Abstract
Urban-dwelling birds can be useful biomonitors to assess the impact of the urbanisation on both public and wildlife health. Widely distributed urban bird species, the House crow, was studied for heavy metal accumulation levels from nine cities of South Asia, Southeast Asia and Africa that border the Indian Ocean. Feathers were spectroscopically investigated for the deposition of ten heavy metals, i.e. As, Zn, Pb, Cd, Ni, iron Fe, Mn, Cr, Cu and Li. Fe and Zn were found to be the most prevalent metals in all sites. Measured concentrations of Pb (4.38–14.77 mg kg−1) overall, and Fe (935.66 mg kg−1) and Cu (67.17 mg kg−1) at some studied sites were above the toxicity levels reported lethal in avian toxicological studies. Multivariate analysis and linear models supported geographical location as a significant predictor for the level of most of the metals. Zn and Cu, generally and Pb, Cd, Mn, Cr at some sites exhibited potential bioaccumulation from surrounding environments. Inter-species comparisons strengthen the inference that the House crow is a reliable bioindicator species for the qualitative assessment of local urban environmental pollution and could be a useful tool for inter-regional monitoring programs.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-24712-z/MediaObjects/11356_2022_24712_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-24712-z/MediaObjects/11356_2022_24712_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-022-24712-z/MediaObjects/11356_2022_24712_Fig3_HTML.png)
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this published article and its supplementary information file.
References
Abbasi NA, Jaspers VLB, Chaudhry MJI, Ali S, Malik RN (2015) Influence of taxa, trophic level, and location on bioaccumulation of toxic metals in bird’s feathers: a preliminary biomonitoring study using multiple bird species from Pakistan. Chemosphere 120:527–537. https://doi.org/10.1016/j.chemosphere.2014.08.054
Abbasi NA, Khan MU, Jaspers VLB, Chaudhry MJI, Malik RN (2015b) Spatial and interspecific variation of accumulated trace metals between remote and urbane dwelling birds of Pakistan. Ecotoxicol Environ Saf 113:279–286. https://doi.org/10.1016/j.ecoenv.2014.11.034
Abdullah M et al (2015) Avian feathers as a non-destructive bio-monitoring tool of trace metals signatures: a case study from severely contaminated areas. Chemosphere 119:553–561. https://doi.org/10.1016/j.chemosphere.2014.06.068
Addis W, Abebaw A (2017) Determination of heavy metal concentration in soils used for cultivation of Allium sativum L. (garlic) in East Gojjam Zone, Amhara Region, Ethiopia. Cogent Chemistry 3 https://doi.org/10.1080/23312009.2017.1419422
Adout A, Hawlena D, Maman R, Paz-Tal O, Karpas Z (2007) Determination of trace elements in pigeon and raven feathers by ICPMS. Int J Mass Spectrom 267:109–116. https://doi.org/10.1016/j.ijms.2007.02.022
Ali H, Khan E (2019) Trophic transfer, bioaccumulation, and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs—Concepts and implications for wildlife and human health. Human Ecol Risk Assess: An Int J 25:1353–1376. https://doi.org/10.1080/10807039.2018.1469398
Ansara-Ross T, Ross M, Wepener V (2013) The use of feathers in monitoring bioaccumulation of metals and metalloids in the South African endangered African grass-owl ( Tyto capensis). Ecotoxicology 22:1072–1083. https://doi.org/10.1007/s10646-013-1095-4
Bichet C, Scheifler R, Cœurdassier M, Julliard R, Sorci G, Loiseau C (2013) Urbanization, trace metal pollution, and malaria prevalence in the house Sparrow. PLoS One 8:e53866–e53866. https://doi.org/10.1371/journal.pone.0053866
Boncompagni E et al (2003) Egrets as monitors of trace-metal contamination in wetlands of Pakistan. Arch Environ Contam Toxicol 45:399–406. https://doi.org/10.1007/s00244-003-0198-y
Borghesi F et al (2017) Assessing environmental pollution in birds: a new methodological approach for interpreting bioaccumulation of trace elements in feather shafts using geochemical sediment data. Methods Ecol Evol 8:96–108. https://doi.org/10.1111/2041-210x.12644
Burger J, Gochfeld M (2000) Metals in albatross feathers from Midway Atoll: influence of species, age, and nest location. Environ Res 82:207–221. https://doi.org/10.1006/enrs.1999.4015
Chatelain M, Gasparini J, Frantz A (2016) Do trace metals select for darker birds in urban areas? An experimental exposure to lead and zinc. Glob Chang Biol 22:2380–2391. https://doi.org/10.1111/gcb.13170
Chrzan A (2016) Monitoring bioconcentration of potentially toxic trace elements in soils trophic chains.(Report) 75:1 https://doi.org/10.1007/s12665-016-5595-4
Cork SC (2000) Iron atorage diseases in birds. Avian Pathology 29:7–12. https://doi.org/10.1080/03079450094216
Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (2000) Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution? Arch Environ Contam Toxicol 39:541–546. https://doi.org/10.1007/s002440010138
Dauwe T, Janssens E, Bervoets L, Blust R, Eens M (2005) Heavy-metal concentrations in female laying great tits (Parus major) and Their Clutches. Arch Environ Contam Toxicol 49:249–256. https://doi.org/10.1007/s00244-003-0209-z
Dauwe T, Jaspers V, Covaci A, Schepens P, Eens M (2005b) Feathers as a nondestructive biomonitor for persistent organic pollutants. Environ Toxicol Chem 24:442–449. https://doi.org/10.1897/03-596.1
DeForest DK, Brix KV, Adams WJ (2007) Assessing metal bioaccumulation in aquatic environments: the inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration. Aquat Toxicol 84:236–246. https://doi.org/10.1016/j.aquatox.2007.02.022
Ding J, Yang W, Wang S, Zhang H, Yang Y, Bao X, Zhang Y (2020) Effects of environmental metal pollution on reproduction of a free-living resident songbird, the tree sparrow (Passer montanus). Sci Total Environ 721 https://doi.org/10.1016/j.scitotenv.2020.137674
Eeva T, Ryömä M, Riihimäki J (2005) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145:629–639. https://doi.org/10.1007/s00442-005-0145-x
Field DJ, D’Alba L, Vinther J, Webb SM, Gearty W, Shawkey MD (2013) Melanin concentration gradients in modern and fossil feathers (Research Article). PLoS One 8:e59451. https://doi.org/10.1371/journal.pone.0059451
Fritsch C, Jankowiak Ł, Wysocki D (2019) Exposure to Pb impairs breeding success and is associated with longer lifespan in urban European blackbirds. Sci Rep 9:486. https://doi.org/10.1038/s41598-018-36463-4
Furtado R, Pereira ME, Granadeiro JP, Catry P (2019) Body feather mercury and arsenic concentrations in five species of seabirds from the Falkland Islands. Mar Pollut Bull 149:110574. https://doi.org/10.1016/j.marpolbul.2019.110574
Gasaway WC, Buss IO (1972) Zinc toxicity in the Mallard Duck. J Wildl Manag 36:1107–1117. https://doi.org/10.2307/3799239
Giammarino M, Quatto P, Squadrone S, Abete MC (2014) The Hooded Crow (Corvus cornix) as an environmental bioindicator species of heavy metal contamination. Bull Environ Contam Toxicol 93:410–416. https://doi.org/10.1007/s00128-014-1362-y
Grúz A et al (2018) Monitoring of heavy metal burden in wild birds at eastern/north-eastern part of Hungary. Environ Sci Pollut Res 25:6378–6386. https://doi.org/10.1007/s11356-017-1004-0
Hasnat GT, Kabir MA, Hossain MA (2018) Major environmental issues and problems of South Asia, Particularly Bangladesh. In: Hussain C (ed) Handbook of environmental materials management. Springer, Cham, pp 1–40. https://doi.org/10.1007/978-3-319-58538-3_7-1
Hattingh C, Spencer JP, Venske E (2011) Economic impact of special interest tourism on Cape Town: a case study of the 2009 Mother City queer project. Afr J Phys Health Educ Recreat Dance 17:380. https://doi.org/10.4314/ajpherd.v17i3.71090
Herath D, Pitawala A, Gunatilake J (2016) Heavy metals in road deposited sediments and road dusts of Colombo capital, Sri Lanka. J Nat Sci Found Sri Lanka 44:193–202. https://doi.org/10.4038/jnsfsr.v44i2.8000
Hill L (2016) Investigation into the ecological and toxicological constraints on a population of lesser flamingos (Phoeniconaias minor) at Kamfers Dam in Kimberley, South Africa. All Dissertations. https://tigerprints.clemson.edu/all_dissertations/1841
Hoff Brait CH, AntoniosiFilho NR (2011) Use of feathers of feral pigeons (Columba livia) as a technique for metal quantification and environmental monitoring. Environ Monit Assess 179:457–467. https://doi.org/10.1007/s10661-010-1748-1
Horai S, Watanabe I, Takada H, Iwamizu Y, Hayashi T, Tanabe S, Kuno K (2007) Trace element accumulations in 13 avian species collected from the Kanto area, Japan. Sci Total Environ 373:512–525. https://doi.org/10.1016/j.scitotenv.2006.10.010
Hossain MA, Ali NM, Islam MS, Hossain HZ (2015) Spatial distribution and source apportionment of heavy metals in soils of Gebeng industrial city, Malaysia. Environ Earth Sci 73:115–126. https://doi.org/10.1007/s12665-014-3398-z
Hossen MF, Hamdan S, Rahman MR (2015) Review on the risk assessment of heavy metals in Malaysian clams. Sci World J 2015:905497–905497. https://doi.org/10.1155/2015/905497
Iqbal F, Krzeminska-Ahmadzai U, Ayub Q, Wilson R, Song BK, Fahim M, Rahman S (2021) The genetic drivers for the successful invasive potential of a generalist bird, the House crow. Biol Invasions. https://doi.org/10.1007/s10530-021-02684-4
Janaydeh M, Ismail A, Zulkifli SZ, Bejo MH, Aziz NAA, Taneenah A (2016) The use of feather as an indicator for heavy metal contamination in house crow (Corvus splendens) in the Klang area Selangor, Malaysia. Environ Sci Pollut Res 23:22059–22071. https://doi.org/10.1007/s11356-016-7223-y
Janaydeh M, Ismail A, Omar H, Zulkifli SZ, Bejo MH, Aziz NAA (2018) Relationship between Pb and Cd accumulations in house crow, their habitat, and food content from Klang area, Peninsular Malaysia. Environ Monit Assess 190:1–15. https://doi.org/10.1007/s10661-017-6416-2
Janssens E, Dauwe T, Bervoets L, Eens M (2002) Inter- and intraclutch variability in heavy metals in feathers of Great Tit nestlings ( Parus major ) Along a Pollution Gradient. Arch Environ Contam Toxicol 43:0323–0329. https://doi.org/10.1007/s00244-002-0138-2
Jaspers VL, Covaci A, Deleu P, Eens M (2009) Concentrations in bird feathers reflect regional contamination with organic pollutants. Sci Total Environ 407:1447–1451. https://doi.org/10.1016/j.scitotenv.2008.10.030
Kalisińska E, Lisowski P, Czernomysy-Furowicz D, Kavetska KM (2008) Serratospiculiasis, mycosis, and haemosiderosis in wild peregrine falcon from POLAND. Bull Vet Inst Pulawy 52:75–79
Kananke T, Wansapala J, Gunaratne A (2016) Detection of Ni, Cd, and Cu in green leafy vegetables collected from different cultivation areas in and around Colombo District, Sri Lanka. Environ Monit Assess 188:1–12. https://doi.org/10.1007/s10661-016-5195-5
Kanwal S, Abbasi NA, Chaudhry MJI, Ahmad SR, Malik RN (2020) Oxidative stress risk assessment through heavy metal and arsenic exposure in terrestrial and aquatic bird species of Pakistan. Environ Sci Pollut Res 1–15 https://doi.org/10.1007/s11356-020-07649-z
Kitowski I, Jakubas D, Wiącek D, Sujak A (2017) Concentrations of lead and other elements in the liver of the white-tailed eagle (Haliaeetus albicilla), a European flagship species, wintering in Eastern Poland. Ambio 46:825–841. https://doi.org/10.1007/s13280-017-0929-3
Kitowski I, Wiacek D, Sujak A, Komosa A, Świetlicki M (2017b) Factors affecting trace element accumulation in livers of avian species from East Poland. Turk Zool Derg 41:901–913. https://doi.org/10.3906/zoo-1606-43
Klaassen CD, Amdur MO (eds) (2013) Casarett and Doull’s toxicology: the basic science of poisons, vol 1236. McGraw-Hill, New York
Krishna IM, Manickam V, Shah A, Davergave N (2017) Environmental management: science and engineering for industry. Elsevier Science & Technology, Oxford
Krzemińska U et al (2016) Genetic diversity of native and introduced populations of the invasive house crow ( Corvus splendens ) in Asia and Africa. Biol Invasions 18:1867–1881. https://doi.org/10.1007/s10530-016-1130-5
Latif MT, Othman MR, Kim CL, Murayadi SA, Sahaimi KNA (2009) Composition of household dust in semi-urban areas in Malaysia. Indoor Built Environ 18:155–161. https://doi.org/10.1177/1420326X09103014
Malik RN, Zeb N (2009) Assessment of environmental contamination using feathers of Bubulcus ibis L., as a biomonitor of heavy metal pollution, Pakistan. Ecotoxicology 18:522–536. https://doi.org/10.1007/s10646-009-0310-9
Manjula M, Mohanraj R, Devi MP (2015) Biomonitoring of heavy metals in feathers of eleven common bird species in urban and rural environments of Tiruchirappalli, India. Environ Monit Assess 187:267. https://doi.org/10.1007/s10661-015-4502-x
Memhood T, Tianle Z, Ahmad I, Li X, Shen F, Akram W, Dong L (2018) Variations of PM2.5, PM10 mass concentration and health assessment in Islamabad, Pakistan vol 133 https://doi.org/10.1088/1755-1315/133/1/012031
Movalli PA (2000) Heavy metal and other residues in feathers of laggar falcon Falco biarmicus jugger from six districts of Pakistan. Environ Pollut 109:267–275. https://doi.org/10.1016/S0269-7491(99)00258-4
Mustafa I et al (2015) Comparative metal profiles in different organs of house sparrow (Passer domesticus) and Black Kite (Milvus migrans) in Sargodha District Punjab, Pakistan. Pak J Zool 47:97–99
World population prospects 2019: Ten key findings (2019) United Nations, Department of Economic and Social Affairs, Population Division. https://www.un.org/development/desa/pd/news/world-population-prospects-2019-0. Accessed 9 July 2020
Pataki DE (2015) Grand challenges in urban. Ecol Front Ecol Evol 3:57. https://doi.org/10.3389/fevo.2015.00057
Pollack L, Ondrasek NR, Calisi R (2017) Urban health and ecology: the promise of an avian biomonitoring tool Current. Zoology 63:205–212. https://doi.org/10.1093/cz/zox011
Qadir A, Malik RN, Husain SZ (2008) Spatio-temporal variations in water quality of Nullah Aik-tributary of the river Chenab, Pakistan. Environ Monit Assess 140:43–59. https://doi.org/10.1007/s10661-007-9846-4
Rainio MJ, Kanerva M, Salminen J-P, Nikinmaa M, Eeva T (2013) Oxidative status in nestlings of three small passerine species exposed to metal pollution. Sci Total Environ 454–455:466–473. https://doi.org/10.1016/j.scitotenv.2013.03.033
Rasheed A (2015) Measurement and analysis of fine particulate matter (PM2.5) in urban areas of Pakistan. Aerosol Air Qual Res 5:426–439. https://doi.org/10.4209/aaqr.2014.10.0269
Rehman K, Fatima F, Waheed I, Akash MSH (2018) Prevalence of exposure of heavy metals and their impact on health consequences. J Cell Biochem 119:157–184. https://doi.org/10.1002/jcb.26234
Ruuskanen S et al (2014) Large-scale geographical variation in eggshell metal and calcium content in a passerine bird (Ficedula hypoleuca). Environ Sci Pollut Res 21:3304–3317. https://doi.org/10.1007/s11356-013-2299-0
Ryall C (2016) Further records and updates of range expansion in House Crow Corvus splendens. Bull British Ornithologists’ Club 136:39–45
Sánchez-Virosta P, Espín S, García-Fernández AJ, Eeva T (2015) A review on exposure and effects of arsenic in passerine birds. Sci Total Environ 512–513:506–525. https://doi.org/10.1016/j.scitotenv.2015.01.069
Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: A review. Environ Pollut 46:263–295. https://doi.org/10.1016/0269-7491(87)90173-4
Shakir SK et al (2017) Toxic metal pollution in Pakistan and its possible risks to public health. Rev Environ Contam Toxicol 242:1–60. https://doi.org/10.1007/398_2016_9
Siddig AA, Ellison AM, Ochs A, Villar-Leeman C, Lau MK (2016) How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecol Indi 60:223–230
Summers CF, Bowerman WW, Parsons N, Chao WY, Bridges WC Jr (2014) Lead and Cadmium in the blood of nine species of seabirds, Marion Island, South Africa. Bull Environ Contam Toxicol 93:417–422. https://doi.org/10.1007/s00128-014-1359-6
Summers C (2012) Lead and cadmium in seabirds of South Africa. Dissertation, Clemson University
Taggart MA, Green AJ, Mateo R, Svanberg F, Hillström L, Meharg AA (2009) Metal levels in the bones and livers of globally threatened marbled teal and white-headed duck from El Hondo, Spain. Ecotoxicol Environ Safety 72:1–9. https://doi.org/10.1016/j.ecoenv.2008.07.015
Tasneem F, Abbasi NA, Iqbal Chaudhry MJ, Mashiatullah A, Ahmad SR, Qadir A, Malik RN (2020) Dietary proxies (δ15N, δ13C) as signature of metals and arsenic exposure in birds from aquatic and terrestrial food chains. Environ Res 183:109191. https://doi.org/10.1016/j.envres.2020a.109191
Tasneem F, Abbasi NA, Iqbal Chaudhry MJ, Mashiatullah A, Ahmad SR, Qadir A, Malik RN (2020b) Dietary proxies (δ15N, δ13C) as signature of metals and arsenic exposure in birds from aquatic and terrestrial food chains. Environ Res 183 https://doi.org/10.1016/j.envres.2020b.109191
Team RC (2020) R: A Language and Environment for Statistical Computing. Austria, Vienna
The ATSDR 2013 Substance Priority List (2013) Agency for toxic substances and disease registry. https://www.atsdr.cdc.gov/spl/resources/2013_atsdr_substance_priority_list.html. Accessed 24 Apr 2020
Bauerová P, Vinklerová J, Hraníček J, Čorba V, Vojtek L, Svobodová J, Vinkler M (2017) Associations of urban environmental pollution with health-related physiological traits in a free-living bird species. Sci Total Environ 601–602:1556–1565. https://doi.org/10.1016/j.scitotenv.2017.05.276
Ullah K, Hashmi MZ, Malik RN (2014) Heavy-metal levels in feathers of cattle egret and their surrounding environment: a case of the Punjab Province, Pakistan. Arch Environ Contam Toxicol 66:139–153. https://doi.org/10.1007/s00244-013-9939-8
van der Schyff V, Pieters R, Bouwman H (2016) The heron that laid the golden egg: metals and metalloids in ibis, darter, cormorant, heron, and egret eggs from the Vaal River catchment, South Africa. Environ Monit Assess 188:1–7. https://doi.org/10.1007/s10661-016-5378-0
Van Wyk E, Van Der Bank FH, Verdoorn GH, Hofmann D (2001) Selected mineral and heavy metal concentrations in blood and tissues of vultures in different regions of South Africa. South African J Anim Sci 31:57–63. https://doi.org/10.4314/sajas.v31i2.3831
Wallensten A (2007) Influenza virus in wild birds and mammals other than man. Microb Ecol Health Dis 19:122–139. https://doi.org/10.1080/08910600701406786
Wen J, Yi Y, Zeng G (2016) Effects of modified zeolite on the removal and stabilization of heavy metals in contaminated lake sediment using BCR sequential extraction. J Environ Manage 178:63–69. https://doi.org/10.1016/j.jenvman.2016.04.046
Wilson R, Sarim D, Rahman S (2015) Factors influencing the distribution of the invasive house crow ( Corvus splendens ) in rural and urban landscapes. Urban Ecosyst 18:1389–1400. https://doi.org/10.1007/s11252-015-0448-6
Nighat S, Iqbal S, Nadeem MS, Mahmood T, Shah SI (2013) Estimation of heavy metal residues from the feathers of Falconidae Accipitridae, and Strigidae in Punjab, Pakistan. Turk Zool Derg 37:488–500. https://doi.org/10.3906/zoo-1112-1
Wu Y (2017) Chapter 3—indicators for monitoring aquatic ecosystem. In: Wu Y (ed) Periphyton. Elsevier, Boston, pp 71–106. https://doi.org/10.1016/B978-0-12-801077-8.00003-X
Yasmeen R, Muhammad H, Bokhari S, Rafi U, Shakoor A, Qurashi A (2019) Assessment of heavy metals in different organs of cattle egrets ( Bubulcus ibis ) from a rural and urban environment in Pakistan. Environ Sci Pollut Res 26:13095–13102. https://doi.org/10.1007/s11356-019-04814-x
Yen LJ et al (2017) Characteristics of water quality of rivers related to land-use in Penang Island Malaysia. In: AIP Conference Proceedings, vol 1. AIP Publishing LLC, p 040008. https://doi.org/10.1063/1.5005688
Acknowledgements
We are highly thankful to Muhammad Farooq Sabar, University of The Punjab and WWF Pakistan for providing support during field sampling in Pakistan. The authors wish to express gratitude to Ms Nur Liyana Afifah Zar Khan, Technical Officer in Civil Engineering Laboratory, Monash University Malaysia, for her assistance in the metal analysis.
Funding
This research was supported by University Graduate Research Grant from the School of Science, Monash University Malaysia. This study was done as the part of the PhD project of the first author in the Monash University Malaysia.
Author information
Authors and Affiliations
Contributions
FI participated in sample collection, performance and optimization of analysis and manuscript writing. RW, QA, BKS and SR participated in development of ideas and commented on manuscript. UKA, AT and AAH provided field data, samples and technical support. All the authors read and approve the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
This study did not involve any protected or endangered species, and no specific permissions were required for the sampling on the collection localities. Legal requirements were followed for dispatching of feathers from sampling countries to Monash University Malaysia for the analysis.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Iqbal, F., Wilson, R., Ayub, Q. et al. Biomonitoring of heavy metals in the feathers of House crow (Corvus splendens) from some metropolitans of Asia and Africa. Environ Sci Pollut Res 30, 35715–35726 (2023). https://doi.org/10.1007/s11356-022-24712-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-24712-z