Application of Columba livia Feather as a Bioindicator of Industrial Pollution

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Application of Columba livia Feather as a Bioindicator of Industrial Pollution

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In developing countries, due to the development of industrial technologies and heavy metals pollution in the environment, the use of bioindicators such as bird feathers could be a good way to transmit pollutants to the environment. In this study, the accumulation of heavy metals such as lead, zinc and cadmium in Columba livia feathers in males and females and live and dead species in Industrial town of Zinc-Zanjan and comparison with control species outside industrial town were studied. The feathers of 164 pigeons were collected and dissolved by chemical digestion method. In this study, heavy metals were measured by the avanta GBC atomic absorption device. The mean concentrations of lead, zinc and cadmium were determined greater in dead female pigeons, dead male pigeons, live female pigeons, and live male pigeons respectively. This was also the case with the control species. Statistical analysis of data was performed with SAS software (Statistical Analysis System). (P ≤ 0.05, 95% confidence level) and (P ≤ 0.01, 99% confidence level) were considered as significant differences. The results of statistical tests in the samples inside Industrial town of Zinc-Zanjan showed that there is a significant statistical relationship between gender (male-female) and live and dead bird and elements of lead, zinc and cadmium, while for the control species were different. Significant levels of heavy metals in bird feathers indicate their usefulness as a non-invasive tool to show the concentration of metals in pigeons to control the level of pollution in the environment. The present study showed that Columba livia had suitable biological characteristics for use as a bioindicator of industrial pollution.

Columba livia

Bioindecator

Zanjan

heavy metals

industrial

Pollution of the living environment in present centuries, is the result of urbanization, industrialization, and developements of human societies (1). Low levels of elements are naturally present in varying amounts in the Earth's crust (14), (28), (3). They enter the life of plants and animals in from natural resources and human activities (Biney et al. 1994) heavy metals also tend to show bioaccumulation (62) and contaminate the soil and water ecosystems by biological accumulation in tissues and biological magnification in the food chains (33). Therefore, concerns about the long-term effects of heavy metals as environmental pollutants have increased (53). Bioindicators of living organisms such as plants, plankton, animals, and microbes are used to assess the health of the environment and biogeographical changes in the environment. They are useful, visible, explicit and recoverable (60). Biological monitoring can be a desirable and satisfactory method for measuring the amount of heavy metals and their bioavailability (24). Since the mid-1960s, birds have been widely used as biomonitors for environmental pollution, especially for heavy metal monitoring (11), (24), (18). The use of feathers for biological monitoring of metals has advantages over the use of other internal tissues (11). Feathers are easy to assemble, easy to maintain because they do not need to be stored at low temperatures (46), (27). Feather is a non-destructive tissue and can also be obtained from live birds. This is a special feature for rare species (10) and can play the role of storing and removing heavy metals (11).

Industrial town of Zinc-Zanjan is located in 6 km from the city of Zanjan, where the ingot production units and their products are operating. Observations show a large number of bird species (Columba livia), nests and lives in the Zinc specialized towns and in the sheds of factories. Due to the pollution in the Industrial town of Zinc to heavy elements and the large population of this species in this polluted place, high mortality of this bird is observed. Therefore, the study of the causes of death and protection of this species has been considered and selected as a bioindicator of industrial pollution in Industrial town of Zinc-Zanjan.

The aim of this study was to use Columba livia feather as a bioindicator of industrial pollution in Industrial town of Zinc-Zanjan and for the first time for this species in Iran. For this purpose, the accumulation of low levels of lead, zinc and cadmium in Columba livia feather in males and females and live and dead species within the Industrial town of Zinc-Zanjan were measured and then were compared with the control species and a statistically significant relationship was obtained between them. Also, Despite the common and varied methods available for chemical digestion and preliminary experiments with several methods such as (32),( 17),(45),(30),(16),(6),(8),(47),(25),(36),(52) Our other aim, introduce the new method, which was suggested for complete digestion and dissolution feather compared to others, was changing the amount and types of chemicals, which could be effective as a new step for this purpose and it`s applicability in future researches.

Study Area

Industrial town of Zinc-Zanjan is located in 6 km southwest of Zanjan towards Bijar. This town is located in the geographical coordinates of 36°36′26′′ to 36°37′01′′ north latitude and 48°23′42′′ to 48°25′33′′ east longitude and 6.8 km distance of Zanjanrood river and 1.6 km of Ajhdahatou village.(Fig. 1) In terms of topography, this industrial town is located in the plain. The area of this industrial town is about 230 hectares, in which Zinc ingot production units and their products are operating. One of the most important raw materials used in Zinc industry is mining soil. The most used soil in industrial units in Zanjan province is from lead mine and from Angoran which is located 110 km west of Zanjan city.

Figure 1.

Sampling Method

This study is descriptive-analytical based. After examining the area and conducting a preliminary experiment on determining the statistical population in 2019 from May to August, a total of 164 statistical samples included 80 male specimens (40 deads and 40 lives) and 80 female specimens (40 deads and 40 lives) were selected randomly. Manual sampling of birds in sheds located on the surface of Zinc industrial town and 4 control samples including (1 live male, 1 dead male, 1 live female, 1 dead female) were performed to minimize damage to the bird. Feather specimens were collected from equal parts (right wing, left wing, tail, and chest) in equal proportions and the live birds were released.

Sample Preparation And Analysis

Several methods have been reported to remove surface contamination from feathers prior to analysis (19). Studies have been reported using unwashed feathers (51) and washed feathers (55),(21),(5), but researches with washed samples makes it possible to study the concentration of small amounts of particles in the environment as well as the absorption of tissues (36). After coding and transferring to the laboratory, samples were washed first to remove any possible grease, parasites, and microorganisms from the alcohol and then were washed with distilled water.

Then, they were washed three times alternately with acetone and distilled water to remove any external contaminants (12). Therefore, it could be concluded that the presence of low levels of elements in the feathers is not due to external pollutants such as air. However it could be contaminated during the formation of feathers and transferring pollutants by their blood and also the amount of trace elements in the blood indicate contamination of their diet (21). The feathers were dried in the oven at 65 °C for 24 hours, and the samples were crushed and weighed for 1 g of sample, and then chemical digestion was used to convert the solid samples to solution. The methods which are used for digestion, must be cost-effective, both in the terms of the chemicals and in the terms of the tools and equipments, because the goal is to analyze the low-value elements present in the sample. Also, the original nature of the sample should not change and all the low-value elements remain. Therefore, 15 ml of nitric acid was added to each sample (1 g) during digestion and remained overnight. Then at least 3 ml of oxygenated water was added to the sample and stirred. After the foam subsided, 2 ml of hydrochloric acid was added to the sample and placed in a Ben Marie bath for 2 hours. After cooling, the samples were subsequently filtered and was reached to 25 ml by distilled water. To ensure the accuracy of digestion operations and the effect of consumables on the concentration of trace elements, one control sample was prepared for every 10 samples. In this case, the samples were ready for injection into the atomic absorption device (avanta GBC atomic absorption Made in Australia with an accuracy of 1 ppb). In the first step, it was necessary to determine the concentration range of each of the elements of lead, zinc, and cadmium, which was determined by performing preliminary analysis of the desired range using pre-samples. Required standards for each element was prepared (63). An acetylene-air mixture was used to create the flame in the metal measurement. The raw data read from the atomic absorption device was calculated in ppm, by the following formula:

(Formula1)\(M=\frac{\text{C}.\text{V}}{ \text{W}}\)

Where C is the concentration, V shows the final volume of the sample (25 ml), W is the amount of dry sample for digestion (1 g) and M is the final concentration of the sample in ppm.

Statistical

SAS 1.9 software (Statistical Analysis System) and Proc Glm (Procedure General Linear Model) statistical procedure were used to analyze the data variance. Obviously, before analyzing the statistical assumptions of variance, the distribution of data was normal. Proc Corr (Procedure Correlation) was used for citizenship analysis. Also Proc ttest (Procedure TTest) procedure was used in this test. (P ≤ 0.05, 95% confidence level) and (P ≤ 0.01, 99% confidence level) were considered as significant differences.

Measurement of heavy metals lead, zinc, and cadmium

In this study, the mean concentrations of lead, zinc, and cadmium elements in the dead male pigeon feather of Zinc Industrial Town 17.125, 319.25, 1.735 (µg/g), respectively, as well as the average concentration of lead, zinc, and cadmium in the live male pigeon feather were determined 14.825, 301.0625, 1.365 (µg/g). as well as the average concentration of lead, zinc, and cadmium in the dead female pigeon feather 17.455, 378.75, 1.927 (µg/g), as well as the average concentration of lead, zinc, and cadmium in the live female pigeon feather were determined ,15.146, 307.562, 1.477(µg/g) (Fig. 2).

Figure 2.

In this study, The mean concentrations of lead, zinc, and cadmium elements in dead male pigeon feather of control species were determined 2.175, 57.5, 0.575 (µg/g), respectively, as well as the average concentration of lead, zinc, and cadmium in the live male pigeon feather were determined 0.8, 34.5, 0.32(µg/g). as well as the average concentration of lead, zinc, and cadmium in the dead female pigeon feather 3, 62.5, 0.95(µg/g), as well as the average concentration of lead, zinc, and cadmium in the live female pigeon feather were determined ,1.425, 44.5, 0.475 (µg/g) (Fig. 3).

Figure 3.

Consequantly, the results of measuring the concentration of lead, zinc and cadmium in feather of Columba livia in the industrial town of Zinc-Zanjan indicated that the amount of these three elements in dead female pigeons > dead male pigeons > live female pigeons > live male pigeons, which indicates that the amount of heavy elements in the dead specimens was higher than in the live specimens and the amount of the same elements in the female was higher than in the males. This was also the case with the control species. In general, in the present study, the mean concentrations of heavy metal in the elements lead, zinc, and cadmium in four groups (dead male -live male-dead female-live female) were evaluated, but the average concentration of lead, zinc and cadmium metals of Columba livia feather in the industrial town of Zinc-Zanjan was obtained 16.14175, 623.678625, and 1.626125 (µg/g), respectively. Compared to the control specimens collected and analyzed outside the industrial town, the average concentration of lead, zinc, and cadmium metals are equal to 1.85, 49.75, and 0.46125 (µg/g) was determined, respectively. Comparing the samples inside the industrial town of Zinc-Zanjan and the control samples also showed a significant level of difference between the two cases.

Statistical analysis

General analysis of lead, zinc and cadmium elements in samples of Columba livia feather in the industrial town of Zinc-Zanjan based on gender and live and dead species (Table 1)

Table 1

General analysis of lead, zinc and cadmium elements in *Columba livia* feather in the Industrial town of Zinc-Zanjan based on gender and live and dead species. The value (P < 0.01, 99% confidence level) was considered to be significant for the samples.
Variable	N	Total mean	Source	Mean squre	F value	pr > f
cd	160	1.626425	Sex Live total	0.92416000 6.70515323 3.81465661	76.14 552.45 314.30	< .0001 < .0001 < .0001
Zn	160	326.6563	Sex Live total	43560.66000 79879.88938 61720.2747	106.88 195.99 151.44	< .0001 < .0001 < .0001
pb	160	16.14444	Sex Live total	3.8800441 210.0663889 106.9732165	98.76 5346.84 2722.80	< .0001 < .0001 < .0001

There was a statistically significant relationship between the gender of the bird (male and female) and the cadmium element. There was a statistically significant relationship between the live and dead bird and the cadmium element. There was a statistically significant relationship between the gender of the bird (male and female) and the zinc element. There was a statistically significant relationship between the live and dead bird and the zinc element. There was is a statistically significant relationship between the gender of the bird (male and female) and the lead element. There was a statistically significant relationship between the live and dead bird and the lead element.

Table 1.

Overall, the results showed that there was a statistically significant relationship between bird gender (male and female) and the elements lead, zinc and cadmium.

Overall, the results showed that there was a statistically significant relationship between (live and dead) and the elements lead, zinc and cadmium.

General analysis of lead, zinc and cadmium elements in samples of Columba livia feather of control samples based on gender and live and dead species (Table 2)

Table 2

General analysis of lead, zinc and cadmium elements in *Columba livia* feather of control sample based on gender and live and dead species. The value (P ≤ 0.05, 95% confidence level) was considered significant for the samples.
source	Variable	N	Total mean	Mean squre	F value	pr > f
cd	Sex Live total	4 4 4	0.580000	0.07022500 0.13322500 0.10172500	5.80 11.01 8.41	0.2505 0.1863 0.2369
Zn	Sex Live total	4 4 4	49.75000	56.2500000 420.2500000 238.2500000	9.00 67.24 38.12	0.2048 0.0773 0.1138
pb	Sex live total	4 4 4	1.850000	0.52562500 2.17562500 1.35062500	52.56 217.56 135.06	0.0873 0.0431 0.0607

There was no statistically significant relationship between bird gender (male and female) and the cadmium element. There was no statistically significant relationship between the live and dead bird and the cadmium element. There was no statistically significant relationship between bird gender (male and female) and the zinc element. There was no statistically significant relationship between the live and dead bird and the zinc element. There was no statistically significant relationship between bird gender (male and female) and the lead element. There was no statistically significant relationship between the live and dead bird and the lead element.

Table 2.

Overall, the results showed that there was no statistically significant relationship between bird gender and live and dead and the zinc element.

Overall, the results showed that there was no statistically significant relationship between bird gender and live and dead and the cadmium element.

Overall, the results showed that there is a statistically significant relationship between live and dead of bird and the lead element, but not between the gender of the bird and the lead element.

General analysis of lead, zinc and cadmium elements in samples of Columba livia feather of control and Zinc-Zanjan specialized town samples based on gender and live and dead species (Table 3)

Table 3

General analysis of lead, zinc and cadmium elements in *Columba livia* feather of control and Zinc-Zanjan industrial town samples based on gender and live and dead species. The value (P ≤ 0.01, 99% confidence level) was considered significant for the samples. **Variable**: (a = town samples,b = control samples, c = town and control samples)
source	Variable	N	mean	Std Dev	t Value	Pr > \|t\|
Cd Cd Cd	a b c	160 4 164	1.6264 0.58 1.0464	0.2449 0.268 0.2453	8.43	< 0.0001
Zn Zn zn	a b c	160 4 164	326.66 49.75 276.91	34.334 12.685 34.058	16.06	< 0.0001
Pb Pb pb	a b c	160 4 164	16.144 1.85 14.294	1.1766 0.9507 1.1728	24.08	< 0.0001

There was a statistically significant relationship between (samples on industrial town of Zinc-Zanjan and control samples) and cadmium element. There was a statistically significant relationship between (samples of Zinc-Zanjan industrial town and control samples) and zinc element. There was a statistically significant relationship between (samples of Zinc-Zanjan industrial town and control samples) and lead element.

Table 3.

In recent decades, numerous studies have been conducted on the presence of trace elements in the environment, many of which have lookedat its effects on human and animal health andon wild birds.(54) Quoted from (2),( 61), (64).

The standard limits for heavy metals have not been stated in the various organs of birds, but the measurement can be comp industrial ared with other studies. In our research, the average total concentration of trace elements in species in the industrial town Zinc-Zanjan (aggregation of male, female, live and dead species) and the final average in the lead, zinc and cadmium elements are 16.14175, 326.678625, and 1.626124 μg/g, respectively, as well as the average concentration of lead zinc and cadmium elements in the control species were obtained 1.85, 49.75, and 0.58 μg/g.

According to Janssen's study, the amount of lead in Parus major feathers was obtained 31.2 ± 230 μg/g and in Eens study, the amount of lead in blue and great tit tail feathers were obtained 15.2±640 and 1.8 ± 16.03 μg/g (38),( 23). Research studies have shown that the average concentration of lead in pigeon feathers in France, Korea, Israel, Slovakia, Brazil are 0-5 μg/g, the average concentrations of zinc in pigeons in France, Israel, and Brazil were between 90-300 μg/g and the average concentrations of cadmium in pigeons in France, Israel, and Brazil were 0.04-3 μg/g) (25),(39),(52),( 4),( 9). In a study of common buzzard in northern Italy, the mean concentrations of lead and cadmium in bird feathers were found to be 1.48 and 0.060 mg/kg dw^{^[1]}, respectively (13). In a study conducted on Laughing dove, the mean lead concentration in feather was 0.01± 19.88 μg/g and for cadmium was 0.03 ± 0.87 μg/g (7). Lead for Hirundo rustica, which was collected near the contaminated area and along a highway in Maryland, USA, was found in the range of 43-820 μg/g (29). In the study of (59), the mean concentration of lead, zinc, and cadmium in great egret were obtained 0.78, 168.96, and 0.25 μg/g, respectively. In the study on E. gularis and L. heuglini, cadmium concentrations were measured at 1.16 and 1.37 μg/g, respectively, and lead concentrations were measured at 7.04 and 5.48 μg/g, respectively (49). In a study conducted on pellets of blue rock pigeon in India, the highest concentration of lead, cadmium, zinc, were found (79.6 ± 42.69 μg/g; 1.12 ± 0.60 μg/; 2250 ± 1390.16 μg/g) respectively ( 15(.

Studies on birds contaminations has shown that the amount of trace elements in gender is different.

In our study, the average concentration of trace elements of lead, zinc and cadmium, aggregation between the dead and the live, about lead element in the female and male were 16.3 and 15.9885 μg/g, the average of zinc element in the female and male were 343.201 and 310.15625 μg/g and the average concentration of cadmium element in the female and male were 1.70225 and 1.55 μg/g, respectively. In addition, the average elements in control species were the average of lead element in the female and male 2.2125 and 1.4875 μg/g, the average of zinc element in the female and male 53.5 and 46 μg/g, and the average of cadmium element in the female and male 0.7125 and 0.4475 μg/g, respectively.

in research on black ducks, the levels of metals in males were higher than in females. In Scaups, lead levels in females were significantly higher than in males (31). In a study of the Fulica atra, the average lead concentration in males was higher than females (35). By researching on the Larus genei, the average concentration of lead and cadmium in the male bird and the amount of zinc in the female bird were higher (34). In the Phalacrocorax carbo study, the amount of zinc metal in the female bird's muscle was higher than in the male (42). Research on Egretta alba has shown that there is a statistically significant difference in the average concentrations of heavy metals of lead, zinc and cadmium in the feather tissue between males and females (59). However, in the study of great tits, there was no significant difference between Cd and Pb levels between males and females. The concentration of Zn in males was higher than in females (21). In a study conducted on Ardea cinerea, the difference between the amounts of heavy metals between the genders is very small compared to other different samples (50).

[1]-Miligram/ Gram/ Dry Weight

Acknowledgements

We would like to thank Mr. Meysam Pashaei for his professional and compassionate guidance.

Funding

The authors declare that no funds, or others pecific grant from any funding agency in the public, commercial, or non-profit sectors support were received during the preparation of this manuscript.

Conflict of interests

The authors declare that they have no conflict of interests.

Competing interests

The authors declare no competing interest.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Authors' contributions

Fariba Asgari, Ph.D student in Environmental Pollution, is the principal author of this article. Nooshin Sajjadi and Mojgan Zaeimdar and Mostafa Sadeghi and Mahnaz Mirza Ebrahim Tehrani , contributed to the study conception and commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethics approval consent to participate

The project was found to be in accordance to the ethical priniciples and the national norms and standards for conducting Medical Reserch in Iran, Approval , ID: IR.IAU.TNB.REC.1400.012, Approval Date: 2020-08-22.

Consent for publication

We affirm that all authors have agreed for submision of the paper to the this journal and are fully aware of ethical responsibilities. The submission to this journal implies that the Paper has not been published previously.

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Application of Columba livia Feather as a Bioindicator of Industrial Pollution

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Abstract

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Introduction

Materials And Methods

Study Area

Sampling Method

Sample Preparation And Analysis

Statistical

Results

Measurement of heavy metals lead, zinc, and cadmium

Statistical analysis

Discussion

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References

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