Archives of

1. Introduction
Due to the importance of biodiversity and the destructive effects of human activities, pollution is now receiving more attention than in the past [1]. Large amounts of pollutants released into the environment are the result of urbanization and industrial processes [2]. Heavy metals are considered a major environmental threat because of their multiple sources of production and environmental stability [3]. Heavy metal pollution in aquatic and marine environments is a major concern due to its bioaccumulation by organisms such as birds and fish [4]. Due to their toxicity, indestructibility, and accumulation, heavy metals are among the most serious pollutants in the natural environment so that they are accumulated from natural and artificial sources and transferred to the bodies and tissues of organisms, and accumulation in tissues and bodies of living organisms is more dangerous than its toxicity [5]. In recent years, rapid development has introduced large amounts of heavy metals into the natural environment [6]. Owing to the high development capabilities of aquatic ecosystems, they are at great risk of heavy metals. On the other hand, atmospheric inflows and outflows to the sea bring large amounts of heavy metals from terrestrial ecosystems, caused by human or natural activities, to marine ecosystems [7]. Heavy metal pollutants can have destructive effects on the ecological balance of environmental receptors and the biodiversity of aquatic organisms [8]. Heavy metals such as Pb, Hg, and Ni are common pollutants scattered throughout the ecosystems. These elements are naturally present in marine environments, but they are not essential elements that can be toxic to humans if present in the diet [9]. Waterfowls are among the ways through which heavy elements are transmitted to humans [10]. Birds are generally considered to be a useful indicator for measuring heavy metal contamination in the environment [11,12]. The ecology of birds is well known. On the other hand, birds can provide useful information about the intensity and extent of contamination across the food web because they feed at higher trophic levels in ecosystems [13,14]. The use of birds as indicators of heavy metal contamination has an extensive research background. Okati et al [15] studied Pb and cadmium in some birds of the Khuzestan province. Albayrak and Pekgöz [16] also investigated bioaccumulation and the effects of heavy metals on the morphometry of house sparrows in Egypt. Likewise, Nardiello et al [17] evaluated the rate of heavy metals in northern Gannet and Morus feathers on the coast of Spain. The use of birds for the pollution index is more effective in wetlands where living organisms are concentrated
Bioaccumulation of Heavy Elements in the Organs of Red-Wattled Lapwing in Shadegan Wetland
Sara Birgani1ID, Maryam Mohammadi Rouzbahani1*ID, Roshana Behbash1, Sima Sabz Alipoor1
1Department of Environmental Sciences, Ahvaz Branch, Islamic Azad University, Ahvaz, Iran
*Corresponding Author: Maryam Mohammadi Rouzbahani, Email: mmohammadiroozbahani@yahoo.com
Abstract
Background & Aims: Heavy metals are highly stable in wetland and marine environments and can be toxic to organisms. Wetland birds play a vital role in the life cycle and food chain. This study aimed to investigate the bioaccumulation of heavy elements such as lead (Pb), mercury (Hg), nickel (Ni), and copper (Cu) in the organs of red-wattled lapwings in Shadegan wetland in 2019.
Materials and Methods: Pb, Hg, Ni, and Cu were studied in this descriptive-applied study. Ten red-wattled lapwings were randomly prepared in Western Shadegan wetland and with the coordination of the environmental unit of the region through hunting in December 2019. A graphite furnace spectrometer, GBcA made in Australia, was used to determine the amounts of these elements in liver, kidney, and tail feathers. The LOD and relative standard deviation of sampling were also determined, and finally, the results were analyzed using correlation and regression analyses.
Results: Based on the results, the highest cumulative concentration belonged to Cu. Its mean values in the liver, kidney, and tail feathers were 4.16%, 3.95%, and 1.77 mg/kg, respectively. The highest and lowest means of Pb, Hg, Ni, and heavy Cu elements in the kidney tissue were 1.974 and 1.08 mg/kg, respectively. Based on these results, the kidney was the most important tissue accumulating heavy elements in red-wattled lapwing.
Conclusion: Overall, there were significant amounts of heavy elements in various organs of the red-wattled lapwing present in Shadegan wetland. These results indicated the relatively high levels of pollution in Shadegan wetland compared to some other bird habitats in Iran, which is probably attributed to the oil, gas, petrochemical, and sugarcane industries around Shadegan wetland.
Keywords: Heavy metals, Wetland, Red-wattled lapwing, Bioaccumulation
Received: November, 18, 2021, Accepted: January, 23, 2022, ePublished: March 18, 2023
https://jhygiene.muq.ac.ir
10.34172/AHS.12.1.13.349
Vol. 12, No. 1, 2023, 1-6
Original Article
Birgani et al
2 Arch Hyg Sci. Volume 12, Number 1, 2023
[18]. Shadegan International Wetland is one of the large
wetlands of Iran, located in the southwest of Iran and the
south of Shadegan in Khuzestan province. This wetland
is the habitat of over 30% of birds (154 species), 25% of
mammals (40 species), and 45% of fish (36 species of marsh
fish and 45 species of sea fish) in Iran [19]. At the same
time, the inflow of sugarcane project effluents into this
wetland through the passage of oil pipelines, the inflow of
urban and industrial sewage, the dumping of city waste,
and the construction of a steel factory next to this wetland
are among the most important dangers threatening this
place [20]. This wetland is one of the sensitive ecosystems.
It is also a host for migratory birds, and due to the siege by
the steel and petrochemical industries, it is also in danger
of environmental destruction [21]. Therefore, biological
monitoring seems necessary to know about the health of
its environment. Among the environmental indicators
are the organs of birds. Red-wattled lapwing is one of the
types of birds living in Shadegan wetland. This species,
with the scientific name Hoplopterus indicus, is a bird with
a red beak and yellow legs that feeds on insects and other
invertebrates and is found in pairs [22]. This paper sought
to investigate the amount of the bioaccumulation of heavy
metals (Pb, Hg, Ni, and Cu) in the tissues of red-wattled
lapwings in Shadegan wetlands and to compare its rate of
pollution.
2. Materials and Methods
In this descriptive research, data were collected through
documentary and field methods. The documentary
method includes desk studies and searching for articles
related to research theory. Sampling and laboratory
measurements of heavy metals in the liver, kidney, and
tail feathers of red-wattled lapwing are used in the field
method. The studied elements included Pb, Hg, Ni,
and Cu. These elements are considered to be the most
important indicators of human-made pollution in the
natural environment. This species is selected because it
is not included in the list of endangered or threatened
species, and it is native to Shadegan wetland. Ten birds
were randomly hunted for laboratory analysis in December
2019 with the coordination of the environmental unit of
the region. It should be noted that this species is on the
list of the “least concern” in the International :union: for
the Conservation of Nature list and is not considered a
prohibited hunting species. The location of Shadegan
wetland and sampling points are displayed in Figure 1.
The collected samples were dissected, and the organs
of the caught birds, including tail feathers, the kidney,
and the liver, were removed. It should be noted that the
feathers were washed with detergent and distilled water
after being transported to the laboratory to remove
possible contamination. Then, kidney, liver, and tail
feather samples were placed in an oven at 50°C for 48
hours to determine dry weight. The graphite furnace
spectrometer (GBcA, Australia) was used to measure
heavy elements in different tissues of this bird. To
calculate the limit of detection (LOD) of the device for
each of the heavy metals, the specified concentration of
heavy metals was injected into the device, and its values
were obtained after three repetitions. Considering the
more favorable precision in the standard increase method
than the working chart method, the recovery percentage
of the atomic absorption device was performed also based
on this method as described in Eq. (1).
0 100 sample
spiked
R C C
C
= − × Eq. (1)
where Csample is the concentration of a sample to which
a certain amount of heavy metal has been added, and
C0 denotes the initial concentration of the sample. In
addition, Cspiked represents the concentration equivalent
to the amount added to the sample [23]. The final
concentration of heavy metals based on the mg/kg wet
weight of the sample was calculated by Eq. (2):
M Cv
W
= Eq. (2)
where M and C represent the final concentration of the
sample based on mg/kg and the concentration estimated
Figure 1. Location of Shadegan wetland and sampling points.
Arch Hyg Sci. Volume 12, Number 1, 2023 3
Bioaccumulation of Heavy Elements in the Organs
by the device, respectively. Further, w and v indicate
the amount of material used for digestion per g and the
final volume of the solution, respectively [24]. Data on
LOD and relative standard deviation in this research are
provided in Table 1.
To analyze the data, one-way analysis of variance
(ANOVA), correlation test, and linear regression were
used to determine the relationship between the measured
values of heavy elements in different red-wattled lapwing
organs by SPSS 19 and OriginPro 2018.
3. Results
The results of the biometry of bird species are presented
in Table 2. The mean weight of red-wattled lapwing and
the mean length of the hunted birds were 455 g and
34.2 cm, respectively. The length of both ends of the
wings was 57 cm.
The results of measuring heavy metals Pb, Ni, Cu, and
Hg in the liver, kidney, and tail feathers of red-wattled
lapwings are presented in Table 3. Based on the findings,
the highest cumulative concentration belonged to Cu, and
its mean values in these organs were 4.16, 3.95, and 1.77
mg/kg, respectively. However, the lowest values of the
measured elements in red-wattled lapwing’s organ were
related to Hg; in addition, its mean values in the liver,
kidney, and tail feathers were equal to 0.06, 0.12, and 0.04
mg/kg, respectively.
Figures 2 and 3 illustrate the results of measuring heavy
elements in red-wattled lapwing organs and samples.
The highest and lowest means of Pb, Hg, Ni, and Cu
were related to the kidney (1.974) and liver tissue (1.08),
respectively. Based on these results, the most important
tissue accumulating heavy elements in this species
was the kidney. The difference in the mean values of
heavy elements in different organs of this species was
investigated using the one-way ANOVA. Based on the
results, there was a significant difference between the
amounts of Hg in the liver and tail feather samples in 10
measured samples (P < 0.05).
The results of one-way ANOVA between the organs
of this species are listed in Tables 4 and 5. A significant
difference was found between the amounts of Pb in all
organs, Ni in the kidney and liver, Hg between the liverkidney
and kidney-liver, and Cu between the liver-liver
and kidney-liver (P < 0.05), indicating the difference
in the amount of the accumulation of heavy metals in
different red-wattled lapwing organs. Accordingly, redwattled
lapwing organs, including the kidney, had a high
potential for the accumulation of heavy metals.
4. Discussion
In general, biological monitoring can be a desirable and
satisfactory method for measuring the amount of heavy
metals and their bioavailability [25]. Burger [26] stated
that the identification of the importance and effects of
heavy metals in ecosystems has led to the development
of biological monitoring plans with the aim of measuring
the levels of pollutants in different organisms, in which
prominent species are used to estimate the levels
of these pollutants in different parts of ecosystems.
Bioaccumulation in the food chain is one of the important
results of the stability of heavy metals. Water ecosystems
Table 1. LOD and RSD of the Measurement of Heavy Elements
Element LOD (ugL-1) RSD (%)
Pb 7.9 0.76
Ni 2.3 0.56
Cu 1.4 0.32
Hg 0.25 0.47
Note. LOD: Limit of detection; RSD: Relative standard deviation; Pb: Lead;
Ni: Nickel; Cu: Copper; Hg: Mercury.
Table 2. The Results of biometry of red-wattled lapwing
Variable Mean ± SD
Weight (g) 455 ± 35
Total length (cm 34.2 ± 2.5
Length of two sides of a wing (cm) 57 ± 5
Note. SD: Standard deviation.
Table 3. The results of measuring lead, mercury, nickel, and copper in the liver, kidney, and tail feathers of red-wattled lapwing
Organs
Lead (mg/kg-1) Mercury (mg/kg-1) Nickle (mg/kg-1) Copper (mg/kg-1)
Concentration Uncertainty Concentration Uncertainty Concentration Uncertainty Concentration Uncertainty
Liver 0.883 ± 0.185 0.068 ± 0.03 1.43 ± 0.462 4.16 ± 2.02
Kidney 1.82 ± 0.334 0.127 ± 0.047 2.01 ± 1.06 3.95 ± 1.34
Tail feather 0.92 ± 0.369 0.044 ± 0.018 1.07 ± 0.44 1.77 ± 0.51
Figure 2. The mean amounts of Pb, Hg, Ni, and Cu in the liver, kidney,
and tail feathers of red-wattled lapwing. Note. Pb: Lead; Hg: mercury; Ni:
Nickel; Cu: Copper.
Birgani et al
4 Arch Hyg Sci. Volume 12, Number 1, 2023
in Iran are highly vast and have significant value. However,
in recent years, the destruction of habitats, illegal hunting,
the introduction of many environmental pollutants,
and other factors have reduced their usefulness for the
population of aquatic wildlife, especially aquatic birds.
The fact that birds are highly sensitive to environmental
pollution is well recognized. In the majority of
ecological toxicology studies, birds are used as biological
indicators for heavy metals due to their wide geographic
distribution, relatively long life span, and appropriate
position in the food chain. Shadegan wetland is one of the
most important water areas in southwest Iran, which is
affected by various environmental pollutions such as oil,
steel, and sugarcane industry effluents. Therefore, this
research focused on investigating the bioaccumulation of
heavy metals (Pb, Hg, Ni, and Cu) in the tissues of redwattled
lapwing in Shadegan wetland in 2019. The results
demonstrated that there were significant amounts of heavy
elements in various organs of the red-wattled lapwing in
Shadegan wetland. The most important accumulating
tissue was kidney. In studies by Cui et al [27] and Lin et
al [28], the kidney tissue was also the most important
organ accumulating heavy elements for domestic pigeon
and white stork species. However, in other studies such
as those by Kenntner et al [29] and Akan et al [30], the
accumulation of heavy elements in the feathers and liver
of the white-tailed eagle and urban chicken was more than
in the kidney tissue. In the study by Hassanpour et al [7],
the mean amount of Pb in the liver and kidney of coots
in Gomishan wetland and Gorgan bay was measured as
0.101 and 0.124 mg/kg, respectively, which was lower than
the values measured in this study (0.883 and 1.82 mg/kg).
In the research by Namroodi et al [31], the mean amount
of Hg in the tissues of graylag geese and rural geese was
estimated between 0.2 and 0.4 μg/kg, which is lower than
the corresponding value reported in the current study.
These results confirmed the presence of relatively severe
pollution in Shadegan wetland compared to some other
bird habitats in Iran.
5. Conclusion
The results of this study revealed that Cu had the
highest level of bioaccumulation in different organs of
red-wattled lapwing in Shadegan wetland. Further, the
kidney was the most important tissue for accumulating
heavy metals in this species. The concentration of heavy
metals in different tissues of this species indicated the
presence of chemical pollution in the Shadegan wetland.
Thus, the results presented in this paper can be used
in the environmental management program for the
Shadegan wetland. To estimate the effect of factors such
as oil facilities, the current study is recommended to be
conducted in wider time frames and areas.
Acknowledgments
The authors would like to express their gratitude to Ahvaz Islamic
Azad University, Environmental Protection Organizations, and
Health and Medical Vice-chancellor for their cooperation in
obtaining the required information.
Authors’ Contribution
Conceptualization: Sara Birgani.
Figure 3. The Mean Amount of Total Heavy Elements in Red-wattled Lapwing Organs (Right) and 10 Measured Samples (Left).
Table 4. The Results of One-way ANOVA
Heavy metals
P value
Liver Kidney Tail feather
Lead 0.062⁕ 0.257 0.88
Nickle 0.569 0.221 0.746
Copper 0.886 0.529 0.556
Mercury 0.024⁕ 0.171 0.038⁕
Note. ANOVA: Analysis of variance.
*The mean difference is significant at the 0.05 level.
Table 5. Results of Pearson correlation test for the amounts of heavy elements
in bird organs
Heavy metal
P value
Liver-kidney Tail feather-liver Tail feather-kidney
Lead 0.00 ⁕⁕ 0.001⁕⁕ 0.03⁕
Nickle 0.188 0.511 0.018⁕
Mercury 0.002⁕⁕ 0.205 0.00⁕⁕
Copper 0.942 0.002⁕⁕ 0.006⁕⁕
*The mean difference is significant at the 0.05 level.
**The mean difference is significant at the 0.01 level.
Arch Hyg Sci. Volume 12, Number 1, 2023 5
Bioaccumulation of Heavy Elements in the Organs
Data curation: Sara Birgani- Roshana Behbash.
Formal Analysis: Sima Sabz Alipoor.
Investigation: Sima Sabz Alipoor.
Methodology: Maryam Mohammadi Rouzbahani.
Project administration: Sima Sabz Alipoor.
Resources: Sima Sabz Alipoor.
Software: Sara Birgani.
Supervision: Roshana Behbash.
Validation: Maryam Mohammadi Rouzbahani-Sima Sabz Alipoor.
Visualization: Maryam Mohammadi Rouzbahani.
Writing – original draft: Sara Birgani.
Writing – review & editing: Roshana Behbash.
Competing Interests
The authors declared that there was no conflict of interests.
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