Selection of Landscape Tree Species of Tolerant to Sulfur Dioxide Pollution in Subtropical China

doi:10.4236/ojf.2013.34017

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Open Journal of Forestry

2013. Vol.3, No.4, 104-108

Published Online October 2013 in SciRes (http://www.scirp.org/journal/ojf) http://dx.doi.org/10.4236/ojf.2013.34017

104

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

Email: zhoupinger@qq.com

Received July 8th, 2013; revised August 9th, 2013; accepted August 21st, 2013

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·m−3 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

Introduction

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,

2010).

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.

X. Z. ZHANG ET AL.

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·kg−1 N, 0.3 g·kg−1 P, 9.761 g·kg−1 K,

21.21 mg·kg−1 hydrolysable N, 4.3 mg·kg−1 rapidly available P,

and 28.47 mg·kg−1 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·m−3 (= 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·m−2·s−1.

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·m−3) 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·m−3. 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:







100%

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·m−2·s−1), stomatal conductance (Gs,

mol·m−2·s−1), transpiration rate (Tr, mmol·m−2·s−1), intercellular

carbon dioxide concentration (Ci, µmol·mol−1), 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

X. Z. ZHANG ET AL.

cally active radiation (PAR, µmol·m−2·s−1), atmospheric carbon

dioxide concentration (Ca, µmol·mol−1), atmospheric tempera-

ture (Ta, ˚C), leaf temperature (Tl, ˚C), RH (%) and water use

efficiency (WUE, µmol·mmol−1). 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

equation:











after before

before

100%



 (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.

Results

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·g−1) and the greatest increase (to

9.345 ± 1.172 µg·g−1), 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·kg−1). 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·kg−1 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-

sis

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·m−1·s−1, in Gs, from 0.09 ± 0.03 mol·m−2·s−1 to 0.02 ±

0.003 mol·m−2·s−1, and in Tr, from 1.23 ± 0.38 to 0.27 ± 0.06

mmol·m−2·s−1. In addition, WUE was reduced by fumigation

from 4.91 ± 0.35 to 2.92 ± 0.47 µmol·mmol−1. Lysidice

rhodostegia had a relatively large decrease in Pn, from 3.28 ±

0.48 to 0.95 ± 0.09 µmol·m−1·s−1. Also, both Gs and Tr de-

creased during fumigation from 0.04 ± 0.006 to 0.02 ± 0.001

mol·m−2·s−1 and from 0.64 ± 0.07 to 0.35 ± 0.02 mmol·m−2·s−1,

respectively. WUE declined the most of the six species, from

5.13 ± 0.25 µmol·mmol−1 before fumigation to 2.71 ± 0.12

µmol·mmol−1 afterwards. Ci increased from 262.7 ± 4.4 to 337

± 2.5 µmol·mol−1. The Pn of C. surattensis declined from 4.22 ±

0.07 to 2.90 ± 0.29 µmol·m−1·s−1, while its Ci increased from

299.4 ± 3.9 to 338.5 ± 1.2 µmol·mol−1, and its Tr reduced mark-

edly from 1.24 ± 0.05 to 0.77 ± 0.04 mmol·m−2·s−1. 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

growth.

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·m−1·s−1. Cinnamo-

mum camphora changed little in Pn, which ranged between 2.75

± 0.18 and 3.16 ± 0.09 µmol·m−1·s−1. 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·mmol−1.

Similarly, M. chapensis did not have a significant change in Pn,

which was 3.81 ± 0.25 before and 3.34 ± 0.73 µmol·m−1·s−1

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·g−1 and the highest value of 350.46

± 43.97 µg·g−1 during the process of fumigation. The proline

content of C. surattensis was also high (207.25 ± 5.05 µg·g−1)

and increased during fumigation to 327.00 ± 21.82 µg·g−1. 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-

106

X. Z. ZHANG ET AL.

Figure 3.

Changes in proline content of leaves during sulfur dioxide fumiga

nnamomum camphora; B, Ilex rotunda; C, Lysidice rhodos-

20.94 ± 12.49

−1

The results could be umental design, because

the

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·g−1. Its Gs increased after fumigation from 0.07 ± 0.012 to

0.10 ± 0.014 mol·m−2·s−1. 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·kg−1)

between 0 and 192 hours of fumigation; the larger this value,

the greater the tree's capacity to absorb SO2.

Discussion

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

repeatable.

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

X. Z. ZHANG ET AL.

108

areas according to our results, it should receive more

att

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

NCES

Chen, J. X., & Wang, Xeffects of stress on the

free proline content iogical experiment ma-

results.

Because I. rotunda was the most suitable species for SO2

polluted

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.

Conclusion

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.

Acknowledgemen

supported by funding from

and Technology Innovatio

JCX012-01) and the Guangzhou Science and Technology

Project (2012Y2-00011), China.

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