. gmelinii forest, but negatively
in the P. tabulaeformis forest and the Q. wutaishanica forest. The
relationships of modeled NPP with annual precipitation for
the three forest types were all positive but the linear fitting
was much stronger for the two forest types of temperate cli-
7 8 9 10 mate than the boreal L. gmelinii forest. Model simulations also
Mean annual air temperature (oC) suggest marked, but differential increases in NPP across the
three forest types in response to predicted changes of climate
in northern China.
The average values of NPP for the three forest types based
on our simulations with present climate are in agreement
with values reported in literature for similar forest types in
China and worldwide (Tables 3–5). In absence of long-term
field data on NPP in our study, we used tree-ring chronolo-
gies to reflect temporal variations in forest productivity. The
established chronologies were examined for quality concern-
ing their correlations with climate signals using descriptive
statistics MS, SD and EPS, all with satisfactory performance as
judged by commonly accepted criteria (Briffa and Jones 1990;
Fritts 1976; Wigley et al. 1984; Wu 1990). The chronologies for
all three forest types had relatively high values in MS, SD and
EPS (Table 2), confirming their qualifications for use in study-
ing the correlation between tree growth and climatic factors.
RWI has been found to correlate well with NPP (Graumlich
et  al. 1989; Krakauer and Randerson 2003; Rathgeber et  al.
2000). In this study, however, we found significant relation-
ships of the modeled NPP with RWI only in the two forest
types of temperate climate; there was no clear relationship
between the modeled NPP and RWI in the boreal L. gmelinii
forest. Similar problem has been found in the study of Su
et al. (2007) with a Picea schrenkiana forest under cold climate.
Ouyang et al.     |     Forest NPP response to variability and change in climate
Table 7:  predicted NPP for the periods 2011–40, 2041–70 and 2070–100 under the IPCC (2000) climate change scenarios SRES A2 and
B2 for the three forest types in northern China, based on simulations with Biome-BGC version 4.2, and the relative changes in NPP
against the reference period 1961–90
Larix gmelinii forest
Climate scenario Period NPP (g C m−2 a−1) Change (%)
SRES A2 1961–90 416 — 515
2011–40 474 +14.1
2041–70 539 +29.7
2071–100 606 +45.7
SRES B2 1961–90 416 — 515
2011–40 487 +17.2
2041–70 528 +27.0
2071–100 562 +35.5
There were large mismatches between the modeled NPP and
RWI series in the L.  gmelinii forest for the periods 1965–68
and 1999–2002, which coincided with two major drought
events in northeastern China (Xiao et al. 2009). The extreme
weather conditions of the two periods could have resulted in
modifications of the permafrost, imposing indirect effects on
tree growth via edaphic processes. However, the Biome-BGC
version 4.2 used in this study does not incorporate the precise
coupling between the permafrost dynamics and biogeochemi-
cal cycle. In fact, most process-based models focus mainly on
the general descriptions of fundamental physiological and
biogeochemical processes; they may lack predictive capabili-
ties during extreme weather conditions (Vetter et  al. 2008).
Therefore, our simulations were constrained for taking into
consideration of the impacts of climate variability on forest
productivity through modification of belowground processes.
Ni et al. (2001) showed that the NPP of Chinese forests is
highly correlated with both annual mean air temperature and
precipitation. There are also studies suggesting a stronger con-
trol of precipitation than temperature on forest NPP in China
(e.g. Piao et al. 2001; Cao et al. 2003). In this study, however,
we show that temperature was a more important constraint
of NPP than precipitation in the L.  gmelinii forest, whereas
precipitation appeared to be a prominent factor limiting the
growth in P.  tabulaeformis and Q.  wutaishanica. Contrasting
responses of NPP to annual mean air temperature were found
between the boreal L. gmelinii forest and other two temper-
ature forest types. The modeled NPP was positively related
to annual mean air temperature in the L. gmelinii forest, but
negatively in the P. tabulaeformis and Q. wutaishanica forests.
Our results further demonstrate the complex interactions
between climate change and forest responses (Churkina et al.
1999; Shaw et al. 2002).
Marked increases in NPP across the three forest types were
predicted to occur in response to predicted changes in climate
and atmospheric CO2 through this century under both the
carbon emissions scenarios SRES A2 and B2 of IPCC (2000).
It is well understood that temperature and precipitation are
Page 9 of 12
Pinus tabulaeformis forest Quercus wutaishanica forest
NPP (g C m−2 a−1) Change (%) NPP (g C m−2 a−1) Change (%)
— 634 —
559 +8.6 692 +8.8
621 +20.5 737 +15.9
727 +41.1 761 +19.8
— 634 —
575 +11.6 713 +12.2
617 +19.9 785 +23.5
671 +30.0 874 +37.5
dominant controls on plant photosynthesis (Dai and Fung
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
1993; Lieth 1975). Raising air temperature may either increase
NPP through metabolically enhanced photosynthesis as well
as by increasing nutrient availability through accelerated
decomposition, or inhibit NPP by enhancing plant respiration
and decreasing soil moisture. Increasing precipitation tends
to alleviate the water stress on plant growth, hence impos-
ing positive effects on NPP in water-limited regions. NPP in
boreal forest is characteristically low compared with temper-
ate forests because of reduced solar radiation, cold climate
and shorter growing seasons at higher latitudes (Keuper et al.
2012; Vanhala et al. 2008). Increased temperature may mark-
edly enhance NPP in the boreal L.  gmelinii forest. However,
the thawing of permafrost with climate warming and drought
could impose some adverse impacts on tree growth in boreal
forests. Long-term field experimental studies are certainly
required to closely examine the interactions between climate
change and forest responses in boreal regions with considera-
tion of the dynamics and impacts of permafrost. The much
conserved responses in the two temperate forest types suggest
that temperature is not a critical factor in constraining for-
est NPP and that increasing temperature may impose some
negative impact on NPP by inducing water deficit, thus par-
tially offsetting the growth response to elevated atmospheric
CO2 concentration and slightly increasing precipitation. Our
results showed that more drastic changes in climate and
atmospheric CO2 concentration under the carbon emissions
scenario SRES A2 would benefit relatively little to the decidu-
ous broadleaved Q. wutaishanica forest compared with other
two types of coniferous forests. The contrasting responses
to inter-annual variations and changes in climate across the
three forest types suggest some genetic controls of tree growth
in response to changing environmental conditions (Law et al.
2004; Sun and Sweet 1996; Sun et al. 1995).
The magnitudes of increase in forest NPP predicted in this
study are in line with predictions in other similar studies (Fang
2000; Ji et al. 2008; Peng et al. 2009), suggesting the adequacy
of using Biome-BGC in simulating forest productivity in the
Page 10 of 12
region with the aid of localized parameterization. Some of the
discrepancies between the simulated and measured patterns
of inter-annual variations in tree growth illustrate the com-
plex control of climate on forest productivity and emphasize
the need for long-term experimental studies addressing fun-
damental mechanisms underlying interactions among climate
change, site abiotic perturbations and forest responses. Lack of
representation of the dynamics and impacts of permafrost in
our simulations may explain the poor relationships between
the modeled NPP and RWI in the boreal L. gmelinii forest.
Supplementary material
Supplementary material is available at Journal of Plant Ecology
online.
Funding
Public Welfare Forestry of the State Forestry Administration
of China (201104008); Beijing Municipal Commission of
Education for development of Key Laboratory for Silviculture
and Conservation.
Acknowledgements
We wish to express our thanks to the Numerical Terradynamic
Simulation Group (NTSG) at the University of Montana for providing
the source code of model Biome-BGC version 4.2. We are also grateful
to Drs Zhongkui Luo and Hongxin Su for their assistance in performing
model simulations. Insightful comments by the handling editor and two
anonymous reviewers helped greatly with improving the manuscript.
Conflict of interest statement. None declared.
References
Bousquet P, Peylin P, Ciais P, et al. (2003) Regional changes in carbon
dioxide fluxes of land and oceans since 1980. Science 290:1342–7.
Briffa KR, Jones PD (1990) Basic chronology statistics and assess-
ment. In Cook ER, Kairiukstis LA (eds). Methods of Dendrochronology:
Applications in the Environmental Sciences. Amsterdam, The
Netherlands: Kluwer Academic Publishers, 137–52.
Cao MK, Price S, Li KR, et al. (2003) Response of terrestrial carbon
uptake to climate interannual variability in China. Glob Change Biol
9:536–46.
Christensen JH, Hewitson B, Busuioc A, et  al. (2007) Regional cli-
mate projections. In Solomon S, Qin D, Manning M, et al. (eds).
Climate Change 2007: The Physical Science Basis. Contribution of Working
Group I to the Fourth Assessment Report of the Intergovernmental Panel
on Climate Change. Cambridge, UK: Cambridge University Press,
847–940.
Churkina G, Running SW, Schloss AL (1999) Comparing global mod-
els of terrestrial net primary productivity: the importance of water
availability. Glob Change Biol 11:46–55.
Churkina G, Tenhunen J, Thornton P, et al. (2003) Analyzing the eco-
system carbon dynamics of four European coniferous forests using
a biogeochemistry model. Ecosystems 6:168–84.
Journal of Plant Ecology
Clark DA, Brown S, Kicklighter DK, et al. (2001) Measuring net pri-
mary production in forests: concepts and field methods. Ecol Appl
11:356–70.
Cook ER, Holmes RL (1986) Users Manual for Program ARSTAN.
Laboratory of Tree–Ring Research. Tucson, AZ: University of Arizona.
Dai A, Fung IY (1993) Can climate variability contribute to the ‘miss-
ing’ CO2 sink. Global Biogeochem Cycle 7:599–609.
Ding Y, Ren G, Shi G, et al. (2006) National assessment report of cli-
mate change (I): climate change in China and its future trend. Adv
Clim Change Res 2:3–8.
Dixon RK, Solomon AM, Brown S, et al. (1994) Carbon pools and flux
of global forest ecosystems. Science 263:185–90.
Editorial Committee on National Assessment Report on Climate
Change (ECNARCC) (2007) China’s National Assessment Report on
Climate Change. Beijing, China: Science Publishing House.
Fang JY (2000) Forest productivity in China and its response to global
climate change. Chin J Plant Ecol 24:513–7.
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
Fang JY, Liu GH, Zhu B, et al. (2006) Carbon budgets of three temper-
ate forest ecosystems in Dongling Mt., Beijing, China. Sci China Ser
D 36:533–43.
Fang JY, Piao SL, Field CB, et al. (2003) Increasing net primary pro-
duction in China from 1982 to 1999. Front Ecol Environ 1:293–97.
Feng L, Yang Y (1985) A study on biomass and production of three
types of Dahurian larch virgin forest. Sci Silv Sin 21:86–92.
Fritts HC (1976) Tree Ring and Climate. London, UK: Academic Press.
Gao Q, Zhang X (1997) A simulation study of responses of the north-
east China transect elevated CO2 and climate change. Ecol Appl
7:470–83.
Gower ST, Krankine O, Olson RJ, et al. (2001) Net primary produc-
tion and carbon allocation patterns of boreal forest ecosystems.
Ecol Appl 11:1395–1411.
Graumlich LJ, Brubaker LB, Grier CC (1989) Long–term trends in
forest net primary productivity: Cascade Mountains, Washington.
Ecology 70:405–10.
Hasenauer H, Petritsch R, Zhao MS, et al. (2012) Reconciling satellite
with ground data to estimate forest productivity at national scales.
Forest Ecol Manag 276:196–208.
Holland EA, Dentener FJ, Braswell BH, et al. (1999) Contemporary and
preindustrial global reactive nitrogen budgets. Biogeochemistry 46:7–43.
Holmes RL (1983) Computer–assisted quality control in tree–ring dat-
ing and measurement. Tree–Ring Bull 43:69–95.
Houghton RA (2005) Aboveground forest biomass and the global car-
bon balance. Glob Change Biol 11:945–58.
IPCC (2000) Emissions Scenarios. Cambridge, UK: Cambridge
University Press.
IPCC (2007) Climate change 2007: synthesis report. In Core Writing
Team, Pachauri RK, Reisinger A (eds). Contribution of Working Group
I, II and III to the Fourth Assessment Report of the Intergovernmental
Panel on Climate Change. In Pachauri RK, Reisinger A (eds). Geneva,
Switzerland: IPCC, 104.
Jarvis PG, Saugier B, Schulze E-D (2001) Productivity of boreal
forests. In Roy J, Saugier B, Mooney HA (eds). Terrestrial Global
Productivity. San Diego, CA: Academic Press, 211–44.
Ji JJ, Huang M, Li KR (2008) Prediction of carbon exchanges between
China terrestrial ecosystem and atmosphere in 21st century. Sci
China Ser D 38:211–23.
Ouyang et al.     |     Forest NPP response to variability and change in climate
Jiang H (1997) Study on biomass of the typical deciduous broad-
leaved forests in Dongling Mountain. In Chen LZ, Huang
JH (eds). Study on the Characteristics and Function of the Forest
Ecosystem in the Warm Temperate Zone. Beijing, China: Science
Press, 104–15.
Jiang H, Apps MJ, Zhang Y, et al. (1999) Modelling the spatial pat-
tern of net primary productivity in Chinese forests. Ecol Model
122:275–88.
Joos F, Prentice IC, Sitch S, et al. (2001) Global warming feedbacks
on terrestrial carbon uptake under the Intergovernmental Panel
on Climate Change (IPCC) emission scenarios. Global Biogeochem
Cycle 15:891–908.
Keenan TF, Baker I, Barr A, et al. (2012) Terrestrial biosphere model
performance for inter-annual variability of land-atmosphere CO2
exchange. Glob Change Biol 18:1971–87.
Keuper F, van Bodegom PM, Dorrepaal E, et al. (2012) A frozen feast:
thawing permafrost increases plant available nitrogen in subarctic
peatlands. Glob Change Biol 18:1998–2007.
Krakauer NY, Randerson JT (2003) Do volcanic eruptions enhance or
diminish net primary production? Evidence from tree rings. Global
Biogeochem Cycle 17:GB002076.
Law BE, Sun OJ, Campbell J, et al. (2003) Changes in carbon storage
and fluxes in a chronosequence of ponderosa pine. Glob Change Biol
9:510–24.
Law BE, Turner D, Campbell J, et al. (2004) Disturbance and climate
effects on carbon stocks and fluxes across Western Oregon USA.
Glob Change Biol 10:1429–44.
Li ZS, Liu GH, Fu BJ, et al. (2011) The potential influence of seasonal
climate variables on the net primary production of forests in east-
ern China. Environ Manage 48:1173–81.
Lieth H (1975) Modeling the primary productivity of the world. In
Lieth H, Whittaker RH (eds). Primary Productivity of the Biosphere.
New York, NY: Springer, 237–63.
Lindner M, Maroschek M, Netherer S, et al. (2010) Climate change
impacts, adaptive capacity, and vulnerability of European forest
ecosystems. For Ecol Manag 259:698–709.
Liu RG, Li N, Su HX, et al. (2009) Simulation and analysis on future
carbon balance of three deciduous forests in Beijing mountain
area, warm temperate zone of China. Chin J Plant Ecol 33:516–34.
Liu ZG, Ma QY, Pan XL (1994) A study on the biomass and pro-
ductivity of the natural Larix gmelinii forests. Chin J Plant Ecol
18:328–37.
Luo ZK, Sun OJ, Wang EL, et  al. (2010) Modeling productivity in
mangrove forests as impacted by effective soil water availability
and its sensitivity to climate change using Biome-BGC. Ecosystems
13:949–65.
Mahecha MD, Reichstein M, Jung M, et  al. (2010) Comparing
observations and process-based simulations of biosphere-atmos-
phere exchanges on multiple timescales. J Geophys Res Biogeosci
115:GO2003.
Melillo JM, McGuire AD, Kicklighter DW, et al. (1993) Global climate
change and terrestrial net primary production. Nature 363:234–40.
Monteith JL (1973) Principles of Environmental Physics. New York, NY:
Elsevier.
Morales P, Sykes MT, Prentice IC, et al. (2005) Comparing and evalu-
ating process–based ecosystem model predictions of carbon and
Page 11 of 12
water fluxes in major European forest biomes. Glob Change Biol
11:2211–33.
Myneni RB, Dong J, Tucker CJ, et al. (2001) A large carbon sink in
the woody biomass of Northern forests. Proc Natl Acad Sci U S A
98:14784–9.
Nemani RR, Keeling CD, Hashimoto H, et al. (2003) Climate-driven
increases in global terrestrial net primary production from 1982 to
1999. Science 300:1560–3.
Ni J, Zhang XS, Scurlock JMO (2001) Synthesis and analysis of bio-
mass and net primary productivity in Chinese forests. Ann Forest
Sci 58:351–84.
Peng CH, Zhou XL, Zhao SQ, et al. (2009) Quantifying the response
of forest carbon balance to future climate change in northeast-
ern China: model validation and prediction. Global Planet Change
66:179–94.
Piao SL, Ciais P, Lomas M, et al. (2011) Contribution of climate change
and rising CO2 to terrestrial carbon balance in East Asia: a multi–
model analysis. Global Planet Change 75:133–42.
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
Piao SL, Fang JY, Guo QH (2001) Application of CASA model to the
estimation of Chinese terrestrial net primary productivity. Chin J
Plant Ecol 25:603–8.
Piao SL, Fang JY, Zhou LM, et al. (2005) Changes in vegetation net pri-
mary productivity from 1982 to 1999 in China. Global Biogeochem
Cycle 19:GB2027.
Piao SL, Friedlingstein P, Ciais P, et al. (2007) Growing season exten-
sion and its impact on terrestrial carbon cycle in the Northern
Hemisphere over the past 2 decades. Global Biogeochem Cycle
21:GB3018.
R Development Core Team (2009) R: A Language and Environment for
Statistical Computing. Vienna, Austria: R Foundation for Statistical
Computing. http://www.R-project.org (20 September 2013, date
last accessed).
Rathgeber C, Nicault A, Guiot J, et al. (2000) Simulated responses
of Pinus halepensis forest productivity to climatic change and
CO2 increase using a statistical model. Global Planet Change
26:405–42.
Rathgeber C, Nicault A, Kaplan JO, et al. (2003) Using a biogeochem-
istry model in simulating forests productivity responses to climatic
change and [CO2] increase: example of Pinus halepensis in Provence
(south–east France). Ecol Model 166:239–55.
Ren GY, Zhou YQ, Chu ZY, et  al. (2008) Urbanization effects on
observed surface air temperature trends in North China. J Climate
21:1333–48.
Ren GY, Ding YH, Zhao Z, et al. (2012) Recent progress in studies of
climate change in China. Adv Atmos Sci 29:958–77.
Ruelle D (1978) Sensitive dependence on initial condition and turbu-
lent behavior of dynamical systems. Ann N Y Acad Sci 316:408–16.
Running SW, Coughlan JC (1988) A general model of forest ecosystem
processes for regional applications I. Hydrologic balance, canopy gas
exchange and primary production processes. Ecol Model 42:125–54.
Scurlock JM, Johnson K, Olson RJ (2002) Estimating net primary
productivity from grassland biomass dynamics measurements.
Glob Change Biol 8:736–53.
Shaw MR, Zavaleta ES, Chiariello NR, et  al. (2002) Grassland
responses to global environmental changes suppressed by elevated
CO2. Science 298:1987–90.
Page 12 of 12
Shi FC, Qu LY, Wang WJ, et  al. (2002) Aboveground biomass and
productivity of Larix gmelinii forests in Northeast China. Eur J Forest
Res 5:23–32.
Su HX, Sang WG, Wang YX, et al. (2007) Simulating Picea schrenkiana
forest productivity under climatic changes and atmospheric CO2
increase in Tianshan Mountains, Xinjiang Autonomous Region,
China. Forest Ecol Manag 246:273–84.
Sun OJ, Campbell J, Law BE, et al. (2004) Dynamics of carbon stor-
age in soils and detritus across chronosequences of different forest
types in the Pacific Northwest, USA. Glob Change Biol 10:1470–81.
Sun OJ, Sweet GB (1996) Genotypic variation in light and tempera-
ture response of photosynthesis in Nothofagus solandri var. cliffor-
tioides and N. menziesii. Aust J Plant Physiol 23:421–8.
Sun OJ, Sweet GB, Whitehead D, et al. (1995) Physiological responses
to water stress and waterlogging in Nothofagus species. Tree Physiol
15:629–38.
Tan K, Piao S, Peng C, et al. (2007) Satellite–based estimation of bio-
mass carbon stocks for northeast China’s forests between 1982 and
1999. Forest Ecol Manag 240:114–21.
Tao FL, Yokozawa M, Zhang Z, et al. (2005) Remote sensing of crop
production in China by production efficiency models: models com-
parisons, estimates and uncertainties. Ecol Model 183:385–96.
Thornton PE, Hasenauer H, White MA (2000) Simultaneous esti-
mation of daily solar radiation and humidity from observed tem-
perature and precipitation: an application over complex terrain in
Austria. Agr Forest Meteorol 104:255–71.
Thornton PE, Law BE, Gholz HL, et al. (2002) Modeling and measur-
ing the effects of disturbance history and climate on carbon and
water budgets in evergreen needleleaf forests. Agr Forest Meteorol
113:185–222.
Thornton PE, Rosenbloom NA (2005) Ecosystem model spin–up: esti-
mating steady state conditions in a coupled terrestrial carbon and
nitrogen cycle model. Ecol Model 189:25–48.
Thornton PE, Running SW (1999) An improved algorithm for
estimating incident daily solar radiation from measurements of
temperature, humidity, and precipitation. Agr Forest Meteorol
93:211–28.
Turner DP, Ritts WD, Cohen WB, et al. (2005) Site–level evaluation of
satellite–based global terrestrial gross primary production and net
primary production monitoring. Glob Change Biol 11:666–84.
Vanhala P, Karhu K, Tuomi M, et al. (2008) Temperature sensitivity of
soil organic matter decomposition in southern and northern areas
of the boreal forest zone. Soil Biol Biochem 40:1758–64.
Journal of Plant Ecology
Vetter M, Churkina G, Jung M, et al. (2008) Analyzing the causes and
spatial pattern of the European 2003 carbon flux anomaly using
seven models. Biogeosciences 5:561–83.
Wang Q, Ni J, Tenhunen J (2005) Application of a geographi-
cally–weighted regression analysis to estimate net primary
production of Chinese forest ecosystems. Global Ecol Biogeogr
14:379–93.
Wang WF, Peng, CH, Kneeshaw DD, et  al. (2012) Quantifying the
effects of climate change and harvesting on carbon dynamics of
boreal aspen and jack pine forests using the TRIPLEX–Management
model. Forest Ecol Manag 281:152–62.
White MA, Thornton PE, Running SW, et al. (2000) Parameterization
and sensitivity analysis of the BIOME–BGC terrestrial ecosys-
tem model: net primary production controls. Earth Interactions
4:1–85.
Wigley TML, Briffa, KR, Jones PD (1984) On the average value of
correlated time series, with applications in dendroclimatology and
hydrometeorology. J Clim Appl Meteorol 23:201–13.
Downloaded from http://jpe.oxfordjournals.org/ by Osbert Sun on January 23, 2014
Wu DX (1990) Tree Rings and Climate Change. Beijing, China: China
Meteorological Press.
Xiao JF, Zhuang QH, Liang E, et  al. (2009) Twentieth-century
droughts and their impacts on terrestrial carbon cycling in China.
Earth Interactions 13:1–31.
Xiao XM, Melillo J, Kicklighter DW, et  al. (1998) Net primary pro-
ductivity of terrestrial ecosystems in China and its equilibrium
response to changes in climate and atmospheric CO2 concentra-
tion. Chin J Plant Ecol 22:97–118.
Yi LT, Han HR, Cheng XQ, et al. (2008) Spatial distribution patterns of
Quercus liaotungensis population in LingKong Mountains. Acta Ecol
Sin 28:3254–61.
Yu M, Sun OJ (2013) Effects of forest patch type and site on herb-
layer vegetation in a temperate ecosystem. Forest Ecol Manag
300:14–20.
Zhai BG, Song CH, Zhang HD, et al. (1992) Studies on biomass and
productivity of Pinus tabulaeformis plantation at a permanent eco-
system plot in Taiyue Forest Region, Shanxi Province. J Beijing
Forest Univ 14:156–63.
Zhao GS, Wang JB, Fan WY, et al. (2011) Vegetation net primary pro-
ductivity in Northeast China in 2000-2008: simulation and sea-
sonal change. Ying Yong Sheng Tai Xue Bao 22:621–30.
Zhu WQ, Pan YZ, Zhang JS (2007) Estimation of net primary produc-
tivity of Chinese terrestrial vegetation based on remote sensing.
Chin J Plant Ecol 31:413–24.