Open Journal of Forestry
2013. Vol.3, No.4, 104-108
Published Online October 2013 in SciRes (
Copyright © 2013 SciRes.
Selection of Landscape Tree Species of Tolerant to Sulfur
Dioxide Pollution in Subtropical China*
Xizi Zhang1, Ping Zhou2, Weiqiang Zhang2, Weihua Zhang3, Yongfeng Wang2
1International Department, The Affiliated High School of South China Normal University, Guangzhou, China
2Department of Forest Ecology, Guangdong Academy of Forestry, Guangzhou, China
3Department of Forest Breeding and Silviculture, Guangdong Academy of Forestry, Guangzhou, China
Received July 8th, 2013; revised August 9th, 2013; accepted August 21st, 2013
Copyright © 2013 Xizi Zhang et al. This is an open access article distributed under the Creative Commons At-
tribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original work is properly cited.
Sulfur dioxide (SO2) is a major air pollutant, especially in developing countries. Many trees are seriously
impaired by SO2, while other species can mitigate air pollution by absorbing this gas. Planting appropriate
tree species near industrial complexes is critical for aesthetic value and pollution mitigation. In this study,
six landscape tree species typical of a subtropical area were investigated for their tolerance of SO2: Cin-
namomum camphora (L.) J. Presl., Ilex rotunda Thunb., Lysidice rhodostegia Hance, Ceiba insignis
(Kunth) P. E. Gibbs & Semir, Cassia surattensis Burm. f., and Michelia chapensis Dandy. We measured
net photosynthesis rate, stomatal conductance, leaf sulfur content, relative water content, relative proline
content, and other parameters under 1.31 mg·m3 SO2 fumigation for eight days. The results revealed that
the six species differed in their biochemical characteristics under SO2 stress. Based on these data, the
most appropriate species for planting in SO2 polluted areas was I. rotunda, because it grew normally un-
der SO2 stress and could absorb SO2.
Keywords: Sulfur Dioxide; Fumigation; Landscape Trees; Air Pollutant Tolerance; Sulfur Content; Net
Photosynthesis Rate
As one of the six major atmospheric pollutants, sulfur diox-
ide (SO2) levels are currently a health concern. Sulfur dioxide
can cause asthma and other respiratory health problems in peo-
ple, forming acid rain that can damage forests and crops, and
erode buildings. Because of industrialization and urbanization,
developing countries, especially China, suffer from increasing
concentrations of SO2 in the air. Since 1990, SO2 generated in
China has been responsible for about one-fourth of the global
emissions and more than 90% of the East Asian emissions.
From 21.7 Tg (1 Tg = 1012 g) in 2000, SO2 emissions increased
by 53% to 33.2 Tg in 2006, at an annual growth rate of 7.3%.
In 2007, Guangdong, a province in the Pearl River Delta Indus-
trial district, emitted a total of 1177 Gg of SO2, about 97% of
which was emitted by power plants and industries (Lu, 2010).
Damage to plants is an important consequence of atmos-
pheric SO2. Gaseous pollutants, particularly SO2, enter plants
through the stomata by the process of photosynthesis and res-
piration. Nitrogen dioxide (NO2) and SO2 react with water on
the cell walls inside leaves; by transfer and assimilation, the
resulting sulfurous, sulfuric, nitrous, and nitric acids, react with
other compounds and are transported to various parts of plants.
If plants are exposed to air pollutants for a long time or the
pollutant concentrations exceed a critical threshold, plants may
be injured (Jim, 2007). Plant injury is usually cumulative in
nature, reducing growth and yield and accelerating senescence.
The injury often has no overt visible symptoms aside from
some degree of chlorosis (WHO, 2000). Because of the harmful
effects of SO2, plants cannot grow robustly and some also die
in severely polluted industrial districts, creating “dead zones”
without greenery in these areas. Many studies have investigated
various aspects of the damage caused by SO2 to plants, includ-
ing photosynthesis (Swanepoel, 2007), stomatal density and func-
tion (Haworth, 2012), and carbon fixation efficiency (Chung,
Each plant is a living entity, and individuals vary in their ad-
aptations to the environment and abilities to absorb pollutants.
Suitable plants must be carefully selected for cultivation; oth-
erwise they may not thrive or may die in adverse conditions of
environmental pollution (Chung, 2010). In 2000, about 42.62
Mg of SO2 was removed from the atmosphere by urban trees in
Guangzhou. Because it costs less to remove SO2 in the air in
China compared to other developed countries, the monetary
value of this service is low (Jim, 2007). Some studies have not
only investigated the effects of air pollutants on plants, but also
evaluated suitable air pollutant-tolerant plants, for example near
a lignite-based thermal power station (Govindaraju, 2011),
industrial complexes (Lee, 2004), and a coal-fired power plant
(Sharma, 2008). The other studies assessed SO2-tolerant plants,
e.g., among wetland plants (Sha, 2010). Nevertheless, few in-
vestigations have continuously observed the responses of land-
scape tree species under high SO2 concentrations in the sub-
tropical areas of southern China. This study aims to understand
how trees adapt to the stress of SO2 and to facilitate the identi-
*Selection of high SO2 tolerance species.
fication of species that can assimilate atmospheric SO2 while
growing normally in this area.
Materials and Methods
Tree Seedlings and Growing Conditions
Six popular landscape tree species in Southern China were
selected for this experiment: Cinnamomum camphora (L.) J.
Presl, Ilex rotunda Thunb., Lysidice rhodostegia Hance, Ceiba
insignis (Kunth) P. E. Gibbs & Semir, Cassia surattensis Burm.
f. and Michelia chapensis Dandy. For each species, eighteen
healthy 1-year-old seedlings of approximately the same size
were potted into 2 kg bags (height: 12 cm, radius: 4 cm) with
loess containing 0.302 g·kg1 N, 0.3 g·kg1 P, 9.761 g·kg1 K,
21.21 mg·kg1 hydrolysable N, 4.3 mg·kg1 rapidly available P,
and 28.47 mg·kg1 rapidly available K.
The average tree height, root collar diameter, and canopy of
the trees are listed in Table 1. These seedlings were grown
under natural conditions for 1 month with regular watering to
allow their physiology to stabilize before the experiment began.
Controlled Environmental Conditions
In the experiment, three seedlings of each species (18 seed-
lings total) were placed under natural conditions with daily
watering as a control group for normal growth without treat-
ment. The other 15 samples of each species were placed to-
gether as an experimental group in a 2.0 m × 1.2 m × 1.8 m
phytotron at Guangdong Academy of Forestry, China. From
January 28 to February 5, 2013, these seedlings experienced 8
days of fumigation with 1.31 mg·m3 (= 0.5 ppm) SO2 (MIC-
SO2) with the following conditions: temperature, 15˚C - 25˚C;
relative humidity (RH), 50% - 60%; concentration of carbon
dioxide, 380 - 400 ppm; and light intensity, 600 µmol·m2·s1.
According to the result of some studies, SO2 can impact the
growth and yield of plants while reducing its foliar starch and
protein contents, pigmentation, and WUE at concentrations as
low as 0.06 - 0.15 ppm (Swanepoel, 2007). We used an un-
naturally high concentration of SO2 (1.31 mg·m3) to determine
the relative sensitivities of species for which this information
was almost unknown. According to the Pearl River Delta re-
gional air quality monitoring reports (2006, 2007, 2008, 2009,
2010), the average of the monthly maxima of hourly averages
of SO2 in Huijingcheng (Foshan), one of the most severely
polluted areas, is 0.394 mg·m3. The SO2 concentration in this
study was about three times that value. During the fumigation,
plants were watered daily.
Measurements of Biochemical Characteristics
Leaf parameters were measured at regular time intervals
during the SO2 fumigation treatment. To observe changes in
different parts of the seedlings, the first round of tests were
conducted the day before the SO2 treatment to serve as a base-
line. Then, every 2 days (on Jan 30, Feb 1, Feb 3, Feb 5), three
seedlings (replicates) of each species were removed from the
phytotron and three to four of their leaves were picked off to
measure relative water content, relative electrolytic leakage and
proline content. Five rounds of tests were done.
Relative chlorophyll content was measured with a portable
chlorophyll content meter (CCM-200 plus, OptiSciences, Hud-
son, NH, USA) on six young fully expanded leaves for each
seedling. Relative water content was determined by the follow-
ing equation:
WCfds d
RWWWW (1)
The fresh weight
W, saturated fresh weight
which was the weight after soaking the leaves in distilled water
for 24 hours, and dry weight ,which was got by drying
the fresh leaves in an oven of 80˚C overnight, were measured
by a electronic scale of 0.01 g (JJ500, G & G GmbH, Neuss,
Germany). Relative electrolytic leakage, P, was evaluated using
a conductivity meter (DSSJ-308A, China) and calculated by the
following equation:
 
10 20100%PCCCC (2)
where the conductivity of distilled water and of the sam-
ple solute before boiling
C and after boiling
C were
known. Proline content in the leaves was determined as de-
scribed by Chen & Wang (2006). To measure photosynthesis, a
portable photosynthesis system (Li-6400, LI-COR, Lincoln, NE,
USA) was used to test three healthy leaves near the top of each
seedling. To ensure the consistency of incident light intensity
and leaf surface temperature, we tested the following parame-
ters in both the control and treatment groups from 9:00 - 11:00
A.M. for 2 days after fumigation (on Feb 6 and 7): net photo
synthetic rate (Pn, µmol·m2·s1), stomatal conductance (Gs,
mol·m2·s1), transpiration rate (Tr, mmol·m2·s1), intercellular
carbon dioxide concentration (Ci, µmol·mol1), photosynthetic
Table 1.
Growth status of the plants before sulfur dioxide fumigation.
Species Code Growth parameters
Height (cm) Root collar diameter (cm) Canopy (cm2) Family
Cinnamomum camphora A 51.20 ± 0.70 0.47 ± 0.01 242.20 ± 17.16 Lauraceae
Ilex rotunda B 67.13 ± 0.80 0.66 ± 0.03 139.07 ± 11.78 Aquifoliaceae
Lysidice rhodostegia C 54.47 ± 1.06 0.59 ± 0.02 377.60 ± 46.51 Caesalpinioideae
Ceiba insignis D 87.53 ± 1.37 1.60 ± 0.05 977.60 ± 88.73 Malvaceae
Cassia surattensis E 46.73 ± 0.76 0.55 ± 0.02 225.53 ± 12.74 Caesalpinioideae
Michelia chapensis F 64.93 ± 1.07 0.70 ± 0.01 281.80 ± 24.36 Magnoliaceae
Copyright © 2013 SciRes. 105
cally active radiation (PAR, µmol·m2·s1), atmospheric carbon
dioxide concentration (Ca, µmol·mol1), atmospheric tempera-
ture (Ta, ˚C), leaf temperature (Tl, ˚C), RH (%) and water use
efficiency (WUE, µmol·mmol1). WUE was calculated as:
WUEP T (3)
The sulfur content was tested by barium sulfate turbidimetry
with various parts of the leaves selected. The ratio of leaf injury
was estimated based on the percentage of visible leaf damages.
Statistical Analysis
Statistical analyses were conducted with Microsoft Office
Excel 2007 (Redmond, WA, USA) and SPSS 16.0 (IBM, Chi-
cago, IL, USA). ANOVAs and multiple comparisons were used
to analyze significant difference of the relative proline content,
sulfur content in leaves and the net photosynthesis rate. The
tests of homogeneity were checked before multiple compari-
sons. The change of Pn (R, %), which was calculated by the
after before
 (4)
and the absolute differences between the value of sulfur content
on 0 hour and 192 hour are calculated to compare the ability of
species of tolerance to the SO2 fumigation.
In general, the sulfur content in the leaves of all six species
increased significantly before and after the treatment (P < 0.05)
Cassia surattensis had both the highest original sulfur content
in the leaves (4.49 ± 1.035 µg·g1) and the greatest increase (to
9.345 ± 1.172 µg·g1), which demonstrated its strong ability to
absorb SO2. It was followed by I. rotunda. The sulfur content in
leaves of I. rotunda was higher under SO2 fumigation than in
the control (5.155 ± 0.411 versus 2.273 ± 0.123 g·kg1). It
showed higher ability to absorb SO2 gas than C. camphora, L.
rhodostegia, C. insignis, or M. chapensis (Figure 1). The sulfur
content in the leaves of C. camphora remained low at around
0.795 ± 0.236 and only increased to 2.616 ± 0.385 g·kg1 dur-
ing the treatment. The sulfur content of L. rhodostegia was not
initially high nor did it increase much during treatment. The
low sulfur contents in C. insignis and M. chapensis showed
their weak ability to absorb SO2.
Figure 1.
Changes in the sulfur content of leaves during sulfur dioxide fumiga-
tion. A, Cinnamomum camphora; B, Ilex rotunda; C, Lysidice rho-
dostegia; D, Ceiba insignis; E, Cassia surattensis; F, Michelia chapen-
In this study, three species showed significantly
. The error bar on each point indicated standard error.
decline in
her species did not show significant changes in Pn be-
ld prevent folded proteins from denaturing,
e Pn after fumigation: L. rhodostegia, C. insignis, Cassia
surattensis (P < 0.05) (Figure 2). Ceiba insignis declined the
greatest amount in Pn, from 5.77 ± 1.33 to 0.75 ± 0.08
µmol·m1·s1, in Gs, from 0.09 ± 0.03 mol·m2·s1 to 0.02 ±
0.003 mol·m2·s1, and in Tr, from 1.23 ± 0.38 to 0.27 ± 0.06
mmol·m2·s1. In addition, WUE was reduced by fumigation
from 4.91 ± 0.35 to 2.92 ± 0.47 µmol·mmol1. Lysidice
rhodostegia had a relatively large decrease in Pn, from 3.28 ±
0.48 to 0.95 ± 0.09 µmol·m1·s1. Also, both Gs and Tr de-
creased during fumigation from 0.04 ± 0.006 to 0.02 ± 0.001
mol·m2·s1 and from 0.64 ± 0.07 to 0.35 ± 0.02 mmol·m2·s1,
respectively. WUE declined the most of the six species, from
5.13 ± 0.25 µmol·mmol1 before fumigation to 2.71 ± 0.12
µmol·mmol1 afterwards. Ci increased from 262.7 ± 4.4 to 337
± 2.5 µmol·mol1. The Pn of C. surattensis declined from 4.22 ±
0.07 to 2.90 ± 0.29 µmol·m1·s1, while its Ci increased from
299.4 ± 3.9 to 338.5 ± 1.2 µmol·mol1, and its Tr reduced mark-
edly from 1.24 ± 0.05 to 0.77 ± 0.04 mmol·m2·s1. Moreover,
its electrolytic leakage increased distinctly from 12.54 ± 0.97 to
29.62% ± 4.94%, indicating that part of the plasma membrane
was damaged by SO2 in fumigation, thus affecting its normal
The ot
re and after fumigation: C. camphora, I. rotunda, and M.
chapensis (P > 0.05) (Figure 2). The Pn of I. rotunda remained
between 3.66 ± 0.51 and 4.01 ± 0.39 µmol·m1·s1. Cinnamo-
mum camphora changed little in Pn, which ranged between 2.75
± 0.18 and 3.16 ± 0.09 µmol·m1·s1. No visible damage was
observed on the surfaces of its leaves. However, there was a
decrease in WUE, from 5.25 ± 0.59 to 4.39 ± 0.59 µmol·mmol1.
Similarly, M. chapensis did not have a significant change in Pn,
which was 3.81 ± 0.25 before and 3.34 ± 0.73 µmol·m1·s1
after fumigation.
The proline cou
teract with phospholipids to stabilize cell membranes, scav-
enge hydroxyl radicals, and function as an energy and nitrogen
source (Claussen, 2004). An increase in proline content indi-
cated that the plant was stressed (Figure 3). The proline was
vital in adjusting osmotic pressure in M. chapensis, C. insignis
and C. surattensi. The proline content of M. chapensis was the
highest among the species during fumigation, with an initial
value of 224.76 ± 50.84 µg·g1 and the highest value of 350.46
± 43.97 µg·g1 during the process of fumigation. The proline
content of C. surattensis was also high (207.25 ± 5.05 µg·g1)
and increased during fumigation to 327.00 ± 21.82 µg·g1. The
Figure 2.
ynthesis rate before and after sulfur dioxide fumigation. A,
nificant differences at 0.05.
Net photos
Cinnamomum camphora; B, Ilex rotunda; C, Lysidice rhodostegia; D,
Ceiba insignis; E, Cassia surattensis; F, Michelia chapensis. The error
bar on each point indicated standard error. The asterisks indicated sig-
Copyright © 2013 SciRes.
Figure 3.
Changes in proline content of leaves during sulfur dioxide fumiga
nnamomum camphora; B, Ilex rotunda; C, Lysidice rhodos-
20.94 ± 12.49
The results could be umental design, because
rown near areas with severe air pollution (Go-
tion. A, Ci
tegia; D, Ceiba insignis; E, Cassia surattensis; F, Michelia chapensis.
The error bar on each point indicated standard error.
proline content of C. insignis ranged between 1
and 226.16 ± 18.57 µg·g, presenting a significant increase (P
< 0.05) under SO2 stress, which corresponded with its remarka-
bly decreased Pn. After fumigation, some leaves were dehy-
drated, yellowing, coiled and chlorotic, and many dehisced, and
the ratio of leaf injury was 100%, which showed it was highly
stressed. The proline content in the leaves of I. rotunda was
relatively low, ranging from 51.44 ± 4.91 to 84.88 ± 7.97
µg·g1. Its Gs increased after fumigation from 0.07 ± 0.012 to
0.10 ± 0.014 mol·m2·s1. Some leaves had rusty piebald
patches or dehisced under SO2. The ratio of leaf injury was
30%. The proline content of L. rhodostegia was not initially
high nor did it increase much during treatment.
These six species could be divided into four types based on
their responses to SO fumigation, as shown in
2Figure 4. The
horizontal axis is the change of Pn (R, %). The smaller the R
value, the lesser the impact on Pn and the better the plant can
adapt to the SO2 environment. The vertical axis shows the ab-
solute values of the differences in leaf sulfur content (g·kg1)
between 0 and 192 hours of fumigation; the larger this value,
the greater the tree's capacity to absorb SO2.
sed for environ
y indicated that these six species have different tolerances
and could be planted for different purposes, as summarized in
Figure 4. Ilex rotunda, in the first quadrant, was the most ap-
propriate of the six species to be planted near industry com-
plexes and along roads, because it could absorb SO2 while still
growing robustly. To clean the air, C. surattensis, in the second
quadrant, was a good choice for its strong SO2 absorption abil-
ity. In contrast, if the goal was simply greenery near factories to
improve aesthetics, the species in the fourth quadrant, C. cam-
phora and M. chapensis, could be selected due to their healthy
growing condition under high concentration of sulfur dioxide.
The net photosynthesis of the plants in the third quadrant, L.
rhodostegia and C. insignis, decreased a relatively large amount
after fumigation, showing their poor growth condition under
SO2 stress. They absorbed almost no SO2, so did not improve
the environment. Thus, these two species were not highly tol-
erant to SO2.
Many studies have investigated which pollutant-tolerant
plants can be g
Figure 4.
Categorization of the six tree species based on their responses to SO
ess. A, C. camphora; B, I. rotunda; C, L. rhodostegi a; D, C.
2008). However, since
ey chose the sampling sites and took the sample leaves to test
rticulates well. Nevertheless, according to our re-
the P of this
t both
pollutant str
insignis; E, C. surattensis; F, M. chapensis.
vindaraju, 2011; Lee, 2004; Sharma,
different parameters, the variables, such as the concentration of
pollutants and the existence of particles, could not be really
controlled. The actual reason for a given species' biochemical
characteristics could not be well explained, because they might
have resulted from any number of factors. Also, climate factors,
such as temperature, latitude, or humidity, might have affected
the plants, so the results might not apply to other places or sea-
sons. In this experiment, the environmental variables were all
controlled, so that the impact of SO2 on plants was isolated and
Jim (2007) demonstrates that C. camphora tolerates SO2,
NOx and pa
lts, although C. camphora could survive in a severely pol-
luted area, it could not extract atmospheric SO2 to improve air
quality. However, C. camphora did not change substantially in
either Pn or sulfur content in the leaves, nor in the values of
other measurements such as chlorophyll relative content, rela-
tive water content, and electrolytic leakage. Because this ex-
periment focused only on the effects of SO2, the tolerance of C.
camphora to other air pollutants is still unknown. A previous
study (Lyu, 2003) showed that C. camphora can absorb a small
amount of SO2, consistent with the results of this experiment.
In addition, this species has a strong ability to extract hydrogen
fluoride and is suitable for mildly polluted areas.
Wen et al. (2003) found that L. rhodostegia was highly sen-
sitive to air pollutants. The authors concluded that n
ecies was reduced by pollutant stress, and the amount of de-
crease was much greater than the decrease in Tr. Thus, the plant
suffered both weaker growth due to less photosynthesis and
excessive water loss. That observation accorded with our data.
Although Wen et al. investigated multiple air pollutants and we
only studied the effects of SO2, both studies concluded that L.
rhodostegia can neither resist nor adapt to air pollution.
Surprisingly, the data for I. rotunda differed between our
study and that of Wen et al. (2003). The latter showed tha
n and Gs decreased nearly 40% under air pollution, while Tr
declined by about 50%. In contrast, we found out that Gs in-
creased and the values of the other measurements did not
change significantly. These differences may result from the
different environments of the two experiments; the other air
pollutants in the study of Wen et al. might offset the effects of
SO2 and change the response of I. rotunda, leading to different
Copyright © 2013 SciRes. 107
Copyright © 2013 SciRes.
areas according to our results, it should receive more
In this study, the perfommon landscape tree
species under SO fumied to help select trees
This study was the Guangdong
Forestry Science n Project (2010
Chen, J. X., & Wang, Xeffects of stress on the
free proline content iogical experiment ma-
Because I. rotunda was the most suitable species for SO2
ention to fully elucidate the mechanisms by which it adapts
to SO2 stress. We believe that other species with similar behav-
ioral responses can be found and planted to mitigate air pollu-
tion. In addition, more parameters of C. camphora can be tested
in order to further understand the adaptation of it under sulfur
dioxide. This species remains poorly understood because most
of the data did not change significantly or show obvious trends
in this experiment. Therefore, future experiments must be con-
ducted to investigate the effects on plants of other air pollutants,
individually and in combination, to permit the selection of the
optimal species for severely polluted regions. To fully under-
stand how plants change under pollution stress, more parame-
ters should be evaluated, including stomatal density, chloro-
phyll fluorescence, and carbon fixation efficiency. To identify
more air pollution tolerant plants, other common subtropical
species, which were also mentioned in Wen et al. (2003), like
Ficus microcarpa, Camellia japonica L., and Tutcheria spect-
abilis (Benth.) Dunn, can also be tested.
ormance of six c
igation was stud
r greenbelts near industrial complexes in subtropical area,
especially where SO2 is the main emission. Ilex rotunda, which
remained green and extracted a great amount of SO2, is rec-
ommended as a key species for greenbelts. Cassia surattensis
can be used to improve air quality in polluted areas. Both C.
camphora and M. chapensis are also recommended for planting
in severely polluted areas because of their high aesthetic values.
From an economic and management perspective, L. rhodoste-
gia and C. insignis are more suitable for cleaner, less-polluted
environments. Integrating different tree species into a landscape
can both contribute to greenery near factories and maintain
biodiversity. As more studies are conducted on the appropriate
species to grow in heavily industrial areas, the problem of air
pollution can be effectively controlled.
supported by funding from
and Technology Innovatio
JCX012-01) and the Guangzhou Science and Technology
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