Skip to main content
SpringerLink
Log in

Monitoring of non-destructive sampling strategies to assess the exposure of avian species in Jiangsu Province, China to heavy metals

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

To assess the exposure of avian species in Jiangsu Province, China to eight heavy metals (As, Cd, Cr, Cu, Hg, Ni, Pb and Zn), the flight feathers, eggshells and feces of total ten avian species (including four herons, four cranes, one stork and one gull) were collected during March to May in 2012. The total concentrations of As, Cd and Hg were measured by Atomic Fluorescence Spectrometer; Cr, Cu, Ni, Pb and Zn were measured by inductively coupled plasma optical emission spectrometer. The determined concentrations of Cr (3.94, 1.33–8.30 mg kg−1), Cu (15.02, 7.34–35.53 mg kg−1) and Zn (134.66, 77.26–242.25 mg kg−1) in fresh feathers and Cd (7.93, 7.44–9.12 mg kg−1), Ni (22.74, 19.38–24.71 mg kg−1), Pb (85.06, 78.72–91.95 mg kg−1) and Zn (63.54, 55.82–72.14 mg kg−1) in eggshells were higher than the mean values of other reported data, indicating a considerable heavy metal pollution status in local area. Comparing to the heavy metal levels in early historic feathers (1992–2000), a significant elevation of concentrations has been observed in recent bird feathers. For feathers of Grus japonensis, the heavy metal concentrations increased by 19–267%. This increased tendency was consistent with local GDP (Gross Domestic Products) development. The anthropogenic economic activity especially industrial development may be a critical reason that caused the increase of heavy metal levels in local avian species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Al-Shawi AW, Dahl R (1999) The determination of cadmium and six other heavy metals in nitrate phosphate fertilizer solution by ion chromatography. Anal Chim Acta 391:35–42

    Article  CAS  Google Scholar 

  • Ayas Z (2007) Trace element residues in eggshells of grey heron (Ardea cinerea) and black-crowned night heron (Nycticorax nycticorax) from Nallihan Bird Paradise, Ankara-Turkey. Ecotoxicology 16:347–352

    Article  CAS  Google Scholar 

  • Ayas Z, Celikkan H, Aksu ML (2008) Lead (Pb) and copper (Cu) concentration in the eggshells of Audouin's gulls (Larus audouinii) in Turkey. Turk J Zool 32:379–384

    CAS  Google Scholar 

  • Barak NAE, Mason CF (1989) Heavy metals in water, sediment and invertebrates from rives in Eastern England. Chemosphere 19:1709–1714

    Article  CAS  Google Scholar 

  • Berglund AMM, Koivula MJ, Eeva T (2011) Species- and age-related variation in metal exposure and accumulation of two passerine bird species. Environ Pollut 159:2368–2374

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (1997) Heavy metal and selenium concentrations in feathers of egrets from Bali and Sulawesi, Indonesia. Arch Environ Con Tox 32:217–221

    Article  CAS  Google Scholar 

  • Burger J, Eichhorst B (2007) Heavy metals and selenium in grebe feathers from Agassiz National Wildlife Refuge in northern Minnesota. Arch Environ Con Tox 53:442–449

    Article  CAS  Google Scholar 

  • Cheng SP (2003) Heavy metal pollution in China: origin, pattern and control. Environ Sci Pollut Res 10:192–198

    Google Scholar 

  • Costagliola P, Benvenuti M, Chiarantini L, Bianchi S, Di Benedetto F, Paolieri M, Rossato L (2008) Impact of ancient metal smelting on arsenic pollution in the Pecora River Valley, Southern Tuscany, Italy. Appl Geochem 23:1241–1259

    Article  CAS  Google Scholar 

  • Cui BS, Zhang QJ, Zhang KJ, Liu XH, Zhang HG (2011) Analyzing trophic transfer of heavy metals for food webs in the newly-formed wetlands of the Yellow River Delta, China. Environ Pollut 159:1297–1306

    Article  CAS  Google Scholar 

  • Currie D, Valkama J (1998) Limited effects of heavy metal pollution on foraging and breeding success in the curlew (Numenius arquata). Environ Pollut 101:253–261

    Article  CAS  Google Scholar 

  • Dauwe T, Bervoets L, Blust R, Pinxten R, Eens M (1999) Are eggshells and egg contents of Great and Blue Tits suitable as indicators of heavy metal pollution? Belg J Zool 129:439–447

    Google Scholar 

  • 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 Con Tox 39:541–546

    Article  CAS  Google Scholar 

  • Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–436

    Article  CAS  Google Scholar 

  • Dauwe T, Janssens E, Bervoets L, Blust R, Eens M (2004) Relationships between metal concentrations in great tit nestlings and their environment and food. Environ Pollut 131:373–380

    Article  CAS  Google Scholar 

  • 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 Con Tox 49:249–256

    Article  CAS  Google Scholar 

  • Denneman WD, Douben PET (1993) Trace metals in primary feathers of the Barn Owl (Tyto alba guttatus) in The Netherlands. Environ Pollut 82:301–310

    Article  CAS  Google Scholar 

  • Fasola M, Movalli PA, Gandini C (1998) Heavy metal, organochlorine pesticide, and PCB residues in eggs and feathers of herons breeding in northern Italy. Arch Environ Con Tox 34:87–93

    Article  CAS  Google Scholar 

  • Fei YL (2011) Study on bird species diversity and geographical distribution patterns in Jiangsu Province. Nanjing Forestry University, Nanjing

    Google Scholar 

  • Frantz A, Pottier M-A, Karimi B, Corbel H, Aubry E, Haussy C, Gasparini J, Castrec-Rouelle M (2012) Contrasting levels of heavy metals in the feathers of urban pigeons from close habitats suggest limited movements at a restricted scale. Environ Pollut 168:23–28

    Article  CAS  Google Scholar 

  • Fu J, Hu X, Tao XC, Yu HX, Zhang XW (2013a) Risk and toxicity assessments of heavy metals in sediments and fishes from the Yangtze River and Taihu Lake, China. Chemosphere (in press)

  • Fu J, Zheng XM, Zhu DD, Wang H, Reduwan Billah SM, Yu HX, Zhang XW (2013b) Heavy metals in seawater, sediments and biota from the coastal area of Yangcheng, China. PLoS ONE (under review)

  • GarciaFernandez AJ, MotasGuzman M, Navas I, MariaMojica P, Luna A, SanchezGarcia JA (1997) Environmental exposure and distribution of lead in four species of raptors in Southeastern Spain. Arch Environ Con Tox 33:76–82

    Article  CAS  Google Scholar 

  • Hashmi MZ, Malik RN, Shahbaz M (2013) Heavy metals in eggshells of cattle egret (Bubulcus ibis) and little egret (Egretta garzetta) from the Punjab province, Pakistan. Ecotox Environ Safe 89:158–165

    Article  CAS  Google Scholar 

  • Ikemoto T, Kunito T, Tanabe S, Tsurumi M, Sato F, Oka N (2005) Non-destructive monitoring of trace element levels in short-tailed albatrosses (Phoebastria albatrus) and black-footed albatrosses (Phoebastria nigripes) from Torishima Island, Japan using eggs and blood. Mar Pollut Bull 51:889–895

    Article  CAS  Google Scholar 

  • Janssens E, Dauwe T, Bervoets L, Eens M (2001) Heavy metals and selenium in feathers of great tits (Parus major) along a pollution gradient. Environ Toxicol Chem 20:2815–2820

    Article  CAS  Google Scholar 

  • 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 Con Tox 43:323–329

    Article  CAS  Google Scholar 

  • Jaspers V, Dauwe T, Pinxten R, Bervoets L, Blust R, Eens M (2004) The importance of exogenous contamination on heavy metal levels in bird feathers. A field experiment with free-living great tits, Parus major. J Environ Monit 6:356–360

    Article  Google Scholar 

  • Kim J, Koo TH (2007) The use of feathers to monitor heavy metal contamination in Herons, Korea. Arch Environ Con Tox 53:435–441

    Article  CAS  Google Scholar 

  • Kim J, Koo T-H (2008) Heavy metal concentrations in feathers of Korean shorebirds. Arch Environ Con Tox 55:122–128

    Article  CAS  Google Scholar 

  • Lam JCW, Tanabe S, Lam MHW, Lam PKS (2005) Risk to breeding success of waterbirds by contaminants in Hong Kong: evidence from trace elements in eggs. Environ Pollut 135:481–490

    Article  CAS  Google Scholar 

  • Landaburu-Aguirre J, Pongracz E, Sarpola A, Keiski RL (2012) Simultaneous removal of heavy metals from phosphorous rich real wastewaters by micellar-enhanced ultrafiltration. Sep Purif Technol 88:130–137

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mandal BK, Suzuki KT (2002) Arsenic round the world: a review. Talanta 58:201–235

    Article  CAS  Google Scholar 

  • Mansouri B, Babaei H, Hoshyari E (2012) Heavy metal contamination in feathers of Western Reef Heron (Egretta gularis) and Siberian gull (Larus heuglini) from Hara biosphere reserve of Southern Iran. Environ Monit Assess 184:6139–6145

    Article  CAS  Google Scholar 

  • Martinez A, Crespo D, Angel Fernandez J, Aboal JR, Carballeira A (2012) Selection of flight feathers from Buteo buteo and Accipiter gentilis for use in biomonitoring heavy metal contamination. Sci Total Environ 425:254–261

    Article  CAS  Google Scholar 

  • Metcheva R, Yurukova L, Teodorova S, Nikolova E (2006) The penguin feathers as bioindicator of Antarctica environmental state. Sci Total Environ 362:259–265

    Article  CAS  Google Scholar 

  • Mora MA (2003) Heavy metals and metalloids in egg contents and eggshells of passerine birds from Arizona. Environ Pollut 125:393–400

    Article  CAS  Google Scholar 

  • Moreno R, Jover L, Diez C, Sanpera C (2011) Seabird feathers as monitors of the levels and persistence of heavy metal pollution after the Prestige oil spill. Environ Pollut 159:2454–2460

    Article  CAS  Google Scholar 

  • Morera M, Sanpera C, Crespo S, Jover L, Ruiz X (1997) Inter- and intraclutch variability in heavy metals and selenium levels in Audouin's gull eggs from the Ebro Delta, Spain. Arch Environ Con Tox 33:71–75

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Mukherjee AB, Zevenhoven R, Brodersen J, Hylander LD, Bhattacharya P (2004) Mercury in waste in the European Union: sources, disposal methods and risks. Resour Conserv Recy 42:155–182

    Article  Google Scholar 

  • Muralidharan S, Jayakumar R, Vishnu G (2004) Heavy metals in feathers of six species of birds in the district Nilgiris, India. B Environ Contam Tox 73:285–291

    Article  CAS  Google Scholar 

  • Orlowski G, Kasprzykowski Z, Dobicki W, Pokorny P, Polechonski R (2010) Geographical and habitat differences in concentrations of copper, zinc and arsenic in eggshells of the Rook Corvus frugilegus in Poland. J Ornithol 151:279–286

    Article  Google Scholar 

  • Otones V, Alvarez-Ayuso E, Garcia-Sanchez A, Santa-Regina I, Murciego A (2011) Arsenic distribution in soils and plants of an arsenic impacted former mining area. Environ Pollut 159:2637–2647

    Article  CAS  Google Scholar 

  • Pain DJ, Burneleau G, Bavoux C, Wyatt C (1999) Levels of polychlorinated biphenlyls, organochlorine pesticides, mercury and lead in relation to shell thickness in marsh harrier (Circus aeruginosus) eggs from Charente-Maritime, France. Environ Pollut 104:61–68

    Article  CAS  Google Scholar 

  • Scheifler R, Coeurdassier M, Morilhat C, Bernard N, Faivre B, Flicoteaux P, Giraudoux P, Noel M, Piotte P, Rieffel D, de Vaufleury A, Badot PM (2006) Lead concentrations in feathers and blood of common blackbirds (Turdus merula) and in earthworms inhabiting unpolluted and moderately polluted urban areas. Sci Total Environ 371:197–205

    Article  CAS  Google Scholar 

  • Shrestha S, Kazama F (2007) Assessment of surface water quality using multivariate statistical techniques: a case study of the Fuji river basin, Japan. Environ Model Softw 22:464–475

    Article  Google Scholar 

  • Swaileh KM, Sansur R (2006) Monitoring urban heavy metal pollution using the House Sparrow (Passer domesticus). J Environ Monitor 8:209–213

    Article  CAS  Google Scholar 

  • Wang XY, Chen XL, Lin QX, Fang Y, Fang WZ (2009) Heavy metal contents and distribution in the eggs of Chinese egret (Egretta eulophotes) in Fujian. J Xiamen Univ (Natl Sci) 48:606–609

    CAS  Google Scholar 

  • Yi Y, Wang Z, Zhang K, Yu G, Duan X (2008) Sediment pollution and its effect on fish through food chain in the Yangtze River. Int J Sed Res 23:338–347

    Article  Google Scholar 

  • Yi YJ, Yang ZF, Zhang SH (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159:2575–2585

    Article  CAS  Google Scholar 

  • Zhong XL, Zhou SL, Zhu Q, Zhao QG (2011) Fraction distribution and bioavailability of soil heavy metals in the Yangtze River Delta—a case study of Kunshan City in Jiangsu Province, China. J Hazard Mater 198:13–21

    Article  CAS  Google Scholar 

  • Zhou LZ, Li JH, Yin HB, Chang W, Wang X, Liu Q, Xu SQ, Gui XQ, Yan RW (2005) Enrichment characteristics of heavy metals in heron eggs. Chin J Appl Ecol 16:1932–1937

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Jiangsu Planned Projects for Postdoctoral Research Funds (No. 1102002C), Scientific Research Projects of Jiangsu Environmental Protection (No. 201135) and China Postdoctoral Science Foundation Funds (No. 2012M510131).

Author information

Authors and Affiliations

  1. State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, 210046, China

    Jie Fu, Hongxia Yu & Xiaowei Zhang

  2. School of Chemistry and Life Science, Nanjing University Jinling College, Nanjing, 210089, China

    Qing Wang

  3. Administration of Yancheng National Natural Reserve, Yancheng, 224002, China

    Hui Wang

Authors
  1. Jie Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongxia Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaowei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiaowei Zhang.

Additional information

Responsible editor: Vera Slaveykova

Electronic supplementary material

Supplementary data include heavy metal concentrations in bird feathers (Table S1) and eggshells (Table S2) from open publications, component matrix of PCA for elements in fresh feathers (Table S3), correlation of element concentrations in fresh feathers (Table S4), and hierarchical dendogram for the concentration changes of heavy metals in feathers of Grus japonensis during the past two decades (1992–2012) (Fig. S1).

ESM 1

(DOC 223 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fu, J., Wang, Q., Wang, H. et al. Monitoring of non-destructive sampling strategies to assess the exposure of avian species in Jiangsu Province, China to heavy metals. Environ Sci Pollut Res 21, 2898–2906 (2014). https://doi.org/10.1007/s11356-013-2242-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2242-4

Keywords

Search

Navigation