Ecosystems (2010) 13: 949–965

DOI: 10.1007/s10021-010-9365-y
 2010 Springer Science+Business Media, LLC

Modeling Productivity in Mangrove

Forests as Impacted by Effective Soil
Water Availability and Its Sensitivity
to Climate Change Using Biome-BGC
Zhongkui Luo,1,2 Osbert Jianxin Sun,1* Enli Wang,3 Hai Ren,4
and Hualin Xu5

1
MOE Key Laboratory for Silviculture and Conservation, Beijing Forestry University, Beijing 100083, China; 2State Key Laboratory of
Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; 3CSIRO Land and
Water, Black Mountain, Canberra, Australian Capital Territory 2601, Australia; 4South China Botanical Garden, Chinese Academy of
Sciences, Guangzhou 510650, China; 5Neilingding-Futian National Nature Reserve of Guangdong, Shenzhen 518040, China

ABSTRACT
Ecosystem dynamics and the responses to climate
change in mangrove forests are poorly understood.
We applied the biogeochemical process model
Biome-BGC to simulate the dynamics of net pri-
mary productivity (NPP) and leaf area index (LAI)
under the present and future climate conditions in
mangrove forests in Shenzhen, Zhanjiang, and
Qiongshan across the southern coast of China, and
in three monocultural mangrove stands of two
native species, Avicennia marina and Kandelia obov-
ata, and one exotic species, Sonneratia apetala, in
Shenzhen. The soil hydrological process of the
model was modified by incorporating a soil water
Received 25 December 2009; accepted 5 July 2010;
published online 7 August 2010
Electronic supplementary material: The online version of this article
(doi:10.1007/s10021-010-9365-y) contains supplementary material,
which is available to authorized users.
Author Contributions: Zhongkui Luo carried out the field measure-
ments and data analysis, ran simulation, and wrote the manuscript. Os-
bert J. Sun designed the experiment and wrote the manuscript. Enli
Wang contributed to modeling and manuscript writing. Hai Ren and
Hualin Xu contributed data and helped with field measurements and data
collections.
*Corresponding author; e-mail: sunjianx@bjfu.edu.cn
(SW) stress index to account for the impact of the
effective SW availability in the coastal wetland. Our
modified Biome-BGC well predicted the dynamics
of NPP and LAI in the mangrove forests at the study
sites. We found that the six mangrove systems
differed in sensitivity to variations in the effective
SW availability. At the ecosystem level, however,
soil salinity alone could not entirely explain the
limitation of the effective SW availability on the
productivity of mangrove forests. Increasing
atmospheric CO2 concentration differentially
affected growth of different mangrove species but
only had a small impact on NPP (<7%); whereas a
doubling of atmospheric CO2 concentration asso-
ciated with a 2C temperature rise would increase
NPP by 14–19% across the three geographically
separate mangrove forests and by 12% to as much
as 68% across the three monocultural mangrove
stands. Our simulation analysis indicates that
temperature change is more important than
increasing CO2 concentration in affecting produc-
tivity of mangroves at the ecosystem level, and that
different mangrove species differ in sensitivity to
increases in temperature and CO2 concentration.
Key words: climate change; effective soil water
availability; leaf area index; mangroves; net pri-
mary production; salinity; simulation.

949
950 Z. Luo and others
INTRODUCTION
Mangrove forests play a vital role in conserving
biodiversity and buffering disturbance in coastal
regions. A clear understanding of the factors that
regulate the growth of mangroves and knowledge
of the dynamics of mangrove ecosystems under
future climate changes are critically important to
devising management strategies aimed for conser-
vation of this unique and threatened biotic system
(Field 1995; Valiela and others 2001). However,
under the prediction that the global mean air
temperature will be likely to rise by 1.1–6.4C
above the current level and the atmospheric CO2
concentration may reach between 730 and
1020 ppm at the end of this century (IPCC 2007), it
is yet uncertain how mangroves may respond to
these future climate changes (Alongi 2002; Luo and
others 2007).
Numerous studies have indicated that increasing
atmospheric CO2 concentration and rising surface
air temperature, individually or in combination,
can have significant impacts on ecosystem pro-
cesses, including vegetation zonation and commu-
nity succession, species interactions within and
among trophic levels, and carbon (C) assimilation
and turnover, across various upland ecosystems
(Field and others 2007; Hyvönen and others 2007;
Tylianakis and others 2008). Although there is
evidence that mangrove ecosystems are function-
ally similar with upland forests (Ellison 2002), the
submerged growth environment and high salinity
in coastal wetlands may significantly differentiate
the two systems in response to future climate
changes. In comparison with canopy processes, soil
processes in mangrove ecosystems may undergo
little alterations by direct impact of changes in
atmospheric environment due to the confounding
effect of poor aeration under submerged or water-
saturated soil conditions, leading consequently to
differentially regulated physiological processes and
patterns of water and nutrient utilizations under
future climate changes in mangrove ecosystems.
Temperature is known as the dominant factor
limiting the distribution and growth of mangroves
(Duke and others 1998; Alongi 2002; Stuart and
others 2007), and considerable variation can be
found among mangrove species in their sensitivity
to changes in temperature (Field 1995). The
majority of mangrove species reach maximal shoot
growth when mean air temperature rises to 25C
(Hutchings and Saenger 1987), whereas the maxi-
mum rates of photosynthesis generally occur at leaf
temperatures around 30C (Ball and others 1988).
In southern Florida, USA, a modeling study indi-
cates that the primary production of Rhizophora
mangle Roxb., a neotropical mangrove species, de-
creases with rising air temperature (Miller 1972).
Elevated atmospheric CO2 concentrations in con-
junction with increases in air temperature are
commonly found to enhance C gain of most plants,
but the effects differ on different plant types and in
different habitats. Photosynthesis-related eco-
physiological attributes, such as leaf conductance to
CO2 and water vapor, also change markedly with
latitude, temperature, precipitation, and fresh wa-
ter supply in mangroves (Duke and others 1998;
Alongi 2002). A study by Ball and others (1997)
shows that although an elevated CO2 concentra-
tion at 700 ppm enhances the growth rate in Rhi-
zophora apiculata Blume and Rhizophora stylosa
Griff., the relative responses of the two species vary
with soil salinity and air humidity, indicating
alteration of the inter-specific relationships among
mangrove species along salinity–aridity gradients
by elevated CO2. A long-term study with R. mangle
indicates that elevated CO2 accelerates growth and
alters growth attributes (Farnsworth and others
1996). Through the various effects on eco-physio-
logical attributes of mangrove species, the rising air
temperature and an increase in atmospheric CO2
concentration may change the distributional pat-
tern, species composition, and C cycling of man-
grove ecosystems.
Because of the technical difficulties in field
experimentation and lack of long-term data, studies
that address the interactive effects of increasing
CO2 concentration and rising air temperature on
the structure and functioning of mangrove forests
are lacking (Field 1995; Alongi 2002), particularly
when considering the variability among species and
over large scales as well as in terms of interactive
effects with other environmental factors. Process-
based simulation modeling can overcome this lim-
itation as it is an effective tool for analyzing the
complex interactions through integration of the
responses in the ecological and physiological pro-
cesses to various environmental constraints (Clark
and Gelfand 2006). Its application can provide in-
sight into the interactions of mangrove ecosystems
with changing environmental conditions when
direct experimental evidence is lacking.
A number of process models have been devel-
oped and used for simulation of mangrove forests
focusing on specific ecological processes; examples
of these types of models include FORMAN (Chen
and Twilley 1998), KiWi (Berger and Hildenbrandt
2000), and NUMAN (Chen and Twilley 1999).
FORMAN is a gap dynamics model developed by
 Modeling Mangrove Forests Using Biome-BGC
Chen and Twilley (1998) for simulation of stand
dynamics in mangrove forests. KiWi is also a stand
dynamic model incorporating population growth,
competition, and demographic processes (Berger
and Hildenbrandt 2000). NUMAN, a process-based
biogeochemical model with a simplified manipu-
lation of aboveground processes, has been devel-
oped for simulation of soil organic matter
decomposition and nutrient cycling (Chen and
Twilley 1999). For simulations of the effects of
salinity in coastal wetlands, a model has been
developed for projecting changes in salinity con-
centrations and species dominance in the coastal
habitats of the Everglades, southern Florida, USA
(Teh and others 2008). However, for simulation at
the ecosystem level, incorporation of various
above- and belowground ecological processes cap-
turing the energy, water, and nutrient dynamics is
crucial for achieving a mechanistic understanding
on the responses of mangroves to changing envi-
ronmental conditions. The existing simulation
models for mangroves are all individual-based and
used for describing simple ecosystem processes,
primarily concerning biotic regulations (Berger and
others 2008). Although these types of models are
useful for simulating specific ecosystem processes
in mangrove forests for management purposes and/
or study of individual processes, they are not useful
for wider applications in the context of global cli-
mate change.
Compared with those for mangrove forests, most
of the process-based simulation models for upland
ecosystems have been developed with more
sophisticated structures and descriptions of more
complex ecosystem processes and interactions,
benefitting from the availability of more detailed
information on, and better understanding of, the
upland ecosystem processes. Biome-BGC is a well-
established biogeochemical model for simulating
the storage and fluxes of water, C, and nitrogen
(N), all in a coupled manner and interactively
linking the above- and belowground processes in
terrestrial ecosystems at a daily time step and var-
ious ecological scales (Churkina and others 2003).
One of the most common applications of the
Biome-BGC model is for assessment of the
dynamics of forest productivity and ecosystem C
storage in response to disturbances and changes in
climate (Law and others 2003, 2004). This makes
the model a relevant tool for studying the responses
of mangrove forests to future climate changes.
However, as mangroves are a special group of
plants that grow in environments normally not
habitable for most of the terrestrial vascular plants,
direct application of Biome-BGC to mangrove
951
forests may be constrained by lack of appropriate
representations of the eco-physiological responses
to simulate the spatiotemporal dynamics in man-
grove ecosystems. Some modifications of the pro-
cesses in Biome-BGC are undoubtedly required to
make it applicable to mangrove forests.
It is known that soil water (SW) availability in
terms of salinity stress can significantly affect on
growth and physiological processes in mangroves
(Ball and Pidsley 1995; Kathiresan and Bingham
2001). López-Hoffman and others (2007) found
that mangroves growing at low soil salinity had
higher stomatal conductance, leaf-level transpira-
tion, and internal CO2 concentrations than those
growing at high salinity, and thus had greater rates
of net photosynthesis, growth, and survival. When
the same mangrove species grow at different
severities of salinity, their growth forms may show
distinct features in response to salinity level. For
example, in R. mangle, tall trees (5–10 m) are found
in habitats with lower salinity, whereas dwarf trees
(1 m or less) are common in habitats with high
salinity due to an apparent impact of water stress
(Hao and others 2009). Therefore, accounting for
the effects of salinity appears to be critical to
accurately model the dynamics of mangrove forests
and the responses to environmental variations
using the models developed based on ecological
processes in upland ecosystems.
In this study, we synthesized data from the lit-
erature and field surveys to parameterize the bio-
geochemical model Biome-BGC to simulate the
dynamics of mangrove forests in response to cli-
mate change. We modified the model to consider
the water stress effect of salinity and applied the
modified model to simulate net primary produc-
tivity (NPP) and leaf area index (LAI) in mangrove
forests at three separate locations (that is, Shenz-
hen, Zhanjiang, and Qiongshan) along the south-
ern coast of China, under the current and predicted
future climate conditions. We also tested the per-
formance of the modified model to simulate NPP
and LAI of three monocultural mangrove stands in
Shenzhen, including two native species, Avicennia
marina (Forssk.) Vierh. and Kandelia obovata Sheue,
Liu and Yong, and one exotic species, Sonneratia
apetala Buch.–Ham. Our objectives were to: (1)
examine the ability of the modified Biome-BGC to
predict NPP and LAI of mangrove forests, (2) test
the hypothesis that effective SW availability, in
term of salinity stress, was a major constraint to
productivity in mangrove ecosystems, and (3)
predict the responses of mangrove forests of
different localities and community structures to
climate change.
952 Z. Luo and others
MATERIALS AND METHODS
Study Sites and Mangrove Systems
Three natural mangrove systems were selected for
ecosystem level simulation. They were from
Shenzhen, Zhanjiang (latitude 2130¢N, longitude
10941¢E), and Qiongshan, along the southern coast
of China (Figure 1). In addition, three monocultural
mangrove stands in Shenzhen were used for stand
level simulation. Most of the mangrove forests at
these locations are in natural reserves and represent
the main mangrove communities across subtropical
and tropical climate zones in China. The site condi-
tions differ among the three locations: Shenzhen is
the northern-most site (latitude 2232¢N, longitude
11400¢E) and has the coarsest soils (clay 29%, silt
59%, and sand 12%) and intermediate soil salinity
(15&), with an average soil depth at 0.9 m; Qiong-
shan is the southern-most site (latitude 1951¢N,
longitude 11024¢E) and has the finest soils (clay
61%, silt 30%, and sand 9%) and lowest soil salinity
(11&), with an average soil depth at 1.2 m; while
Zhanjiang is characterized by the highest soil salinity
(18&) and intermediate soil texture (clay 37%, silt
57%, and sand 6%), with an average soil depth at
0.9 m. The average stand ages are approximately
65 years at Shenzhen, approximately 80 years at
Zhanjiang, and approximately 70 years at Qiong-
shan.
Of the three locations, Qiongshan has the highest
mangrove species diversity, where mangrove
communities usually associate with other salt-tol-
erant species and compose ‘‘mangrove associates’’
(Mao and others 2003; Wang and others 2010).
The dominant species include Bruguiera gymnorrh-
iza (Linn.) Savigny, Bruguiera sexangula (Lour.)
Poir., K. obovata, and R. stylosa. Those mangrove
Figure 1. Location of study sites.
species usually occupy distinct zones along the
intertidal regions from the sea to upland. In
Zhanjiang, the composition of mangrove commu-
nity and the stand structure is relatively simple;
natural mangrove forests occur along the coastline
and extend hundreds of meters seaward from the
upland. Aegiceras corniculatum (L.) Blanco., B. gym-
norrhiza, K. obovata, and R. stylosa are the most
dominant species at this site. In Shenzhen, natural
mangrove forests occur along the coastline and
extend 50–150 m seaward from the upland. Three
native species, A. corniculatum, A. marina, and K.
obovata, dominate the mangrove community, and
usually occur as mosaics of monocultural stands
with open understory (Luo and others 2010). In
1993, two exotic mangrove species, S. apetala and
Sonneratia caseolaris (L.) Engl., were introduced to
Shenzhen from Hainan Province (originally intro-
duced to Hainan from Bangladesh in 1985), China,
and cultivated successfully and dispersed rapidly.
We used the monocultural stands of A. marina,
K. obovata, and S. apetala in Shenzhen for stand
level simulation of different mangrove species. The
three types of stands have contrasting characteris-
tics: A. marina is a small tree and forms stands with
an average age of 68 years and canopy height of
approximately 4.5 m at the study site; K. obovata is
a small or medium tree and forms stands with an
average age of 63 years and canopy height of
approximately 6 m; S. apetala is a fast-growing tree
and forms stands with an average age of 13 years
and canopy height of approximately 10 m.
Field Measurements and Literature
Survey
For the three monocultural mangrove stands in
Shenzhen, field surveys and measurements were
conducted in 2005 and 2006. Measurements were
made on stand biomass, LAI, and selected leaf
traits.
Stand Biomass
Four 10 9 10 m2 plots were established for each
stand. Tree diameter at breast height (DBH, 1.3 m)
and the average canopy height (H) were measured.
Biomass was then estimated from DBH and H using
species-specific allometric equations (Tam and
others 1995; Weng 1999).
LAI
Hemispherical photographs, taken with a Nikon
Coolpix 4500 camera with a FC-E8 fisheye lens
at 1 m above the ground surface, were used to
 Modeling Mangrove Forests Using Biome-BGC
analyze the understory light environment and
calculate the canopy LAI. True color photographs
were taken at multiple locations on each plot under
diffuse light conditions (that is, at dawn and dust or
under overcast sky conditions). These photos were
analyzed using the imaging software GLA 2.0
(Frazer and others 1999). Separating the canopy
from the sky is one of the most critical steps, which
requires a binary transformation usually done by
setting a manual threshold. We used the software
SideLook 1.1 to calculate automatic thresholds
thereby avoiding subjectivity and improving the
accuracy of the analyses (Nobis and Hunziker
2005).
Leaf Traits
Leaf samples were collected from three randomly
selected trees on each plot for measurements of C:N
ratio and specific leaf area (SLA, m2 [kg C]-1). Total
C and N concentrations were determined on oven-
dried leaf samples (70C to constant mass) using
wet-combustion and Kjeldahl methods (Gallaher
and others 1976), respectively.
For the mangrove forests at the three different
locations, we conducted a literature survey to ob-
tain data required for the Biome-BGC simulation
(see appendix in Supplemental materials).
Model Simulations
Description of Biome-BGC
Biome-BGC is a biogeochemical model that simu-
lates the storage and fluxes of water, C and N in
terrestrial ecosystems using a daily time step and at
different ecological scales (Kimball and others
1997; Churkina and others 2003). It requires daily
weather data as inputs, including radiation, maxi-
mum and minimum temperatures, precipitation,
and daytime vapor pressure deficit (VPD). It also
requires information describing the soil properties
and eco-physiological traits of vegetation.
In Biome-BGC, NPP is defined as the difference
between gross primary productivity (GPP) and
autotrophic respiration (Ra), where GPP is a func-
tion of air temperature (T), VPD, SW content, solar
radiation at the top of the canopy (SRAD), CO2
concentration, and LAI; Ra is a function of T, leaf N
content (LN), and root N content (RN). There is
only one layer in the canopy, but the leaf area is
divided into shaded and sunlit fractions. Photo-
synthesis is based on the Farquhar equation (Far-
quhar and others 1980). Leaf conductance is
regulated by air temperature, radiation, leaf water
potential, LN, and atmospheric humidity and CO2.
953
Leaf-level C and water fluxes are scaled to the
canopy level based on LAI. A detailed description of
the model can be found in Churkina and Running
(1998) and Churkina and others (2003).
We used the Biome-BGC 5.0 for Excel (http://
www.ntsg.umt.edu/models/bgc/index.php), and
focused on the ability of the model to simulate
annual NPP and LAI of the six mangrove systems
under the present environment and future condi-
tions based on climate change scenarios.
Model Modification
Mangroves mainly grow under water-logged con-
ditions, and thus the quantity of water supply is
generally not an issue without a substantial modi-
fication of the habitat. However, salinity-induced
water stress could greatly affect water uptake by
mangrove roots and constrain the water transpor-
tation from roots to leaves along the water poten-
tial gradient, causing leaf water deficits (Hao and
others 2009). We therefore modified the water
stress index (SI) by introducing a parameter
accounting for the impact of water salinity.
In Biome-BGC, leaf water potential is one of the
dominant factors relating to SW condition and
controlling the capacity of leaf C assimilation. In
the original model, a SI based on leaf and SW po-
tential is used to regulate maximum stomatal
conductance and then leaf photosynthesis (module
BGC_FUNCTIONS CanopyET):
LWPc  SWP
fLWP ¼ ; 0  fLWP  1; ð1Þ
LWPc  LWPs
where LWPs is leaf water potential when leaf con-
ductance starts to decline, LWPc is leaf water po-
tential when the stomata are closed, and SWP is
SW potential, which changes with SW content and
texture, and is calculated as (module BGC_FUNC-
TIONS SoilPSI):
 
SWC a
SWP ¼ SWPs  ; ð2Þ
SWCs
where SWPs is SW potential at saturation water
content (that is, SWCs), both SWPs and SWCs are a
function of soil texture (that is, relative distribution
of clay, silt, and sand), SWC is the actual SW con-
tent, and a is a factor relating to soil texture. The-
oretically, total water potential, w, can be expressed
as the sum of several components (Brady and Weil
2008):
w ¼ wg þ wm þ wp þ wo ; ð3Þ
where the subscripts g, m, p, and o represent
gravitational potential, matric potential, pressure
954 Z. Luo and others
potential, and osmotic potential, respectively. Os-
motic potential occurs when solutes are dissolved
in water. It is linearly related to the solute con-
centration of the soil (that is, soil salinity in this
study). Equation (2) assumes that SW potential is
only regulated by SW content and soil texture, and
no salinity impact is considered. In the case of
mangrove forests, we assume that SW content
remains saturated. Thus,
SWC ¼ SWCs : ð4Þ
SW potential is additionally regulated by soil
salinity (that is, wo). According to Eqs. (3) and (4),
Eq. (2) can be simplified as:
 
SWCs a
SWP ¼ SWPs  þ wo ¼ SWPs þ wo ; ð5Þ
SWCs
where wo is assumed to be linearly related to soil
salinity (Ss) and given as:
wo ¼ b  Ss ; ð6Þ
where b is an empirical parameter describing the
impact of salinity that regulates SW potential in
mangrove forest soils. Hence, fLWP under the
mangrove systems is calculated as:
LWPc  ðSWPs  b  Ss Þ
fLWP ¼ : ð7Þ
LWPc  LWPs
Here, we refer to fLWP as the SI of SW availability
on leaf water potential. A SI of 1 indicates that
leaf water potential is not limited by SW avail-
ability; a SI of 0 indicates that the leaf cannot use
SW.
Model Parameterization
Many years of research on mangroves in China
have accumulated a rich amount of information
on the eco-physiological characteristics of the
mangrove species (see reviews by Lin 1997; Luo
and others 2007; Chen and others 2009). Eco-
physiological parameterization of the modified
Biome-BGC was made using data collected from
the literature for mangrove forests at the three
different locations without differentiating species
(Table 1). Species-specific parameterization was
carried out for the three monocultural mangrove
stands in Shenzhen using data both from the lit-
erature and the field measurements in this study
(Table 2). Average values were used if multiple
data sources were found for the same attributes. If
the site- and/or species-specific information were
not available, the generic values of White and
others (2000) were used as default (Table 1).
Climate Data
Data on the daily maximum, minimum, and aver-
age temperatures and precipitation were obtained
from the China Meteorological Data Sharing Ser-
vice System (http://cdc.cma.gov.cn; Figure 2).
Other meteorological variables (for example, radi-
ation and daytime vapor pressure) required by the
Biome-BGC were derived using the microclimate
simulator MTCLIM-XL, which provides an estima-
tion of the missing meteorological variables based
on measurements of temperature, precipitation,
and geographical and topographical information
such as latitude, longitude, elevation, slope, and
aspect (Thornton and Running 1999; Thornton and
others 2000).
Model Calibration and Validation
We used the following formula to set the best-fit SI
(SIopt, that is, the value when observed variable
and the modeled variable have the best agree-
ment):
sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
Pn 2
i¼1 ðxm  xo Þ
RMSE ¼ ; ð8Þ
n
where xm is the modeled value (mainly for NPP in
this study), and xo is the observed value (that is,
observed NPP), n is the number of the observed
values, RMSE is the square root of the mean of the
squared prediction errors. We derived the value of
SIopt when RMSE was at the minimum. In fact,
SIopt shows the real stress of SW on mangroves in
situ. We also set the threshold value of SI (SItlv, that
is, the tolerance of mangroves to SW stress) when
modeled NPP became 0, that is, GPP = Ra. For the
mangrove forests at the three different locations
and the three monocultural stands in Shenzhen,
we assumed that each site and species had a specific
SIopt and SItlv.
In the model run process, we first conducted a
spin-up run for each site to get initial C and N state
variables, based on the assumption that the eco-
system is in equilibrium with the long-term cli-
mate. For the three monocultural stands in
Shenzhen, we used the initialization results based
on the spin-up run of the same site. As the target
mangrove forests of the simulations are all at cer-
tain ages, the tree C and N pools were consequently
reinitialized with the minimum initial values pos-
sible to represent a young stand (Churkina and
others 2003). For all the six target mangrove sys-
tems, initial C and N pools of live stems and roots
were set to zero. Alternatively, the initial leaf C
pool was set to the minimum possible values so that
Table 1. Values Used in the Eco-physiological Parameterization for Simulation of NPP and LAI in Mangrove Forests in Qiongshan, Zhanjiang, and
Shenzhen, South China, using the Biome-BGC Model
Parameter Unit Value Data source

Annual turnover rates

Annual leaf and fine root turnover fraction y-1 0.75 Lin and others (1985, 1990, 1992); Zheng and others (1995b, c)
Annual live wood turnover fraction y-1 0.7 White and others (2000)
Annual whole-plant mortality fraction y-1 0.03 Lin and others (1990, 1992); Zheng and others (1994, 1995b, c, 1998); Zheng and
Lin (1995); Peng and others (2005)
Allocation ratios
New fine root C to new leaf C DIM 1 White and others (2000)
New stem C to new leaf C DIM 0.6 Lin and others (1985, 1990, 1992, 1995, 1998); Yin and Lin (1993b); Zheng and
Lin (1995); Zheng and others (1995b, c); Liao and others (1999); Wen (1999);
Zan and others (2001b); Han and others (2004)
New live wood C to new total wood C DIM 0.31 Lin and others (1985, 1990, 1992, 1995, 1998); Yin and Lin (1993b); Zheng and
Lin (1995); Zheng and others (1995b, c); Zan and others (2001b); Han and
others (2004)
New coarse root C to new stem C DIM 1.5 Lin and others (1985, 1990, 1992, 1995, 1998); Yin and Lin (1993b); Zheng and
Lin (1995); Zheng and others (1995b, c); Liao and others (1999); Zan and
others (2001b); Han and others (2004)
Current growth to storage growth DIM 0.5 White and others (2000)
C/N ratios
Leaves g C g-1 N 26 This study; Yin and Lin (1993a, c); Zheng and others (1994); Zheng and others
(1995a, b, c)
Leaf litter after retranslocation g C g-1 N 52 Yin and Lin (1993c); Lu and others (1994); Zheng and others (1994, 1995b, c)
Fine roots g C g-1 N 49 Yin and Lin (1993a); Yin and Lin (1993c); Zheng and others (1994, 1995b, c)
Live wood g C g-1 N 49 Yin and Lin (1993a, c); Zheng and others (1994, 1995b, c)
Dead wood g C g-1 N 225 Yin and Lin (1993c); Zheng and others (1994, 1995b, c)
Labile, cellulose and lignin fractions in decomposition pools
Leaf litter labile proportion DIM 0.32 White and others (2000)
Leaf litter cellulose proportion DIM 0.44 White and others (2000)
Leaf litter lignin proportion DIM 0.24 White and others (2000)
Fine root labile proportion DIM 0.34 White and others (2000)
Fine root cellulose proportion DIM 0.44 White and others (2000)
Fine root lignin proportion DIM 0.22 White and others (2000)
Dead wood cellulose proportion DIM 0.76 White and others (2000)
Dead wood lignin proportion DIM 0.24 White and others (2000)
Canopy parameters
Water interception coefficient LAI-1 d-1 0.045 White and others (2000)
Light extinction coefficient DIM 0.65 This study
Modeling Mangrove Forests Using Biome-BGC

All-sided to projected leaf area ratio DIM 2 White and others (2000)
Average SLA (projected area basis) m2 kg-1 C 25 This study; Lin and Wang (2001)
955
956 Z. Luo and others

1996, 1998); Yang and others (2001); Zan and others (2001a); Jing and others
the model can run meaningfully (that is, the min-

Zheng and Lin (1990); Lei and Lin (1995, 1996, 1998); Jing and others (2005)
Zheng and Lin (1990, 1992, 1997); Lu and others (1994); Lei and Lin (1995,
imum leaf biomass that is needed to assimilate C
and maintain the stand growth); and the corre-

Zheng and Lin (1990); Lei and Lin (1996, 1998); Jing and others (2005)
sponding LN pool was set according to the leaf C:N
ratio (Tables 1, 2) . The model was then run to the
number of years to the age of the specific stand
with continuously increasing atmospheric CO2
concentration according to the attached
CO2_Worksheet in the model.
For the ecosystem level simulation, we assumed
that mangrove growth was mainly regulated by soil
salinity (Ss), whereas other eco-physiological
parameters remained the same. We performed a
calibration to derive the b value when the best-fit
SI was attained, that is, when RMSE was at the
minimum, using the dataset from the site in
(2005); Chen and others (2008)

Shenzhen with site-specific soil salinity. Sensitivity

analysis was done at different SI values, and RMSE
was calculated for each SI. Using the calibrated b
White and others (2000)
White and others (2000)

White and others (2000)

White and others (2000)
White and others (2000)
White and others (2000)

value, we then applied the modified model to

mangrove forests in Shenzhen and Qiongshan to
validate the model performance. Sensitivity anal-
ysis was also performed to determine the best-fit SI
Data source

and the threshold value of SI at both sites.

For the stand level simulation, species-specific
eco-physiological parameters (Table 2) were used
with the same soil salinity condition (Ss). The ef-
fects of soil salinity on growth were assumed to be
species-specific. For each monocultural stand, the b
value and the best-fit SI were derived when RMSE
0.00006
0.033

0.006

was at the minimum.

0.01
–0.6
–3.9
Value

Model outputs of NPP and LAI were compared

2500
350
2

with the observed values for each of the six man-

grove systems. Values of observed NPP for man-
Refer to appendix in Supplemental material for a list of references used for data collection.

grove forests at different locations were estimated

m s-1

m s-1
m s-1

as the sum of increases in biomass and litterfall over

Unit

DIM
DIM

MPa
MPa

a given period using data from the literature,

Pa
Pa

ignoring the biomass consumed by herbivores. In

studies where the litterfall data were not reported,
Conductance parameters (projected area basis)

Vapor pressure deficit: complete gs reduction

the average of the known values was applied. The

Leaf water potential: complete gs reduction
Vapor pressure deficit: start of gs reduction

stand-specific values of NPP from field measure-

Leaf water potential: start of gs reduction
Maximum stomatal conductance (gsmax)

ments were used as the observed NPP for the three

monocultural mangrove stands in Shenzhen. We
Ratio of shaded SLA to sunlit SLA

compared the observed accumulative NPP with the

model outputs without explicit description of the
Boundary layer conductance
Fraction of leaf N in Rubisco

site locations for the three geographically separate

mangrove forests. If multiple values of NPP were
Cuticular conductance
continued

reported for the same stand age of a given site, the

average value was calculated. For each of the study
sites, observed LAI values were calculated as the
average of the data collected from the literature,
irrespective of the stand age, and the model output
Parameter
Table 1.

of LAI was the maximum LAI during the develop-

ment of the mangrove forest. For each of the
monocultural stands in Shenzhen, observed LAI
Table 2. Values Used in the Species-Specific Eco-Physiological Parameterization for Simulation of NPP and LAI in Three Monocultural Stands in
Shenzhen, South China, Using the Biome-BGC Model
Parameter (unit) Value (data source, as listed in Appendix)

Avicennia marina Kandelia obovata Sonneratia apetala

Annual turnover rates

Annual leaf and fine root turnover 0.88 (Lin and others 1995 and 1998) 0.9 (Lin and others 1985) 0.65 (Han and others 2004)
fraction (y-1)
Annual whole-plant mortality 0.03 (Lin 1997) 0.05 (Lin and others 1985; Lu and 0.014 (Han and others 2004; Peng and
fraction (y-1) others 1988; Peng and others 2005) others 2005)
Allocation ratios
New fine root C to new leaf C (DIM) 0.2 (Lin and others 1995, 1997, 1998; 0.6 (Lin and others 1985; Zheng and Lin, 2.4 (Zan and others 2001b; Han and
Miao and others 1998) 1995; Miao and others 1998; Zan and others 2004)
others 2001b)
New stem C to new leaf C (DIM) 0.62 (Lin and others 1995, 1997, 1998; 1.1 (Lin and others 1985; Zheng and Lin 4 (Liao and others 1999, Zan and
Miao and others 1998; Wen, 1999) 1995; Liao and others 1999; Miao and others 2001b; Han and others 2004)
others 1998; Wen, 1999; Zan and others
2001b)
New live wood C to new total wood C 0.9 (Lin and others 1995, 1997, 1998; 0.2 (Lin and others 1985; Zheng and Lin 0.09 (Zan and others 2001b; Han and
(DIM) Miao and others 1998; Wen 1999) 1995; Miao and others 1998; Wen 1999; others 2004)
Zan and others 2001b)
New coarse root C to new stem C 1 (Lin and others 1995, 1997, 1998; 0.5 (Lin and others 1985; Zheng and Lin 0.25 (Zan and others 2001b; Liao and
(DIM) Miao and others 1998) 1995; Liao and others 1999; Miao and others 1999; Han and others 2004)
others 1998; Zan and others 2001b)
Canopy and conductance parameters (proportion)
C:N of leaves (g C g-1 N) 14.54 (this study) 25.54 (this study) 15.95 (this study)
Canopy average SLA (projected area 16.53 (this study) 15.75 (this study) 26.68 (this study)
basis; m2 kg-1 C)
Canopy light extinction coefficient 0.64 (this study) 0.58 (this study) 0.65 (this study)
(DIM)
Maximum stomatal conductance 0.006 (Zheng and Lin 1997; Chen and 0.009 (Lei and Lin 1995, 1996, 1998; 0.013 (Jing and others 2005; Chen and
gsmax (m s-1) others 2008) Zan and others 2001a; Chen and others 2008)
others 2008)
Leaf water potential: start of gs -1.1 (Zheng and Lin 1997; Chen and -1.7 (Zheng and Lin 1990; Lei and Lin -0.6 (Chen and others 2008)
reduction (MPa) others 2008) 1996)
Leaf water potential: complete gs -3.2 (Zheng and Lin 1997; Chen and -3.3 (Zheng and Lin 1990; Lei and Lin -3.9 (Chen and others 2008)
reduction (MPa) others 2008) 1996)
Vapor pressure deficit: start of gs 300 (Zheng and Lin 1997) 400 (Zheng and Lin 1990; Lei and Lin 350 (Jing and others 2005)
reduction (Pa) 1995, 1996, 1998)
Modeling Mangrove Forests Using Biome-BGC

Vapor pressure deficit: complete gs 2400 (Zheng and Lin 1997) 2500 (Zheng and Lin 1990; Lei and Lin 2500 (Jing and others 2005)
reduction (Pa) 1995, 1996, 1998)

Refer to appendix in Supplemental material for a list of references used for data collection.
957
958 Z. Luo and others

Model Simulations Under Predicted Future Climate

Change Scenarios
In the latest IPCC (2007) assessment on climate
change, it was reported that the global atmospheric
CO2 concentration was 379 ppm in 2005; the glo-
bal surface warming is likely to be in the range of
2–4.5C following a doubling of CO2 concentration.
Here, we started with a temperature increase of
2C, and assumed further increases in surface
temperature with increasing atmospheric CO2
concentration. A sensitivity test was performed
with temperature increases by 0.5, 1, 1.5, and 2C
and the corresponding CO2 concentration at 427.5,
475, 570, and 760 ppm, respectively. Sensitivity
analysis was also performed at these CO2 concen-
trations without interactions with temperature in-
creases. Relative changes in NPP as a result of
climate change from the present conditions to the
predicted future scenarios were calculated.

Figure 2. Mean annual temperature (A) and annual
rainfall (B) in Qiongshan, Zhanjiang and Shenzhen,
southern China.
was measured in the field, and modeled LAI
referred to the modeled LAI in the corresponding
stand ages when we carried out this study.
RESULTS
Model Performance
Application of the original Biome-BGC overesti-
mated NPP (data not shown) with large RSME
(Figures 3, 5). Using the modified Biome-BGC with
alteration to the soil hydrological process, the
modeled and observed NPP reached the best
agreement when the values of SI and b were 0.25
and 205, respectively, at the ecosystem level in
Shenzhen (Ss = 15&, Figure 3). Using the cali-
brated value 205 for b, SI was estimated to be 0.16

Figure 3. Comparison of modeled NPP and observed NPP at Shenzhen (A), and the square root of the mean of the
squared prediction errors (RMSE) for fitting the observed and the modeled NPP using different SI values (B). Filled circle
(d) shows RMSE when reaching the threshold limit value of SI (SItlv, mangrove cannot survive beyond this value), gray-
filled circle shows RMSE when reaching the best-fit stress index (SIopt), and filled club-shaped symbol (¤) shows the RMSE
under the simulation without incorporating soil water stress, that is, b = 0. See details in the text for the SIopt, SItlv, b, and
RMSE.
 Modeling Mangrove Forests Using Biome-BGC
in Zhanjiang (Ss = 18&) and 0.50 in Qiongshan
(Ss = 11&); and values of NPP were underesti-
mated to some extent by the modified Biome-BGC
in both the locations (Figure 4). Sensitive analysis
indicates that modeled and observed NPP reach the
best agreement when the value of SI is 0.31 in
Zhanjiang and 1 in Qiongshan (data not shown).
For the monocultural stands of A. marina, K.
obovata, and S. apetala in Shenzhen, the values of SI
were 0.09, 0.60, and 1, with the corresponding b
values of 200, 209, and 54, respectively, when the
modeled and observed NPP reached the best
agreement (Figure 5). Although we did not vali-
date the model prediction due to lack of sufficient
data, our calibration results showed that the mod-
ified model simulated NPP reasonably well for the
three monocultural stands in Shenzhen when the
best-fit SI was attained (Figure 5A, C, E).
The sensitivity of NPP to changes in SI differed
among the mangrove forests at different locations
as well as among the three monocultural stands in
Shenzhen (Figures 3, 5B, D, F). The threshold of SI
(that is, SItlv), an indicator of the maximum toler-
ance of mangroves to water stress, varied from 0.14
in Zhanjiang to 0.17 in Qiongshan, and to 0.22 in
Shenzhen (Figure 3, the data for sensitivity analy-
sis were not shown for Zhanjiang and Qiongshan),
and were 0.005, 0.10, and 0.065 for the stands of A.
marina, K. obovata, and S. apetala, respectively, in
Shenzhen (Figure 5B, D, F).
In the mangrove forests at the ecosystem level in
the three different locations, modeled maximum
LAI in the time interval of the corresponding stand
age were slightly overestimated in comparison with
the average of observed LAI (Figure 6); whereas in
the three monocultural stands, modeled LAI in
2005 were underestimated in comparison with the
observed value (Figure 6). Overall, modeled LAI
959
Figure 4. Observed and
modeled NPP of
mangrove forests in
Zhanjiang (A) and
Qiongshan (B) under
b = 205.
exhibited a similar trend as observed LAI with site
differences in temperature.
Sensitivity of NPP to Climate Change
Increasing atmospheric CO2 concentration had
negligible effects on NPP of mangrove forests at the
ecosystem level across the three locations (Fig-
ure 7A). The relative change in NPP was less than
7% at all CO2 levels for the Shenzhen site, and less
than 2% for the Qiongshan and Zhanjiang sites
(Figure 7A).
The three monocultural stands in Shenzhen
showed distinct responses to increasing CO2 con-
centration (Figure 7C). In K. obovata, the effects of
increasing CO2 concentration on NPP were negli-
gible; whereas in A. marina, NPP increased by 58%
at the CO2 level of 427.5 ppm, followed by a steady
and slight increase until reaching a CO2 level of
760 ppm; the stand of the exotic species, S. apetala,
showed a gradual increase of NPP with increasing
CO2 concentration, and increased by as much as
35% at a CO2 level of 760 ppm.
When coupling the increasing CO2 concentration
with a rise in air temperature, NPP markedly in-
creased across the three locations and in the three
monocultural stands (Figure 7B, D). For all the six
mangrove systems, NPP showed a logarithmic re-
sponse to increasing CO2 concentration in associa-
tion with an increase in temperature. The relative
changes of NPP with different climate change sce-
narios were comparable among the three locations,
and increased by 14% in Qiongshan, 19% in
Zhanjiang, and 18% in Shenzhen, at the CO2 level
of 760 ppm in association with a temperature in-
crease of 2C (Figure 7B). On the contrary, there
were large differences among the three monocul-
tural stands in Shenzhen; the model simulations
960 Z. Luo and others

Figure 5. Left panels

observed and modeled
NPP of three
monocultural mangrove
stands in Shenzhen,
southern China. Dotted
lines are the 1:1 line. Right
panels the square root of
the mean of the squared
prediction errors (RMSE)
for fitting the observed
and modeled NPP using
different b values in the
calibration process. Filled
circle (d) shows RMSE
when reaching the
threshold limit value of SI
(SItlv, mangrove cannot
survive beyond this
value), gray-filled circle
shows RMSE when
reaching the best-fit stress
index (SIopt), and filled
club-shaped symbol (¤)
shows the RMSE under
the simulation without
incorporating soil water
stress, that is, b = 0. See
details in the text for the
SIopt, SItlv, b, and RMSE.

indicate an increase in NPP by 68% in A. marina,
12% in K. obovata, and 31% in S. apetala, at the CO2
level of 760 ppm in association with a temperature
increase of 2C (Figure 7D). In the stand of the
exotic species, S. apetala, a concurrent increase in
both CO2 concentration and temperature increased
NPP by 10% less than did an increase in CO2
concentration alone (Figure 7C, D).
DISCUSSION
Using a modified biogeochemistry model, Biome-
BGC, NPP and LAI of mangrove forests along the
southern coast of China were analyzed under the
present climate conditions and the predicted future
climate change scenarios at the stand and ecosys-
tem levels. We considered the effective SW avail-
ability as the primary factor differentiating the
mangrove forests and the upland ecosystems. After
modifying the SW process to account for salinity-
induced SW stress, the Biome-BGC generally well
predicted the dynamics of NPP of the six mangrove
systems in our study. Our simulation results indi-
cate that different mangrove systems and species
could well differ in response to the variability in the
effective SW availability climate conditions.
Our simulation was based on the assumption
that mangrove ecosystems follow similar rules as
 Modeling Mangrove Forests Using Biome-BGC
Figure 6. Observed and modeled maximum LAI in
mangrove forests in Qiongshan, Zhanjiang, and Shenz-
hen, southern China, and three monocultural stands in
Shenzhen. All modeled LAI values were the maximum
LAI when the square root of the mean of the squared
prediction errors (RMSE) was at a minimum in fitting the
observed and modeled NPP. Vertical bars show the stan-
dard deviation.
upland ecosystems (Ellison 2002) except for the
SW process. The good agreement between the
modeled and the observed NPP using our modified
Biome-BGC shows that ecosystem-process models
developed in upland systems could perform well in
simulating the productivity of mangroves by
introducing a SW stress factor into the model. In
Biome-BGC, LAI is a principle variable controlling
biomass growth and canopy development (Churk-
ina and Running 1998; Churkina and others 2003).
Optimization of the b value, which is a factor
describing the impact of salinity, resulted in good
predictions of LAI in all the six mangrove systems.
This generally agrees with Ellison (2002) that
‘‘ecological theory developed in upland forests can
be readily applied to mangrove forests,’’ but mod-
ification of the key processes that differentiate
mangroves and upland ecosystems appears to be
necessary for this technological extension.
There is sufficient evidence that salinity is one of
the main constraints to the growth and physiolog-
ical processes in mangroves (Ball and others 1997;
Chen and Twilley 1998; Suárez and Sobrado 2000;
López-Hoffman and others 2007; Hao and others
2009). In our simulation, we used two indexes,
SIopt and SItlv, to reflect the real stress of SW and
the tolerance of mangroves to SW stress. The sim-
ulation results indicate that mangroves can be
highly susceptible to effective SW availability,
which varies with environmental conditions and
species. For instance, in Qiongshan, the produc-
961
Figure 7. Relative changes of NPP in mangrove forests in
Qiongshan, Zhanjiang, and Shenzhen, southern China,
and in three monocultural stands in Shenzhen, with
different climate change scenarios. All simulations were
performed when the square root of the mean of the
squared prediction errors (RMSE) was at a minimum in
fitting the observed and the modeled NPP under the
normal run (on temperature and CO2 concentration in-
crease).
tivity of mangrove forests did not appear to be af-
fected by effective SW availability (SIopt = 1), likely
because of the relatively low salinity (11&). This is
consistent with results from many other studies
showing that a low level of soil salinity only has
slight effects on mangrove plant performance (Ball
1988; Zheng and Lin 1992; Ball and Pidsley 1995;
Suárez and Medina 2005). In comparison, the va-
lue of SIopt was 0.31 in Zhanjiang and 0.25 in
Shenzhen, where the soil salinity was relatively
high (that is, 18& in Zhanjiang and 15& in
Shenzhen). These results further demonstrate that
the modified model could well capture the stress of
SW availability on the growth of mangroves.
Sensitivity analysis of SItlv suggests that different
mangrove systems and species can differ in toler-
ance to SW stress. A number of field studies that
compared the performance of different species
under the same soil salinity gradients showed
similar patterns (for example, Ball and others 1988;
962 Z. Luo and others
Ye and others 2005). In the monocultural K. obov-
ata and A. marina stands in Shenzhen, for example,
the values of SItlv were 0.10 and 0.005, respec-
tively, indicating possibly the greater tolerance of
A. marina to salinity-induced SW stress than
K. obovata. Controlled pot experiments show that
K. obovata (also known as K. candel, see Sheue and
others 2003) is more sensitive to soil salinity than
A. marina in the activity of ATPase, the function of
the plasma membranes, membrane potential, and
transmembrane proton gradient (Zhao and others
2004). Further evidence of the greater sensitivity to
salinity in K. obovata when compared to A. marina is
provided by a study using the d13C technique (Wei
and others 2008). Those experimental results
indirectly verify our modeling predictions of K.
obovata and A. marina in response to salinity.
However, future studies directly comparing the
response of growth performance (for example,
biomass and growth rate) of different mangrove
species to SW stress gradients may help to validate
our postulations based on the modeling study.
We found that soil salinity (Ss) alone could not
entirely explain the response of mangrove growth
to the effective SW availability. Simulations using
the same b value that was calibrated at the
Shenzhen site overestimated NPP at the other two
locations. This might be attributable to several
reasons. First, we assumed that SW potential was
linearly related to soil salinity. As mangroves are
relatively tolerant to salinity, this assumption
might mask some information on the growth re-
sponses of mangroves at either low (that is, in
Qiongshan with Ss value of 11&) or high soil
salinity (that is, in Zhanjiang with Ss value of 18&),
which emphasizes the need for more experimental
data on the relationship between soil salinity and
the effective SW availability for mangroves at dif-
ferent scales. Secondly, soil salinity may not be the
only factor that determines growth responses of
mangroves to effective SW availability. Other soil
properties, such as temperature, nutrients, aera-
tion, and chemical composition of the soil solution,
can interplay with soil salinity, confounding the
effects of soil salinity on mangrove growth. Both N
and phosphorus have been suggested to limit
mangrove growth (McKee and others 2002; Feller
and others 2003a, b). In our simulation study we
did not consider the impacts of soil nutrient avail-
ability and balances, which may account for some
biases in our model outputs. Thirdly, we used the
common generic average values of parameters for
the three ecosystem level simulations, neglecting
the possible influences of variations in species
composition and site conditions on the growth
responses of mangroves to soil salinity. The stand
level simulation of the three mangrove species
highlights the importance of species level response
to soil salinity. Lastly, because of a lack of site- and
species-specific data, we used the same set of values
for C allocation across the three locations, possibly
contributing to uncertainties in the modeled NPP
by not accounting for the impact of changes in C
allocation with species and site conditions. It has
been found that C allocation among plant parts
varies with soil salinity (Rasse and others 2005;
Cherry and others 2009).
Our modeling results demonstrate that increas-
ing atmospheric CO2 concentration only has slight
positive effects on the net C gain of mangrove
ecosystems. This differs with results obtained for
upland ecosystems in which elevated atmospheric
CO2 concentration shows marked effects on C
assimilation (Churkina and others 2003; Shaw and
others 2002; Körner and others 2005). As different
mangrove species can have distinct responses to
increasing atmospheric CO2 concentration, that is,
from neutral to a large increase, an increase in CO2
concentration under future climate conditions
might have moderate stimulating effects on the
productivity of mangroves at the ecosystem level.
Furthermore, when the ambient CO2 concentra-
tion is sufficient for photosynthesis, C assimilation
could be limited by other factors such as LN con-
centration, water use efficiency, enzyme activity,
and stomatal conductance. The contrasting effects
between elevated CO2 concentration and adverse
environmental conditions such as salinity stress
might cause the responses of mangrove plants to
climate change to significantly differ from that of
upland ecosystems. It has been previously found
that elevated CO2 concentration has little effect on
mangrove growth rate in the presence of high
salinity stress (Ball and others 1997).
In this study, we found that the impact of
increasing CO2 concentration on mangrove forests
differs with locations; the greater stimulating effects
on NPP were demonstrated for the Zhangjiang and
Shenzhen sites, where mangroves suffer greater
soil salinity stress (SI), than at the Qiongshan site
with the lowest soil salinity. This is consistent with
the findings that enhancement of NPP may in-
crease with water stress (Kimball and others 1993;
Wullschleger and others 2002; Cherry and others
2009), possibly resulting from increased water use
efficiency when plants are exposed to elevated CO2
concentration in a water-limiting growth environ-
ment (Erickson and others 2007; Robredo and
others 2007). In a brackish marsh community,
Cherry and others (2009) found that elevated
 Modeling Mangrove Forests Using Biome-BGC
CO2 stimulated biomass production of C3 plants as
a result of amelioration of negative effects of soil
salinity stress. These results, together with our
findings, indicate that the interactions between
environmental stresses (that is, water availability in
this study) and species-specific responses to
increasing CO2 concentration can greatly compli-
cate the prediction of the dynamics in wetland
plants and ecosystem processes with future climate
change (Rasse and others 2005). When considering
a concurrent increase in both atmospheric CO2
concentration and temperature, we found that the
net C assimilation capability greatly increased in all
the six mangrove systems. In general, the optimal
temperature for photosynthesis is about 30C for
plants in tropical forests, a reduction in the rates of
photosynthesis may occur at temperatures above or
below this level (Lloyd and Farquhar 2008). All our
study sites had average air temperatures far below
the optimal level for photosynthesis. An increase in
temperature may facilitate a greater rate of photo-
synthesis in mangroves of subtropical China, and
hence a greater requirement for atmospheric CO2
as an explanation for the positive interaction be-
tween temperature rise and increasing atmospheric
CO2 concentration on NPP.
Results in this study showed that the exotic
mangrove species S. apetala had much higher LAI
and annual NPP than the other two native species
in Shenzhen. Mangroves play a key role in main-
taining and shaping the unique habitat as a nursery
for biodiversity. The higher productivity of the
exotic mangrove species could profoundly change
the stand structure and energy transformation
among the ecosystem components. This potential
alteration of ecosystem structure might break the
original balance of trophic cascades (Tilman and
others 1997) and nutrient cycling (Ehrenfeld 2003;
Allison and Vitousek 2004) in native forests.
Contrary to our findings, Chen and others (2008)
found that S. apetala had fewer competitive
advantages and lower C assimilation capacities
than other native mangrove species. In our simu-
lation study, a concurrent increase in both atmo-
spheric CO2 concentration and temperature had
less effect in promoting the growth of S. apetala
than increasing atmospheric CO2 concentration
alone. We do not yet have a logical explanation for
this phenomenon. Rather, the contradictory results
stress the need for longer term studies to better
understand this species’ invasive potential as well
as C assimilation process. S. apetala has different
physiological characteristics from the native man-
grove species, such as a lower gas exchange rate
and water use efficiency (Chen and others 2008),
963
which might contribute to distinct responses to
rising temperatures and increasing atmospheric
CO2 concentrations in the future climate.
Our simulation study demonstrates that Biome-
BGC can be modified to predict the productivity
and growth of mangroves by incorporating a SW
SI. Future climate change could change the per-
formance of mangrove forests depending on local
environmental conditions and mangrove species.
This highlights the need to consider both species
and environmental conditions when devising con-
servation and management strategies. Application
of ecological models can be a useful and valuable
tool for understanding and predicting the dynamics
of mangrove forests under different environmental
conditions across different scales if the underlying
processes that differentiate mangroves with upland
ecosystems are better understood. It needs to be
noted, however, our simulation was based on the
assumption that the growth of mangrove plants
responds linearly to soil salinity, which downplays
the possible impacts of a greater range of soil
salinity at both the stand and the ecosystem levels.
Moreover, the interaction between soil salinity and
soil nutrient availability (that is, N and phospho-
rus) can have significant effects on mangrove
growth (Ball and others 1997; Feller and others
2003a, b; Rasse and others 2005; Cherry and others
2009), which needs to be explicitly addressed be-
fore a confident prediction can be made on the
dynamics of mangroves in response to changes in
climate and other environmental constraints. More
sophisticated application of modeling approaches
depends on our understanding of these topics and
the ability of models to capture these phenomena.
ACKNOWLEDGEMENTS
This study was jointly funded by the Chinese
Academy of Sciences (grant KSCX2-SW-132), the
State Forestry Administration of China (2008
04001), and the Ministry of Science and Technol-
ogy of China (2008BADB0B0302). Financial sup-
port from a joint PhD program to Zhongkui Luo
under the CSIRO-MOE (Ministry of Education,
China) Scientific Exchange Agreement is also
greatly acknowledged. We thank Luzhen Chen and
Xueqing Zeng for field assistance, Charlie Chen for
help with the graphic drawing, and Futian Man-
grove Natural Reserve for site access permission
and technical support.
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