Environment, Development and Sustainability (2021) 23:1579–1600

https://doi.org/10.1007/s10668-020-00640-1

Assessment of air pollution tolerance index (APTI) for some

ornamental woody species in green space of humid
temperate region (Rasht, Iran)

Sara Ghafari1 · Behzad Kaviani2 · Shahram Sedaghathoor2 ·

Mohammad Sadegh Allahyari3

Received: 11 August 2019 / Accepted: 10 February 2020 / Published online: 21 February 2020
© Springer Nature B.V. 2020

Abstract
The green space of parks with its vegetation population of trees and shrubs plays a key
role in air purification and the absorption of air pollutions, thereby contributing to the alle-
viation of environmental pollutions. The present factorial experiment was carried out in
urban parks with 18 treatments. The leaf samples of 18 ornamental species were collected
in two sites [(1) the margin and (2) the downtown] of Rasht city in north of Iran. Then,
they were subjected to the measurement of leaf relative water content, total chlorophyll
content, leaf extract pH, and ascorbic acid content to evaluate their air pollution tolerance
index (APTI). The tolerance of the species was assessed by two methods: the comparison
of their APTI with the average APTI of all species and the use of a constant APTI as a
standard. The results showed that the species differed in their tolerance in different sites.
Among the studied 18 species, Yucca filamentosa and Berberis thunbergii were identified
as air pollution-tolerant species, so they are recommended for the use in parks. Yucca had
an APTI of 78.24 and Berberis had an APTI of 67.56. The lowest APTI was obtained from
Fraxinus excesio and Ligustrum texanum.

Keywords Shrubs · APTI · Yucca filamentosa · Pollution tolerant

1 Introduction

Urban areas have been faced with massive development of urbanization, construction, and
transportation in the recent decade. There is heavy traffic around urban parks in the city of
Rasht every day with a lot of traffic jams during the day, especially at morning and evening
rush times, so that the neighborhood of most parks looks like parking spaces in most hours
of the day and is suffering from air pollution. Parks are an attraction for a lot of tourists and

* Behzad Kaviani
[email protected]
1
Ornamental Plants, Rasht Branch, Islamic Azad University, Rasht, Iran
2
Department of Horticulture, Rasht Branch, Islamic Azad University, Rasht, Iran
3
Department of Agricultural Management, Rasht Branch, Islamic Azad University, Rasht, Iran

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Vol.:(0123456789)
1580 S. Ghafari et al.

an exercise field for many local people. Given the high humidity in cities like Rasht, it is
more likely to have acid rains, so air pollution in these regions is more dangerous than in
arid regions and these chemical changes are more likely to affect plant species that are sen-
sitive to air pollution (Mohammadi 2014).
Plants are regarded as environment purifiers in the design of urban green spaces. Among
plant species, trees and shrubs are important components in urban green spaces. Not only
do they purify air, water, and soil but they also contribute to beautifying urban and indus-
trial regions. It has been documented that excessive accumulation of most pollutants in the
exhaust gas of cars hurts plants (Grantz et al. 2003). Nitrogen oxides, sulfur oxides, carbon
monoxide, suspended particles, hydrocarbons, and carbon dioxide are among the pollutant
greenhouse gasses that are emitted into the atmosphere and change its chemical composi-
tion by increasing its gases, volatiles, and suspended particles (Rai et al. 2011). It has been
reported that acid rain induced by air pollution is harmful to plants (Velikova et al. 2000).
Since plant leaves are the most sensitive part to air pollution, they can be used as a good
indicator in attempts to assess pollution (Shafiq et al. 2009). It has been reported that pol-
lutants make a lot of physiological and biochemical changes in plants, and by the study of
these indicators, one can estimate the resistance of plants against pollutants (Zhang et al.
2016). The impacts of air pollutants have been examined on the parameters of ascorbic
acid (Hoque et al. 2007), chlorophyll (Flowers et al. 2007), leaf extract pH (Klumpp et al.
2000), and relative water content (RWC) of leaves (Rao 1979). Leaf RWC contributes to
preserving the physiological exchange of plants exposed to pollution stress and protecting
them against drought stress, especially when plant transpiration rate is high (Dedio 1975).
Chlorophyll plays a crucial role in plant physiology and is perceived as a major indicator
of environmental stresses imposed to plants with a critical role to play in adjusting photo-
synthesis-induced synthesis (Onwurah et al. 2007). In addition to being a strong reducer,
ascorbic acid plays a critical role in the synthesis of cell walls, defensive system, and cell
division (Conklin 2001). Leaf extract pH of plants has a close correlation with air pollu-
­ O2 content (Swami and Chauhan 2015). Plants with higher leaf extract
tion, especially its S
pH are more capable of the uptake of ­SO2 and ­NO2 (Zou 2007).
Researchers have revealed that no single parameter can provide us with a clear image
of the variations arising from air pollution, but four parameters should be used to identify
the tolerance of plant species (Escobedo et al. 2008; Singh et al. 1991). Some researchers
argue that plants exposed to air pollution can be divided into tolerant, moderately toler-
ant, moderately sensitive, and sensitive in terms of biochemical indicators, physiological
responses, growth, and flowering (Seyyednejad et al. 2011a). The present study aims to
select plant species from a pool of 18 ornamental plant species that are more pollution tol-
erant in order to provide a new approach to developing urban landscapes.

2 Materials and methods

2.1 Study site

Rasht, the capital city of Guilan province, is located in the Guilan plain to the south of
the Caspian Sea, Iran. It is located at the latitude of 37° 16′ N and the longitude of 49°
36′ E, covering an area of about 180 km2 with moderate and humid climate and an annual
rainfall rate of over 1300 mm. The study focused on parks in the margin and downtown
of Rasht, selected for their common plant species abundance making it possible to make

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Assessment of air pollution tolerance index (APTI) for some… 1581

comparisons. The marginal site included two parks with light traffic: Mafakher Park
(7000 m2), or the so-called Chamarsara Park, in the western part of Rasht (Lat. 37° 27′ N,
Long. 49° 56′ E) in the vicinity of the Gohar Rood River and Daneshjoo Park (2000 m2)
located at the entrance of the city in western part (Lat. 37° 16′ N, Long. 49° 35′ E) in
the vicinity of the Eynak lagoon (the second most important boating river of Iran). The
downtown site included Mohtasham Park (144,000 m2) which is the oldest park of the city
located in the southern part (Lat. 37°26′ N, Long. 49° 58′ E) in the vicinity of the Gohar
Rood River (the river polluted with municipal sewage) and Mellat Park (120,000 m2)
which is the second biggest park of the city after Mohtasham Park, located in the northern
part of the city (Lat. 37° 29′ N, Long. 49° 59′ E). These two parks are in the crowded parts
of the city with heavy traffic so that the neighborhood of the parks looks like a parking
space in most hours of the day (Fig. 1).

2.2 Sampling of ornamental species

Out of 112 tree, shrub, and hedge species identified in the study sites, 43 species were assessed
to be dominant in terms of importance and growth capability against the criteria that were
considered by the experts. Of these 43 species, leaves were sampled from 18 plant species
existing in both marginal and downtown sites (Table 1) from July 17 to July 21, 2018. The
samples were taken from mature trees and shrubs that were in the same conditions in terms
of age, vegetative growth, height, trunk diameter, chest, and crown asymmetry and were fully
exposed to sunlight. Then, they were sent to a laboratory for the measurement of their physi-
ological and biochemical parameters.

Fig. 1  The map of the studied parks (https​://www.googl​e.com/maps/@37.27100​27,49.57928​72,2772m​/

data=!3m1!1e3)

13
1582 S. Ghafari et al.

Table 1  The list of the common plant species in the studied sites and their primary characteristics
Species no. Scientific name Latin name Life form Life cycle Leaf type

1 Lagerstroemia indica Crepe myrtle Shrub Perennial Broad leaf

2 Chaenomeles japonica Japanese quince Shrub Perennial Broad leaf
3 Quercus castaneifolia Chestnut-leaved oak Tree Perennial Broad leaf
4 Acer negundo Box elder Tree Perennial Broad leaf
5 Laurus nobilis Bay leaf Shrub Perennial Broad leaf
6 Ligustrum texanum Ivory silk tree lilac Shrub Perennial Broad leaf
7 Acer Pseudoplatanus Sycamore maple Tree Perennial Broad leaf
8 Cercis silquastrum Judas-tree Shrub Perennial Broad leaf
9 Zelkowva carpinifolia Japanese zelkova Tree Perennial Broad leaf
10 Berberis thunbergii Japanese barberry Shrub Perennial Broad leaf
11 Fraxinus excesio Weeping ash Tree Perennial Broad leaf
12 Euonymus japonicus Green spire Shrub Perennial Broad leaf
13 Pyracantha coccinaea Red firethorn Shrub Perennial Broad leaf
14 Ligustrum vulgare Common privet Shrub Perennial Broad leaf
15 Hibiscus syriacus Rose of sharon Shrub Perennial Broad leaf
16 Prunus ceracifera Cherry plum Shrub Perennial Broad leaf
17 Cedrus deodara Himalaya cedar Tree Perennial Needle
18 Yuccea filamentosa Adam’s needle Shrub Perennial Broad leaf

2.3 Measurement of physiological and biochemical parameters

2.3.1 Leaf relative water content (RWC)

0.5 g of developed leaves of each plant (FW) was floated in distilled water in darkness at 4 °C
for 24 h. Then, it was dried with a filter paper and its turgidity weight (T) was determined.
Then, it was oven-dried at 75 °C for 24 h to determine its dry weight (DW) (Ritchie et al.
1990). RWC was obtained from the following equation:
[ ]
(FW − DW)
RWC = × 100. (1)
(TW − DW)

2.3.2 Leaf extract pH

4 g of fresh leaf was grind and soaked in 40 ml of deionized water. Then, it was centrifuged
at 7000 rpm at 25 °C for 20 min to determine its pH with a pH meter (Liu and Ding 2008a).

2.3.3 Total chlorophyll content (TCH)

0.4 g of fresh weight was ground by liquid nitrogen. It was, then, extracted by 10 ml of
acetone 80%, adjusted to 20 ml, centrifuged at 4500 rpm (F = 34.9 g) for 15 min, and sub-
jected to a spectrophotometer to be read at 645 and 663 nm (Lichtenthaler 1987). Then, the
following equation was used to find out chlorophyll contents:

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Assessment of air pollution tolerance index (APTI) for some… 1583

Chl.a (mg/ml) = (12.25 A663.2 − 2.79A646.8 ) (2)

Chl.b (mg/ml) = (21.50A646.8 − 5.10A663.2 ) (3)

TCH (mg/ml) = Chl.a + Chl.b (4)

in which Chl.a, Chl.b, and TCH denote chlorophyll a, chlorophyll b, and total chlorophyll
contents, respectively.

2.3.4 Ascorbic acid (AA)

It was measured by the method of titration with 2,6-dichlorophenolindophenol (DCIP)

(Helrich 1990).

2.3.5 Air pollution tolerance index (APTI)

APTI of the plant species was measured by four parameters of RWC, pH, TCH, and AA for
all samples taken from the study sites (Singh and Rao 1983) using the following equation:
[ ]
AA × (TCH + pH) + RWC
APTI = (5)
10
in which AA is in mg/g, TCH is in mg/g, and RWC is in percentage.

2.3.6 APTI classification

In the first classification method, the tolerance of each ornamental plant species was com-
pared with the APTI averaged across the all studied plant species plus one standard devi-
ation (SD) based on Liu et al. (1983)’s study. In this procedure, the plant species were
divided into four tolerance levels:

Level (1)—tolerant (T) species APTI > mean APTI + SD

Level (2)—moderately tolerant (MT) species mean APTI < APTI < mean APTI + SD
Level (3)—intermediate (I) species mean APTI − SD < APTI < mean APTI
Level (4)—sensitive (S) species APTI < mean APTI – SD

In the second classification method, the tolerance level of each ornamental plant was
directly obtained by comparing its APTI with index values described in Ogunkunle et al.
(2015), by which tolerance was divided into three levels:

Level (1) < 11 sensitive (S)

Level (2) 12–16 = intermediate (I)
Level (3) > 17 = tolerant (T)

13
1584 S. Ghafari et al.

2.4 Data analysis

Data were statistically analyzed by the MSTATC software package, and the graphs were
drawn in MS-Excel 2010.

3 Results and discussion

3.1 Air pollutants in Rasht

For a 3.5-month period before the initiation of leaf sampling, the concentration of
­PM2.5, ­PM10, ­SO2, ­NO2, ­O3, and CO was recorded with respect to the database of air
pollutants prepared by Air Pollution Monitoring Station of the Rasht Office of Environ-
ment (Table 2). Overall, these pollutants were found to be in the concentration order of
­PM2.5 > PM10 > O3 > NO2 > CO > SO2.

3.2 Relative water content (RWC)

Leaf RWC is a critical physiological parameter that is directly affected by air pollution.
RWC was significantly influenced by the simple effect of site and plant species at the
p < 0.01 and by their interaction effect at the p < 0.05 level (Table 3). It ranged from 38.1
to 92.28% in all leaf samples (Table 4). The highest RWC was 92.28% observed in the
leaf samples of Yuccea filamentosa, which was significantly (p ≤ 0.05) higher than that of
Cedrus deodara and Laurus nobilis in the marginal site and that of Lagerstroemia indica,
C. deodara, Y. filamentosa, and Hibiscus syriacus in the downtown site. The lowest RWC
of 38.1% was recorded by the leaf samples of Quercus castaneifolia in the downtown site,
which was lower than that of Zelkowva carpinifolia (46.99%) and L. indica (46.77) in the
marginal site. As well, 66.6% of plant species in the downtown site including H. syriacus,
C. deodara, L. indica, Chaenomeles japonica, B. thunbergii, Prunus ceracifera, Pyracan-
tha coccinaea, Fraxinus excesio, Ligustrum vulgare, C. silquastrum, L. texanum, and Z.
carpinifolia and 33.4% of them in the marginal site including Y. filamentosa, L. nobilis,
Acer negundo, Euonymus japonicus, A. pseudoplatanus, and Q. castaneifolia had higher
average RWC than their counterparts in the alternate site (Fig. 2).
It has been reported that higher humidity of the Milu Park site than two other sites,
i.e., Bai-Zhi-Fang Riverfront and Yue-Ge-Zhuang Bridge as well as Milu Deers wetland
in Beijing, has been involved in lower temperatures and higher relative humidity and
increasing leaf RWC of most common species (Zhang et al. 2016). The temperature
difference between the urban heat island of Rasht city (the Sabzemeydan Park site) and

Table 2  The concentration range of air pollutants in Rasht city

Pollutants PM2.5 (mg/m3) PM10 (mg/m3) SO2 (mg/m3) NO2 (mg/m3) O3 (mg/m3) CO (mg/m3)

Maximum 94 69 13 32 54 30
Minimum 28 15 8 19 11 4
Daily average 68.53 68.36 11.23 24.71 28.53 45.18
(March 21–
July 16, 2018)

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Assessment of air pollution tolerance index (APTI) for some… 1585

Table 3  Analysis of variance for the effect of different treatments on the traits of the studied ornamental
trees and shrubs
Source of variables df Means of squares
Leaf RWC​ TCH Vitamin C Leaf extract pH APTI

Site 1 762.57** 0.261ns 0.043ns 0.532* 5.769ns

Ornamental species 17 753.914** 10.281** 32.185** 6.150*** 2037.318**
Site × species 17 198.032* 7.37** 1.514** 0.232** 154.773**
Experimental error 70 90.256 1.813 0.315 0.103 13.612
C.V. 14.07 27.58 54.47 6.33 44.58

** and * show significance of the means at p < 0.01 and p < 0.05, respectively

the surrounding parts (the marginal site) amounts to 2–5.5 °C under minimum temper-
ature conditions and to 3–5.6 °C under maximum temperature conditions (Ramezani
and Mohammadi 2011). In our study, other factors were involved in lower temperature
and higher relative humidity of the marginal site including the flowing of the Gohar
Rood River and the Eynak lagoon in the vicinity of the marginal site (the Mafakher
and Daneshjoo park sites), less temperature difference between the marginal site and
the urban heat island when compared to that of the downtown site, and the presence of
taller buildings and less urban asphalt around the marginal site than in the downtown
site. All these factors can be enumerated as the likely reasons for higher RWC of the
leaves of Y. filamentosa in the marginal site. It has been documented that plants (e.g.,
Elaeocarpus sylvestris) exhibit an increase in leaf stomatal density in the case of expo-
sure to air pollution (Liao et al. 2011), and this increases leaf water content (Jiang et al.
1997). This higher water content contributes to maintaining the physiological balance
and enhancing stress tolerance of plants (Agarwal and Tiwari 1997). We found that Y.
filamentosa in the marginal site had the highest pollution tolerance among all studied
species. Leaf water content variation reflects the impact of air pollution and the sen-
sitivity of the plant. The mechanism of plants to cope with and survive through stress
is to maintain the water content of their tissues. Huang et al. (2004) reported the loss
of water content in the tissue of rye and Poa (sensitive plants) and no change in that of
fescue (resistant plant) in creosote-contaminated soil. In a similar finding, we observed
the loss of intra-tissue water content in Q. castaneifolia (sensitive plant) in the down-
town site and its increase in Y. filamentosa (resistant plant) in the marginal site. Amini
et al. (2009) found the highest leaf RWC (66.09%) in Cupressus arizonica and the low-
est (83.44%) in mulberry and noted that the highest leaf RWC was an indicator of the
plant’s better resistance against water stress. Some researchers (Enete et al. 2013; Jyothi
and Jaya 2010) have reported that plants with higher RWC are resistant to air pollution.
In our study, the highest RWC was related to Y. filamentosa in the marginal site and the
lowest to Q. castaneifolia in the downtown site, implying that with this characteristic, Y.
filamentosa is resistant not only to air pollution but possibly to water stress.
According to Dedio (1975), leaf RWC is involved in maintaining the physiological bal-
ance of pollution-exposed plants. In our research, Y. filamentosa in the marginal site, H.
syriacus in the downtown site, and L. nobilis in the marginal site had high leaf RWC, which
could contribute to keeping their physiological balance. The loss of RWC is a symptom
of physiological disorder in plants induced by pollution (Ramakrishnaiah and Somashekar

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 Table 4  Means comparison for the interaction of site and ornamental species for the measured traits
1586

Treatments Leaf RWC (mg/g) TCH (mg/g) Vitamin C Leaf extract pH APTI
Ornamental Marginal site Downtown Marginal site Downtown Marginal site Downtown Marginal site Downtown Marginal site Downtown site

13
species site site site site

Lagerstroemia 68.14 dj 82.27 ad 6.52 ad 5.53 cg 0.037 g 0.05 g 5.43 fj 5.44 ej 0.26 e 0.47 e
indica
Chaenomeles 47.77 mn 47.99 bg 2.87 ik 4.14 fj 0.09 g 0.09 g 5.51 dj 5.42 gj 0.72 e 0.8 e
japonica
Quercus cas- 56.8 im 38.1 n 6.76 ad 6.8 ad 0.13 g 0.32 g 5.63 di 5.27 hk 1.009 e 1.65 e
taneifolia
Acer negundo 73.71 bg 69.34 cj 3.36 gk 6.68 ad 0.36 g 0.48 fg 3.35 pq 3.8 op 2.89 e 3.85 e
Laurus nobilis 84.62 ac 77.22 af 5.18 cg 5.35 cg 0.29 g 0.22 g 6.01 ad 6.34 ab 2.73 e 1.99 e
Ligustrum 51.77 kn 62.1 fm 3.62 fk 5.1 ch 0.037 g 0.041 g 5.21 ik 5.3 hk 0.21 e 0.3 e
texanum
Acer Pseudo- 61.8 fm 59.65 gm 8.43 a 5.62 bf 0.43 fg 0.27 g 5.55 dj 5.96 ae 3.31 e 1.98 e
platanus
Cercis sil- 49.96 ln 64.62 fl 3.66 fk 3.53 fk 0.25 g 0.14 g 4.47 mn 4.32 no 1.95 e 1.05 e
quastrum
Zelkowva 49.99 mn 54.08 jm 7.74 ab 3.82 ek 0.14 g 0.15 g 5.61 di 5.74 ch 0.98 e 1.99 e
carpinifolia
Berberis 67.73 dj 74.51 bg 3.81 ek 2.04 jk 6.8 c 9.67 a 2.72 rs 2.52 s 42.76 c 67.56 b
thunbergii
Fraxinus 66.75 ek 71.71 ci 2.94 hk 5.86 be 0.03 g 0.04 g 5.53 dj 5.37 gk 0.22 e 0.36 e
excesio
Euonymus 70.45 ci 64.34 fl 1.78 k 4.66 di 0.23 g 0.15 g 5.86 bg 5.95 af 1.84 e 1.08 e
japonicas
Pyracantha 57.15 im 72.91 ch 8.6 a 4.2 ej 0.09 g 0.03 g 5.04 jl 5.32 hk 0.62 e 0.3 e
coccinaea
Ligustrum 58.02 hm 69.36 cj 4.68 di 5.61 bf 0.15 g 0.08 g 5.16 ik 5.48 ej 1.06 e 0.68 e
vulgare
S. Ghafari et al.
 Table 4  (continued)
Treatments Leaf RWC (mg/g) TCH (mg/g) Vitamin C Leaf extract pH APTI
Ornamental Marginal site Downtown Marginal site Downtown Marginal site Downtown Marginal site Downtown Marginal site Downtown site
species site site site site

Hibiscus syri- 75.36 bf 88.49 ab 4.76 di 4.85 di 0.09 g 0.08 g 6.39 a 6.21 ac 0.88 e 0.85 e
acus
Prunus 57.76 hm 72.92 ch 2.72 ik 4.21 ej 1.7 e 1.29 ef 4.86 km 6.25 ac 11.26 d 13.33 d
ceracifera
Cedrus deo- 81.4 ae 81.53 ad 5.64 bf 7.1 ac 0.23 g 0.202 g 3.28 pq 3.16 qr 2.12 e 1.87 e
dara
Yuccea fila- 92.28 a 84 ac 3.83 ek 3.56 fk 7.77 b 4.82 d 4.56 ln 4.86 km 78.24 a 44.6 c
mentosa
Assessment of air pollution tolerance index (APTI) for some…
1587

13
1588 S. Ghafari et al.

Fig. 2  The interaction effect of site and species on leaf RWC of the ornamental trees and shrubs

2003; Kiran Kumar et al. 2016). The significant reduction of leaf RWC of spinaches that
were exposed to pollutants for the longest time reflected the response of the plants to pol-
lution stress, the stomatal closure, and the resulting loss of leaf transpiration rate (Kohan
et al. 2018). Swami et al. (2004) pointed to the reduction of leaf RWC of plant species due
to the impact of pollutants on the transpiration rate of the leaves. We observed the same
impact in Q. castaneifolia in the downtown site, which may show the reduction of RWC by
stomatal closure. In the study of Rashidi et al. (2017), the reduction of leaf RWC of Fraxi-
nus rotundifolia Mill reflected the plant’s response to pollution stress and its resistance to
adverse environmental conditions, which is inconsistent with our finding of the significant
loss of leaf RWC of Q. castaneifolia in the downtown site, C. japonica and Z. carpinifolia
in the marginal site, and the susceptibility of these trees to pollution stress.

3.3 Leaf extract pH

Air pollutants adversely affect physiological processes including pH in plants and impair
their resistance to other stresses (Rai et al. 2011). The simple and interaction effects of
ornamental species and parks were significant on leaf extract pH (Table 3). When the effect
of site was considered, the pH of the studied leaf samples varied in the range of 2.52–6.39,
while 55.5% of the samples had a pH in the range of 5–6 (Table 4). The highest leaf pH
was 6.39 observed in the leaves of H. syriacus in the marginal site followed by L. nobilis in
the marginal site (6.01) and H. syriacus, P. ceracifera, and L. nobilis in the downtown site
(6.21, 6.25, and 6.34, respectively). The lowest leaf extract pH was related to B. thunbergii
in the downtown and marginal sites (2.52 and 2.72, respectively), which was lower than
that of A. negundo in the downtown site (3.8), A. negundo and C. deodara in the marginal
site (3.35 and 3.28, respectively) and C. deodara in the downtown site (3.16). As well,
61.1% of species (L. nobilis, P. ceracifera, A. pseudoplatanus, E. japonicus, Z. carpinifo-
lia, L. indica, P. coccinaea, L. texanum, L. vulgare, Y. filamentosa, and A. negundo) in the
downtown site and 38.9% of them (H. syriacus, Q. castaneifolia, F. excesio, C. japonica,
C. silquastrum, C. deodara, and B. thunbergii) in the marginal site had higher mean leaf
pH than their counterparts in the alternate site (Fig. 3).
The pH adjustment has a critical role to play in the mobilization of vesicle and com-
pounds inside the cells (Verweij et al. 2008). When plants are exposed to air pollutants
(especially ­SO2), a great deal of ­H+ is produced in their intercellular fluid to react with ­SO2.

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Assessment of air pollution tolerance index (APTI) for some… 1589

This ­H+ may produce H ­ 2SO4, which will reduce pH. This is consistent with our results and
the significant loss of pH of B. thunbergii in the marginal and downtown sites (Zhen 2000).
Consequently, the higher the leaf extract pH is, the better the ability of the plants to absorb
­SO2 and N­ O2 will be (Zou 2007). This is in agreement with our research and the significant
increase in pH of H. syriacus in the marginal site. High pH is effective in enhancing the
productivity of the transformation of hexoses into ascorbic acid (Escobedo et al. 2008).
The increased pH of leaf extract may improve the efficiency of hexose conversion into vita-
min C (Escobedo et al. 2008; Pasqualini et al. 2001). This is dissimilar to our finding of
the significant increase in leaf extract pH of H. syriacus in the marginal site and that of L.
nobilis and P. ceracifera in the downtown site. The efficiency of pH is severely dependent
upon leaf extract pH. Photosynthesis is reduced in plants when their pH is lower (Türk and
Wirth 1975). We obtained similar results for chlorophyll of B. thunbergii in the downtown
site so that their chlorophyll content was decreased with the decrease in pH. The results of
Zhang et al. (2016) on the loss of average leaf extract pH of the plant species in Bai-Zhi-
Fang site with higher S ­ O2 than the other two sites in Beijing reveal the importance of pH in
dictating the susceptibility/resistance of plants to pollutant concentrations. We found that
the average pH of the ornamental plant species in the downtown site (about 61.1%) sur-
passes that in the marginal site (38.9%). So, leaf extract pH can be suggested as an indica-
tor of local air pollution. Amini et al. (2009) observed the highest leaf extract pH (7.15) in
mulberry and the lowest (5.09) in Laurus nobilis and reported that high pH was a sign of
plant resistance to pollution stress.
Higher pH of plants improves their resistance to air pollution (Prajapati and Tripathi
2008), which confirms our results about the significant increase in P. ceracifera showing its
intermediate or moderate resistance to pollution. The reduction of leaf extract pH in plants
exposed to pollution stress (particularly S ­ O2 and ­NO2) has been reported to reflect stomatal
susceptibility to pollutants and their rapid closure in response to stress (Uka and Chukwuka
2014; Swami et al. 2004; Lacher 1995). Our result about the significant reduction of pH in
B. thunbergii in the marginal and downtown sites shows its pollution resistance trait and is
in agreement with some studies. But, Scholz and Reck (1977) reported a dissimilar finding
about the correlation of low leaf extract pH with pollution susceptibility. In Enete et al.
(2013), air pollution-susceptible plants had higher pH than resistant plants. We found a
similar result when we observed a significant increase in pH of H. syriacus in the marginal
site and L. nobilis in the downtown site, reflecting their susceptibility to pollution stress.

Fig. 3  The interaction effects of site and species on leaf extract pH of ornamental trees and shrubs

13
1590 S. Ghafari et al.

3.4 Total chlorophyll content (TCH)

In general, air pollution is very influential on plant health and its TCH so that TCH is
reduced as air pollution is aggravated (Wu 2006). The results showed that the simple
effect of ornamental species and the interaction effect of site and species were significant
(p < 0.01) on TCH, but the simple effect of site was insignificant (Table 3). TCH of leaf
samples varied in the range of 1.78–8.6 mg/g FW (Table 4). The highest TCH (8.6 mg/g
FW) was related to P. coccinaea in the marginal site and the lowest (1.78 mg/g FW) to
E. japonicus in the same site. Also, 55.5% of species (C. deodara, Q. castaneifolia, A.
negundo, L. nobilis, L. texanum, F. excesio, L. vulgare, H. syriacus, E. japonicus, P.
ceracifera, and C. japonica, respectively) in the downtown site and 44.5% (P. coccinaea,
A. pseudoplatanus, Z. carpinifolia, L. indica, L. vulgare, Y. filamentosa, B. thunbergii, and
C. silquastrum, respectively) in the marginal site had higher TCH than their counterparts in
the alternate studied site (Fig. 4).
Similarly, Zhang et al. (2016) enumerated species with higher leaf TCH as plants more
tolerant to ­SO2 pollution and those with very low TCH in their leaves or needles as plants
susceptible to S­ O2 pollution. They also stated that the decrease in TCH can be considered
an indicator of the increasing rate of ­SO2 and ­O3. In our study, P. coccinaea, A. pseudopla-
tanus, and Z. carpinifolia in the marginal site had higher leaf TCH, so they can be listed
among more pollution-tolerant species. E. japonicus and P. ceracifera in the marginal site
and B. thunbergii in the downtown site had very low TCH, implying that they are pollution
susceptible. This factor alone is consistent with Zhang et al. (2016). Severe air pollution
reduces leaf TCH of plants (Su et al. 2002; Du et al. 2007). We observed the lowest TCH
in P. ceracifera in the marginal site, B. thunbergii in the downtown site, and E. japoni-
cus in the marginal site, respectively. Similar results showed a decrease in the chlorophyll
content of Prosopis guliflira in response to air pollution so that the species was named
the most susceptible, whereas the chlorophyll contents of Eucalyptus camaldulensis and
Albizia lebbeck were increased, so these two species were pollution resistant (Assadi et al.
2011; Seyyednejad et al. 2011b). Chlorophyll retention and increase in exposure to air pol-
lution can signify plant tolerance and resistance to air pollution (Singh and Verma 2007).
Our results revealed that TCH was increased in some species (P. coccinaea, A. pseudo-
platanus, and Z. carpinifolia) in the marginal site. Kammerbauer and Dick (2000) showed
that exhaust gases increased the synthesis of photosynthetically active pigments by 15%.
They attributed chlorophyll increase to N ­ O2 uptake and the increase in nitrogen precursors,

Fig. 4  The interaction effect of site and species on leaf total chlorophyll content of ornamental trees and
shrubs

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Assessment of air pollution tolerance index (APTI) for some… 1591

which is in agreement with our result of the increased TCH of A. pseudoplatanus in the
marginal site.
Amini et al. (2009) reported the highest TCH (2.25) in the leaves of C. arizonica and
the lowest (0.86) in the leaves of F. excesio and stated that the increase in TCH was a
sign of plant tolerance of pollution. Our results showed that A. pseudoplatanus had the
highest and B. thunbergii had the lowest TCH. This reflects that TCH alone cannot be a
sign of pollution tolerance. Air pollution is much more dangerous in cities like Rasht that
have higher humidity than drier regions because of the risk of acidic rains. These chemi-
cal changes are likely in air pollution-sensitive plants in the present study. Patidar et al.
(2016) reported that the decrease in TCH due to vehicle-emitted pollution was mainly
associated with the damage of reactive oxygen species to chloroplast. The greatest loss of
plant pigments was observed in strawberries exposed to high concentrations of CO, ­SO2,
and ­NO2 (Muneer et al. 2014). Also, air pollution reduced photosynthesizing pigments and
disrupted the photosystem II function in tobacco (Hui Yun 2007). The same reduction of
photosynthesizing pigments, as well as the disruption of bioprocesses, has been reported in
Pinus nigra and Pinus elderic (Olumi et al. 2016). Joshi and Swami (2009) revealed that
air pollution reduced the concentration of photosynthesizing pigments in six tree species.
Also, exposure to air pollutant peroxyacetyl nitrate reduced photosynthesizing pigments
of Petunia hybrida ‘White Champion’ and ‘Blue Champion’ (Oka et al. 2003) which is
consistent with our result of the significant decrease in TCH of P. ceracifera in the mar-
ginal site, B. thunbergii in the downtown site, and E. japonicus in the marginal site. Lau-
enorth and Dodd (1981) attributed chlorophyll degradation to the presence of ­NO2 and ­SO2
greenhouse gases in the air and their effect on plant metabolism. Consistent with them, we
observed the descending trend of TCH in P. ceracifera in the marginal site, B. thunbergii
in the downtown site, and E. japonicus in the marginal site, which may be related to chlo-
rophyll degradation by ­NO2 and ­SO2 existing in the air of Rasht and its impact on plant
metabolism and their conversion into pheophytin.

3.5 Ascorbic acid (AA)

Ascorbic acid is involved in the synthesis of cell walls, defensive system, and cell division
(Conklin 2001) and can improve plant tolerance of air pollutants (Ghosh et al. 2014). The
simple effect of ornamental plant and the interaction of site and ornamental species was
significant (p < 0.01) on vitamin C content, but the simple effect of site was insignificant
(Table 3). Considering the effect of site, vitamin C content of leaf samples varied from
0.03 to 9.67 mg/g FW and it was less than 1 mg/g FW in 88.8% of the samples (Table 4).
The highest vitamin C content of 9.67 mg/g FW was related to B. thunbergii in the down-
town site, and the lowest (0.03 mg/g FW) was observed in the leaves of F. excesio in the
marginal site. Also, 61.1% of species (Y. filamentosa, P. ceracifera, A. pseudoplatanus, L.
nobilis, C. silquastrum, C. deodara, E. japonicus, L. vulgare, H. syriacus, C. japonica,
and P. coccinaea, respectively) in the marginal site and 38.9% (B. thunbergii, A. negundo,
Q. castaneifolia, Z. carpinifolia, L. indica, F. excesio, and L. texanum, respectively) in the
downtown site had higher average vitamin C content than their counterparts in the alterna-
tive sites (Fig. 5).
As already mentioned, plant species with higher leaf ascorbic acid content may be
more tolerant of air pollution due to the antioxidant property of ascorbic acid, whereas
plant species with lower ascorbic acid content may be more susceptible to air pollution.

13
1592 S. Ghafari et al.

Fig. 5  The interaction effect of site and species on leaf vitamin C content of trees and shrubs

Y. filamentosa, B. thunbergii, and P. ceracifera in the urban sites had higher ascorbic acid
content and were likely to be more tolerant of air pollution. Higher ascorbic acid content
is a sign of more tolerance of ­SO2 pollution (Chaudhary and Rao 1977; Varshney and
Varshney 1984). Ascorbic acid can improve the tolerance of plants living in polluted air
(Zhang et al. 2016). This is consistent with our finding that Y. filamentosa and B. thun-
bergii had higher vitamin C content among ornamental species and were more pollution
tolerant. Zhang et al. (2016) reported the reduction of vitamin C content due to pollution
in 13 common plant species of BZF and YGZ sites in Beijing and the increase in this trait
in three common plant species. They enumerated the first group to be pollution-sensitive
species and the second to be pollution-resistant species. Prajapati and Tripathi (2008), also,
reported that an increase in vitamin C antioxidant is a sign of the increased resistance of
the plant to pollution stress. In our study, among the 18 studied plant species, pollution
induced a decrease in vitamin C content in 16 species and an increase in its content in Y.
filamentosa and B. thunbergii in the urban sites. So, the first 16 species formed the pol-
lution-sensitive species and the second two species were found to be pollution-resistant.
Amini et al. (2009) found that the leaves of C. arizonica had the highest vitamin C content
(4.41) and the leaves of F. excesio had the lowest one (0.705). This is in agreement with
our finding that F. excesio had the lowest vitamin C content. Enete et al. (2013) noted the
high levels of ascorbic acid in the leaves of trees than in the leaves of shrubs and stated that
trees were pollution resistant and shrubs were pollution sensitive. But, we observed higher
ascorbic acid in the leaves of shrubs than in the leaves of trees, so shrubs were found to be
more pollution resistant than trees.

3.6 Air pollution tolerance index (APTI)

Air pollution tolerance index (APTI) reflects a plant’s ability to tolerate air pollution. Plants
with higher APTI can act as a source of pollution alleviation, whereas plants with lower
APTI can be an indicator of air pollution level (Singh and Rao 1983). The simple effects of
ornamental species and the interaction of site and ornamental species were significant on
APTI at the p < 0.01 level, but the simple effect of site was insignificant (Table 3). APTI
of leaf samples varied in the range of 0.21–78.24. It was lower than 11 in 83.3% of the
samples and lower than 1 in 38.8% of them (Table 4). The highest APTI was related to the
leaves of Y. filamentosa in the marginal site with an APTI of 78.24, and the second highest

13
Assessment of air pollution tolerance index (APTI) for some… 1593

Fig. 6  The interaction effect of site and species on APTI of ornamental trees and shrubs

was observed in the leaves of B. thunbergii in the downtown site with an APTI of 56.56.
The lowest were 0.21, 0.22, and 0.26 observed in L. texanum, F. excesio, and L. indica in
the marginal site, respectively. Also, it was revealed that 50% of species in the marginal site
(Y. filamentosa, A. pseudoplatanus, L. nobilis, C. deodara, C. silquastrum, E. japonicus, L.
vulgare, H. syriacus, and P. coccinaea) and 50% in the downtown site (B. thunbergii, P.
ceracifera, A. negundo, Z. carpinifolia, Q. castaneifolia, C. japonica, L. indica, F. excesio,
and L. texanum) had higher mean APTI than their counterparts in the alternate site (Fig. 6).

3.7 APTI classification and tolerance degree

The APTI level was categorized for 18 studied ornamental species in the marginal and
downtown sites in two ways (Table 5). APTI of the species was compared with four indi-
ces listed in Liu et al. (1983) in the first method and with three indices enumerated by
Ogunkunle et al. (2015) in the second method (Zhang et al. 2016). In the first method,
considering the environmental conditions and irrespective of the tolerance of the studied
species, the ornamental plants were divided up into tolerant (T), moderately tolerant (MT),
intermediate (I), and sensitive (S). The second method was used to select ‘real’ tolerant
ornamental species irrespective of the environmental conditions. The plants categorized
in the tolerant (T) group by the second method could be regarded as resistant and could
be used in green spaces of parks. The second method placed all species in intermediate
(I) or sensitive (S) groups but B. thunbergii, P. ceracifera, and Y. filamentosa. This was
re-tested by the first method. For example, all plant species but B. thunbergii and Y. fila-
mentosa were categorized in sensitive group in the marginal site by the second method. So,
it was necessary to re-categorize them by the first method. In reclassification, A. negundo,
L. nobilis, and A. pseudoplatanus were found to be moderately tolerant. P. ceracifera that
was categorized in MT group by the first method can also be used in parks. The application
of the second method to the plant species in the downtown site showed that B. thunbergii
and Y. filamentosa were in the tolerant group, P. ceracifera was in the intermediate group,
and most other ornamental species were in the sensitive group. Reclassification by the first
method showed that A. negundo was in intermediate group and P. ceracifera in moderately
tolerant group. P. ceracifera, which was found to be moderately tolerant by the first method
can also be proposed. In the marginal and downtown sites, B. thunbergii and Y. filamentosa
showed high tolerance so that they were placed in T group by both methods.
Different classification methods categorized some species in the sampling sites in dif-
ferent tolerance groups. For example, the first and second method categorized A. negundo

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Table 5  The results of two methods used to classify APTI of the plant species in the studied sites

13
Treatments Marginal ­sitea Marginal ­siteb Downtown ­sitea Downtown ­siteb Grade in literature References

Lagerstroemia indica S S S S T, MT, I, S Zhang et al. (2016)

Chaenomeles japonica S S S S
Quercus castaneifolia S S S S
Acer negundo I S I S
Laurus nobilis I S S S
Ligustrum texanum S S S S T Zhang et al. (2016)
Acer Pseudoplatanus I S S S
Cercis silquastrum S S S S
Zelkowva carpinifolia S S S S
Berberis thunbergii T T T T
Fraxinus excesio S S S S T, MT, I, S Zhang et al. (2016)
Euonymus japonicus S S S S MT, I, S Zhang et al. (2016)
Pyracantha coccinaea S S S S
Ligustrum vulgare S S S S MT, I, S Zhang et al. (2016)
Hibiscus syriacus S S S S
Prunus ceracifera MT S MT I I, S Zhang et al. (2016)
Cedrus deodara S S S S
Yuccea filamentosa T T T T T Kermani et al. (2017)

S sensitive, I intermediate, MT moderately tolerant, T tolerant

a
Classification by Liu et al. (1983)’s method
b
Classification by Ogunkunle et al. (2015)’s method
S. Ghafari et al.
Assessment of air pollution tolerance index (APTI) for some… 1595

in the intermediate and sensitive groups in both marginal and downtown sites, respectively.
The second method categorized all plant species in the marginal site, except for B. thunber-
gii and Y. filamentosa, in sensitive group. Even if a single classification method was used,
a few species would be placed in different tolerance groups in different sites. For instance,
L. nobilis and A. pseudoplatanus were classified in intermediate group in the marginal
site but in sensitive group in the downtown site by the first method. This may be associ-
ated with the differences in air pollution level, temperature, moisture, the presence of the
river and the Eynak lagoon, or other factors underlying the parameters that influence the
APTI formula. Ailanthus altissima and locust were evaluated to be moderately tolerant by
the assessment of four physiological parameters of APTI (Liu and Ding 2008a), but the
method of enzyme superoxide dismutase (SOD) activity showed that they were sensitive
(Han et al. 1995).
In this case, Liu and Ding (2008a) state that the use of four biochemical and physi-
ological parameters to evaluate air tolerance gives more reliable results than the use of
only one biochemical parameters like SOD. In another study, it was found that mulberry
trees had the highest dust precipitation on their leaves and the highest APTI among nine
plant species in the green belt in the east of Isfahan, Iran and that the APTI method out-
performed other methods in identifying resistant species (Abed Esfahan et al. 2011). Enete
et al. (2013) reported that APTI was a suitable instrument to select ornamental plants and
shrubs to reduce urban heat island in Enugu. They recommended ornamental shrubs with
lower APTI (sensitive species) as a bioindicator of urban air pollution and trees with higher
APTI (resistant species) for planting in green spaces of polluted area. This is in agreement
with our results for the city of Rasht as it has an urban heat island too. In separate studies,
some ornamental species were categorized in MT/T group by the first method in a steel
factory in Beijing (Liu and Ding 2008b), in MT group by inspection of individual plant
species (Zhou 1996), and in S group by SOD value in Liaoning University in Northeastern
China (Han et al. 1995). This supports our result on A. pseudoplatanus and L. nobilis.
Amini et al. (2009) found the highest APTI in the leaves of C. arizonica and mulberry
(10.07 and 9.65, respectively) and the lowest in the leaves of F. excesio (7.35). Zhang et al.
(2016) reported that F. excesio was sensitive, which is consistent with our assessment of F.
excesio as an air pollution susceptible species. The parameters of AA, pH, TCH, and leaf
RWC separately give contradictory results for plant species. For instance, amaranth was
found to be pollution sensitive with one parameter (Han et al. 1995) but pollution tolerant
with another (Zhou 1996). This is similar to our finding that B. thunbergii was found to be
pollution tolerant by the parameter AA but pollution sensitive by the parameters TCH and
pH. Different plant species vary in their susceptibility to air pollution remarkably. Plants
with high or low APTI can be recognized as tolerant or sensitive species (Singh and Rao
1983). Similarly, we found that Y. filamentosa was pollution tolerant and F. excesio was
pollution sensitive.
According to Liu and Ding (2008a), the higher APTI of shrubs than trees showed
more resistance of shrubs than trees to air pollution. In the study of Yan-Ju and Hui
(2008), ornamental shrubs were more pollution tolerant than trees. Likewise, the shrubs
Y. filamentosa and F. excesio were found to be pollution tolerant in our study. Liu and
Ding (2008a) recommended the use of plants ranked as resistant and the avoidance of
those ranked as sensitive, which is in agreement with the reasons for our classification
(Zhang et al. 2016). Assadi et al. (2011) pointed out that plants may differ significantly
in their responses to air pollutants and this difference may be dictated by factors such as
differences in pollutant concentrations and their temporal distribution, genetic origins,
physiological activity, meteorological parameters, nutritional status of plants, and other

13
1596 S. Ghafari et al.

environmental factors. In a study in Beijing by Liu et al. (1983) and Ogunkunle et al.
(2015), Euonymus japonicus was found to be in S group in the BZF site, in I group in
the YGZ site, and in MT group in the MLP site. This contradiction may be attributed to
differences in temperature, moisture, the presence of wetland, four parameters of APTI,
and air pollution level (Zhang et al. 2016). Mickler et al. (2003) mentioned leaf area
expansion, nutritional status, and environmental parameters as the main factors in the
analysis of pollution tolerance. Enete et al. (2013) noted that study site, difference in
expansion area, climate change, and climate diversity were the possible reasons for the
inconsistency of the results of APTI among plants species.

4 Conclusions

The present study utilized two assessment methods to determine the tolerance of certain
plant species to air pollution at sites located at the margin and downtown of the city. B.
thunbergii and Y. filamentosa are recommended as the first choice and P. ceracifera as
the second choice for the marginal site. L. nobilis, A. negundo, and A. pseudoplatanus
should be selected with cautious, but L. indica, C. japonica, Q. castaneifolia, L. texa-
num, C. silquastrum, Z. carpinifolia, F. excesio, E. japonicus, P. coccinaea, L. vulgare,
H. syriacus, and C. deodara should be avoided. The first choice for the downtown site
should be B. thunbergii and Y. filamentosa, and the second choice should be P. ceracif-
era. When selecting A. negundo, we should be cautious, but it is not recommended to
use L. indica, C. japonica, Q. castaneifolia, L. nobilis, L. texanum, A. pseudoplatanus,
C. silquastrum, Z. carpinifolia, F. excesio, E. japonicus, P. coccinaea, L. vulgare, H.
syriacus, and C. deodara. It is suggested to widely use Y. filamentosa and B. thunber-
gii across the city because it was categorized in tolerant group in all sites. Overall, the
ornamental species that were classified in tolerant or moderately tolerant groups can
be used in the design of green spaces in the marginal and downtown site. The meth-
ods used here proved to be very useful. Some species were classified in quite different
tolerance groups in different sites, possibly emanating from the differences in the traf-
fic around the sites, air pollution, and environmental conditions. It is recommended to
focus on supplementary methods in the future research by studying physiological and
biochemical parameters across different months or studying them across different plant
species including cover plants or runners.

Compliance with ethical standards

Conflict of interest All authors have read and approved the final manuscript. The authors have no conflict of
interest.

Research involving human participants and/or animals For this type of study, formal consent is not required.

Informed consent Informed consent was obtained from all individual participants included in the study.

Ethics approval This article does not contain any studies with human participants or animals performed by
any of the authors.

13
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