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Case Study

Tree Bark as a Bioindicator for Arsenic and Heavy Metal Air


Pollution in Rajnandgaon District, Chhattisgarh, India
Khageshwar Singh Patel 1; Ankit Yadav 2; Yaman Kumar Sahu 3; Lesia Lata, Ph.D. 4;
Huber Milosh 5; Warren T. Corns, Ph.D. 6; and Pablo Martín-Ramos 7
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Abstract: Rajnandgaon district (Chhattisgarh, India) faces serious arsenic pollution problems. Tree bark could be a valuable indicator of
As and heavy metals air contamination. In this study, road dust was sampled in 13 locations, finding As, Cr, Mn, Cu, Zn, and Pb concen-
trations in the 165–329 , 107–151 , 704–998 , 43–84, 61–117 , and 26–62 mg · kg−1 range, respectively. The sensitivity of bark from 32 tree
species—widespread in the area of study—was assessed with a view to their utilization as bioindicators, and correlations between contam-
inant contents in the road dust and in the tree barks were calculated. The high accumulation of pollutants and strong correlations attained
suggest that M. indica, P. sylvestris, E. globulus, D. sissoo, A. marmelos, and F. benghalensis may be promising choices for As, Cr, Cu, Mn,
Zn, and Pb air quality monitoring, respectively. DOI: 10.1061/(ASCE)HZ.2153-5515.0000475. © 2019 American Society of Civil
Engineers.
Author keywords: Arsenic; Bioindicator; Heavy metals; Road dust; Tree bark.

Introduction Tree bark is a good bioindicator of the aforementioned pollu-


tants because its outer part consists of dead material, which is
Road traffic emissions significantly contribute to the particulate neither physiologically active nor has interfering growth cycles
matter concentration in the urban atmosphere (Harrison et al. 2004; or metabolic processes. Therefore, it comes very close to an ideal
Pant and Harrison 2013), and the emitted particles have been re- accumulation indicator (Walkenhorst et al. 1993).
ported to penetrate human organs (Kumar et al. 2013). Road dust In India, the states of Assam, Bihar, Chhattisgarh, Jharkhand,
contamination with As and heavy metals has been reported in Manipur, Uttar Pradesh, and West Bengal have been reported to be
several regions (Lu et al. 2009; Wei et al. 2010; Atiemo et al. 2011; the most affected by arsenic contamination (Shanmugapriya et al.
Li et al. 2015; Nazzal et al. 2014). Emissions of arsenic-bearing 2015). The environment of Ambagarh tehsil, in Rajnandgaon district
dust are of particular concern for human populations living in the (Chhattisgarh, India), has been reported to be seriously contaminated
proximity of an emission source (Martin et al. 2014) provided that with As at hazardous levels due to geogenic sources (Acharya et al.
the inorganic arsenic compounds are classified as Group-1 carcin- 2001, 2005; Patel et al. 2005). In this work, arsenic and heavy metals
ogens associated with lung, bladder, kidney, skin, liver, and pros- contamination in this area has been determined both in highway road
tate cancer (IARC 2012). Heavy metals, such as Cr, Mn, Fe, Cu, dust and in bark samples from various tree species, assessing the
Zn, Cd, and Pb, are also hazardous air pollutants, which feature a sensitivity of the latter to diagnose this problem.
cumulative behavior (WHO 2007).

Materials and Methods


1
Professor Emeritus, School of Studies in Chemistry, Pt. Ravishankar
Shukla Univ., Raipur 492010, India (corresponding author). Email:
Study Area
patelkhagrshwarsingh@gmail.com
2
Ph.D. Student, School of Studies in Environmental Science, Pt. Thirteen villages (Arajkund, Bihari Khurd, Dhaditola, Joratarai,
Ravishankar Shukla Univ., Raipur 492010, India. Email: yadavankit Jadutola, Kaudikasa, Mangatola, Meregaon, Murethitola, Netamtola,
.yadav9@gmail.com Sangali, Sonsaitola, and Thailitola) of an arsenic prone area in
3
Ph.D. Student, School of Studies in Chemistry, Pt. Ravishankar Shukla Ambagarh tehsil, Rajnandgaon district, Chhattisgarh, India
Univ., Raipur 492010, India. Email: yamankumarsahu8@gmail.com
4 (20.78209°N 80.74117°E), were selected for the proposed investiga-
Dept. of Soil Science, Maria Curie-Sklodowska Univ., Lublin 20-031,
Poland. Email: lata@poczta.umcs.lublin.pl tion (Fig. 1).
5
Professor, Dept. of Geology, Maria Curie-Sklodowska Univ., Lublin
20-031, Poland. Email: miloh@interia.pl
6
PS Analytical Ltd., Arthur House, Unit 11 Cray Fields Industrial Sample Collection
Estate, Orpington, Kent BR5 3HP, UK. Email: wtc@psanalytical.com Eighteen road dust samples (0.5 kg) from 13 villages were man-
7
Professor, Dept. of Agricultural and Environmental Sciences, Instituto ually collected in February 2017 from the main highways with
de Investigación en Ciencias Ambientales de Aragón, Univ. of Zaragoza, a Teflon spoon. They were kept in plastic bags. Bark samples
Carretera de Cuarte, s/n, Huesca 22071, Spain. ORCID: https://orcid.org
(0.5 kg) from the three most heavily polluted villages (Kaudikasa,
/0000-0003-2713-2786. Email: pmr@unizar.es
Note. This manuscript was submitted on March 15, 2019; approved on Sonsaitola, and Dhaditola) were collected. Seventeen tree species
June 28, 2019; published online on September 13, 2019. Discussion period of ages above 10 years [Aegle marmelos (Corrêa), Acacia nilotica
open until February 13, 2020; separate discussions must be submitted for (Schumach. & Thonn.), Azadirachta indica (A. Juss.), Butea mono-
individual papers. This paper is part of the Journal of Hazardous, Toxic, sperma (Lam.) Taub., Dalbergia sissoo (Roxb.), Diospyros mela-
and Radioactive Waste, © ASCE, ISSN 2153-5493. noxylon (Roxb.), Eucalyptus globulus (Labill.), Ficus benghalensis

© ASCE 05019006-1 J. Hazard. Toxic Radioact. Waste

J. Hazard. Toxic Radioact. Waste, 2020, 24(1): 05019006


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Fig. 1. Sampling locations in Ambagarh tehsil, Rajnandgaon, Chhattisgarh, India.

L., Ficus religiosa L., Madhuca longifolia (J. F. Macbr.), a 0.2 g of sample and subjected to shaking overnight so that the
Mangifera indica L., Phoenix sylvestris (Roxb.), Shorea robusta acid and the sample completely reacted, thus ensuring good As
(C. F. Gaertn.), Tamarindus indica L., Tectona grandis L.f., extraction. The next day, the sample was removed from the shaker
Terminalia chebula (Retz.), and Ziziphus mauritiana (Lam.)], and put in the centrifuge for 10 min. The extract was filtered
widespread in the Kaudikasa village, were manually collected in using 25 mm × 0.45 μm polytetrafluoroethylene (PTFE) disc fil-
February 2017. However, the bark of fifteen species (i.e., Acacia ters. A 2 mL aliquot was taken and diluted to 10 mL with Na3 PO4
nilotica, Ficus benghalensis L., Madhuca longifolia, Azadirachta (previously filtered), which was the mobile phase for HPLC. The
indica, Butea monosperma, Ficus religiosa, Shorea robusta, levels of As(III), As(V), monomethyl arsonic acid (MMA) and
Dalbergia sissoo, Diospyros melanoxylon, Ziziphus mauritiana, dimethyl arsinic acid (DMA) present in the sample were then de-
and Mangifera indica) and two (Ziziphus mauritiana and Mangi- tected by the HPLC-AFS (PSA 10.825 Isocratic LC System, PS
fera indica) that grow in the Sonsaitola and Dhaditola village were Analytical, Orpington/UK).
collected in May 2019 for the comparison studies. The collected
bark samples were packed in plastic bags and transported to the QA/QC Analysis
lab for further studies.
The surface of road where samples were to be collected was
cleaned by removing particles; i.e., stone, debris, and plant materi-
Analyses
als. Surface road dust (0–10 cm depth) was collected over an area of
The dried processed solid samples (0.25 g) were digested in acid 10 × 10 cm2 into a plastic bag. The sample was mixed thoroughly
(3 mL HCl and 1 mL HNO3 ) in a closed system with a microwave and sun dried for 1 week in a glass room. The matured bark samples
digestion system (P/T MARS CEM, Varian, Palo Alto, California). were collected manually. They were washed with de-ionized water
The acid extract was used for metal monitoring. The total arsenic and sun dried for 1 week.
content in the samples was analyzed with a cold vapor−atomic Samples were crushed into powder form, and particles of
absorption spectrophotometer (SpectrAA 55B, Varian, Palo Alto, mesh size ≤0.1 mm (≤100 μm) were sieved out into a glass bottle.
California). Other heavy metals (viz. Cr, Mn, Cu, Zn, Cd, and Pb) Samples were dried in a hot oven overnight at 50°C. Samples were
were analyzed by an induced coupled plasma–atomic emission spec- then digested with analytical reagent (AR)-grade acids (Sigma-
trophotometry (ICP-OES-700-ES, Varian, Palo Alto, California). Aldrich, St. Louis) for elemental analysis. Two reference materials
were used to control data quality: NCS DC 73382 CRM soil
Arsenic Speciation (Beijing) and NIST-1515 apple leaf (Sigma-Aldrich, St. Louis).

High-pressure liquid chromatography–hydride generation–atomic


Statistical Analyses
fluorescence spectrometry (HPLC-HG-AFS) was used for the
quantification of arsenic species, according to the following pro- Three analysis of each sample were carried out for each of the ana-
cedure. In a centrifuge tube, 5 mL of 0.5M H3 PO4 were added to lytical techniques. The range, mean value, and standard deviation

© ASCE 05019006-2 J. Hazard. Toxic Radioact. Waste

J. Hazard. Toxic Radioact. Waste, 2020, 24(1): 05019006


Table 1. Concentration (mg · kg−1 ) of total, organic, and inorganic As species in road dust samples obtained by HPLC-AFS
Arsenic species found by HPLC-AFS methoda
Serial Calculated Extraction
Number total As As(III) DMA MMA As(V) Total As efficiency (100%)
1 31.2  0.5 0.06 — — 6.07 6.13 19.6
2 85.1  4.4 — — — 9.47 9.47 11.1
3 48.5  0.1 — — — 5.50 5.50 11.3
a
Mean three analysis.

Table 2. Arsenic and heavy metals concentration (mg · kg−1 ) in road dust samples
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Serial
Number Location As Cr Mn Cu Zn Pb
1 Murethitola 214  11 126  8 896  53 65  4 98  5 36  3
2 Netamtola 234  13 113  6 719  38 51  3 67  4 29  2
3 Kaudikasa-I 312  17 132  9 918  55 71  5 106  6 44  4
4 Kaudikasa-II 329  19 135  10 962  57 75  4 110  7 51  3
5 Sonsaitola-I 281  14 151  8 998  59 84  6 117  8 62  4
6 Sonsaitola-II 299  16 122  8 875  51 48  3 86  4 31  3
7 Joratarai 189  10 128  9 902  50 54  4 77  4 28  2
8 Thailitola 204  12 110  7 708  46 43  3 61  3 26  2
9 Jadutola 318  20 107  6 718  43 45  4 68  3 28  3
10 Arajkund 178  11 118  7 810  39 56  5 73  4 36  2
11 Bihari Khurd 167  10 127  8 818  42 59  5 79  5 39  2
12 Sangali 228  13 132  8 826  47 61  6 84  5 42  3
13 Mangatola 198  11 126  9 812  37 54  5 80  4 40  3
14 Dhaditola 165  9 109  7 714  35 47  3 68  3 36  2
15 Meregaon 255  15 111  8 704  41 44  4 65  4 31  2
Note: All values are averaged across three replicates.

(±) of the various elements (viz. As, Cr, Mn, Cu, Zn, Cd, and Pb) Kaudikasa village. As concentration in the studied area was much
were computed. The metal contents of the tree bark samples were higher than those reported in Chinese cities (Lu et al. 2009; Li et al.
expressed in the dried weight (dw) form. The correlation coefficient 2015). On the contrary, the heavy metals concentration was lower
values (r) between the road dust contamination and the barks were than those in the road dust of African, Canadian, and Chinese cities
also determined. All statistical analyses were performed with reported in the literature (Wei et al. 2010; Atiemo et al. 2011;
STATISTICA version 7.1 software (Dell, Round Rock, TX). Nazzal et al. 2014).

Distribution of Arsenic and Heavy Metal in Bark


Results and Discussion
Because tree bark is continually exposed to air pollution over a
period of several years, it may give precise information about
Arsenic Speciation changes that occur in the air conditions of a certain ecosystem. The
The As speciation data in 3 dust samples collected from Kaudikasa As, Cr, Mn, Cu, Zn, and Pb contents in tree bark from the 32 se-
are shown in Table 1. In the dust samples, all arsenic was found in lected tree species are presented in Table 3. They ranged (n ¼ 32)
the inorganic As(V) form. Only in one sample was As(III) identi- from 2.4 to 39.6 mg · kg−1 (As), from 11 to 80 mg · kg−1 (Cr),
fied at trace levels. No organic arsenic species (MMA or DMA) from 31 to 378 mg · kg−1 (Mn), from 7 to 31 mg · kg−1 (Cu), from
were detected. 24 to 82 mg · kg−1 (Zn), and from 1.2 to 10.0 mg · kg−1 (Pb).
Based on their average concentrations (As: 13.5 mg · kg−1 ; Cr:
Distribution of Arsenic and Heavy Metals in Dust 23.5 mg · kg−1 , Mn: 95.6 mg · kg−1 ; Cu: 15.6 mg · kg−1 ; Zn:
50.9 mg · kg−1 ; and Pb: 3.4 mg · kg−1 ), their abundance would
The As and heavy metals contents in the dust samples are summa- follow by increasing order: Pb < As < Cu < Cr < Zn < Mn, which
rized in Table 2. The concentrations of As, Cr, Mn, Cu, Zn, and Pb differed from that indicated previously for road dust.
were in the 165–329, 107–151, 704–998, 43–84, 61–117, and Among the 32 tree species tested, the bark from M. indica and P.
26–62 mg · kg−1 range, respectively. On the basis of the average sylvestris showed the highest accumulation of As (>30 mg · kg−1 ).
concentrations (As: 238  29 mg · kg−1 ; Cr: 123  6 mg · kg−1 ; Apropos of heavy metals, the sum of their total concentration
Mn: 825  50 mg · kg−1 ; Cu: 57  6 mg · kg−1 ; Zn: 83  (ΣHMs ) ranged from 84 to 457 mg · kg−1 . The highest heavy metals
9 mg · kg−1 ; and Pb: 37  5 mg · kg−1 ), the pollutants in the road accumulation was found in the bark from E. globulus followed by
dust would follow by increasing order: Pb < Cu < Zn < Cr < P. sylvestris and D. sissoo. In particular, P. sylvestris and E. glob-
As < Mn. ulus bark samples exhibited remarkably high concentrations of
The concentration of As was the second highest (after Mn) in all Cr and Mn, respectively. The bark from D. sissoo accumulated the
road dust samples, and it was several times higher than the back- highest concentration of Cu, followed by A. indica, D. melanoxy-
ground level of 5 mg · kg−1 . Among the 13 locations studied, the lon, and P. sylvestris. The bark from A. marmelos, followed by that
highest concentrations of both As and heavy metals were found in from D. sissoo, showed a notable accumulation of Zn. The bark

© ASCE 05019006-3 J. Hazard. Toxic Radioact. Waste

J. Hazard. Toxic Radioact. Waste, 2020, 24(1): 05019006


Table 3. Arsenic and heavy metals concentration (mg · kg−1 ) in road dust samples
Serial
Number Location Bark As Cr Mn Cu Zn Pb
1 Kaudikasa Mangifera indica 30.7  1.2 38  3 123  7 20  2 50  2 4.2  0.2
2 Acacia nilotica 2.6  0.1 11  1 39  2 12.0  0.5 52  3 2.6  0.1
3 Ficus benghalensis L. 13.4  0.2 24  2 86  4 14.0  0.4 65  5 10.0  0.5
4 Aegle marmelos 9.4  0.3 26  3 145  9 10.0  0.3 82  3 1.7  0.1
5 Ziziphus mauritiana 9.4  0.3 19  2 116  6 13.0  0.4 56  4 2.1  0.2
6 Phoenix sylvestris 39.6  1.2 80  4 109  6 22  1 77  5 3.1  0.2
7 Terminalia chebula 10.6  0.3 20  2 31  2 10.0  0.4 47  3 2.2  0.2
8 Tamarindus indica 10.2  0.3 13  1 33  3 13.0  0.5 45  2 4.7  0.3
9 Madhuca longifolia 24.8  0.5 25  2 196  6 14.0  0.6 52  3 2.2  0.1
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10 Azadirachta indica 19.0  1.8 20  2 45  3 22  2 64  4 4.2  0.2


11 Eucalyptus globulus 15.6  0.6 16  1 378  22 18  2 24  2 5.7  0.3
12 Butea monosperma 9.2  0.2 20  2 124  7 13.0  0.5 49  3 4.7  0.2
13 Ficus religiosa 15.9  0.4 18  1 32  2 15.0  0.6 35  2 1.9  0.1
14 Shorea robusta 8.6  0.2 16  1 46  3 15.0  0.7 40  3 1.3  0.1
15 Tectona grandis 13.3  0.3 23  2 71  4 12.0  1 48  3 1.9  0.1
16 Dalbergia sissoo 10.4  0.4 42  4 135  8 27  2 80  5 2.1  0.2
17 Diospyros melanoxylon 2.4  0.1 32  3 78  4 22  1 52  3 4.2  0.3
18 Sonsaitola Acacia nilotica 2.7  0.1 12.0  0.5 41  2 13.0  0.6 55  2 2.8  0.1
19 Ficus benghalensis L. 10.1  0.4 21  1 75  2 11.0  0.5 63  2 7.1  0.3
20 Madhuca longifolia 20.1  0.5 19  1 172  8 11.0  0.6 45  2 2.5  0.1
21 Azadirachta indica 17.0  0.4 21  1 41  3 19.0  0.8 59  3 4.8  0.3
22 Butea monosperma 8.1  0.2 22  1 115  5 11.0  0.6 45  3 4.1  0.2
23 Ficus religiosa 11.2  0.3 16  1 39  4 17.0  0.8 47  2 2.3  0.1
24 Shorea robusta 6.1  0.2 11.0  0.5 31  3 14.0  0.7 51  3 2.1  0.1
25 Dalbergia sissoo 11.2  0.3 21  1 118  6 25  2 74  4 3.5  0.2
26 Diospyros melanoxylon 5.1  0.1 34  2 87  4 31  2 55  3 6.2  0.2
27 Ziziphus mauritiana 9.0  0.2 18  1 105  5 13.0  0.6 54  3 1.2  0.1
28 Mangifera indicaa 27.5  0.7 35  2 110  4 19.0  0.9 47  2 3.9  0.2
29 Mangifera indicab 20.2  0.5 26  2 81  3 14.0  0.7 32  1 2.9  0.1
30 Mangifera indicac 17.4  0.4 23  1 70  3 12.0  0.6 28  1 2.5  0.1
31 Dhaditola Ziziphus mauritiana 5.3  0.3 11.0  0.6 65  3 7.0  0.3 32  2 1.2  0.1
32 Mangifera indica 14.5  0.7 19  1 59  2 10.0  0.5 25  1 2.1  0.2
Note: All values are averaged across three replicates.
a
Sample from an approximately 15-year-old tree.
b
Sample from an approximately 10-year-old tree.
c
Sample from an approximately 5-year-old tree.

from F. benghalensis accumulated the highest concentration of derived from three villages, Kaudikasa, Sonsaitola, and Dhaditola,
Pb. Therefore, the bark from M. indica, P. sylvestris, E. globulus, were found to be in comparable range: 0.30–0.96. The obtained
D. sissoo, A. marmelos, and F. benghalensis can be considered as values of r (ranked in descending order) were E. globulus, 0.96;
effective bioindicators for the air pollution detection of As, Cr, Mn, M. longifolia, 0.95–0.96; M. indica, 0.91–0.94; B. monosperma,
Cu, Zn, and Pb, respectively, and could play a similar role to that of 0.89–0.91; Z. mauritiana, 0.79–0.88; A. marmelos, 0.81; T.
pine tree bark in European cities (Sawidis et al. 2011). The con- grandis, 0.77; D. sissoo, 0.77–0.80; F. benghalensis: 0.69–0.72;
centration of the total content of the metals in the bark was found D. melanoxylon, 0.69–0.74; P. sylvestris, 0.68; S. robusta, 0.63–
to increase (153–242 mg=kg) as the age of Mangifera indica tree 0.80; F. religiosa, 0.46–0.51; A. nilotica, 0.38–0.40; A. indica,
increased from ≈5 to ≈15 years (Table 3). 0.34; T. chebula, 0.30; and T. indica, 0.30. Strong correlations were
All bark samples were found to be contaminated with As found for the barks from several of the species (in particular from
concentrations several times higher than the permissible limit of E. globulus, M. longifolia, M. indica, and B. monosperma), indi-
1 mg · kg−1 (WHO 1998). Similarly, all bark was loaded with cating that the pollutants would likely have originated from road
Zn and Cr at higher levels than the permissible limits of 20 and dust. On the other hand, low to moderate correlations were found
2.3 mg · kg−1 , respectively (FAO/WHO 2011). However, some for A. nilotica, A. indica, T. chebula, and T. indica, which suggests
bark was contaminated with Pb above the permissible limit of that the pollutants would have multiple sources (road dust or
5.0 mg kg−1 (WHO 1998). accumulation from soil).

Correlation Coefficients
Conclusions
The correlation coefficient (r) values between the pollutant con-
tents in the road dust samples and in the tree bark samples were Arsenic contamination is a major problem in Chhattisgarh state,
computed. Some of the studied species (e.g., Eucalyptus globulus, India. Arsenic concentrations in road dust samples from 13 loca-
Dalbergia sissoo, and Ficus benghalensis) feature high growth tions (165–329 mg · kg−1 ) and in bark samples from 32 tree spe-
rates, whereas other species show slow-to-moderate growth rates cies (2.4–39.6 mg · kg−1 ) were found to be much higher than the
(e.g., Mangifera indica, Phoenix sylvestris, and Aegle marmelos), permissible limit and higher than those reported, for example,
which may have had an influence on the results. The values of r in Chinese cities. Zn, Cr, and Pb levels also exceeded allowed

© ASCE 05019006-4 J. Hazard. Toxic Radioact. Waste

J. Hazard. Toxic Radioact. Waste, 2020, 24(1): 05019006


exposure limits. Bark samples from 32 tree species were assessed Environ. 67 (Mar): 252–277. https://doi.org/10.1016/j.atmosenv.2012
as air pollution bioindicators, finding correlation values with ar- .11.011.
senic and heavy metals contamination ranging from fair to strong Li, K., T. Liang, L. Wang, and Z. Yang. 2015. “Contamination and health
(r up to 0.96). Taking into account both the pollutant accumulation risk assessment of heavy metals in road dust in Bayan Obo Mining
and the correlation coefficients, the bark from M. indica, P. sylvest- Region in Inner Mongolia, North China.” J. Geog. Sci. 25 (12):
ris, E. globulus, D. sissoo, A. marmelos, and F. benghalensis can be 1439–1451. https://doi.org/10.1007/s11442-015-1244-1.
Lu, X., L. Y. Li, L. Wang, K. Lei, J. Huang, and Y. Zhai. 2009. “Contami-
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“Health effects associated with inhalation of airborne arsenic arising
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