Skip to main content
SpringerLink
Log in

Heavy metals in liver, kidney, brain, and muscle slender-billed gull (Chroicocephalus genei) from south-eastern Iran

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

Abstract

The concentrations of four heavy metals nickel (Ni), cadmium (Cd), lead (Pb), and zinc (Zn) were determined in liver, kidney, muscle, and brain tissues of 40 slender-billed gulls (Chroicocephalus genei) from the Chahnimeh water reservoirs of Sistan and the Oman Sea coast of Iran. There were significant differences between Ni, Cd, Pb, and Zn concentrations observed in the liver and brains of birds from the Oman Sea coast than in the liver and brains of gulls from the Chahnimeh water reservoirs (P < 0.05). Higher levels of Pb, Cd, and Zn were found in the brain and liver of gulls than in the kidney and muscles tissues. There were significant gender differences in heavy metals in liver and brain tissue. In gulls from the coast of Oman Sea, all four elements (Cd, Pb, Ni, and Zn) were positively correlated with levels in all organs, and except for muscle, the elements were positively correlated with the other elements in the other tissues (except Ni in the brain). Thus, the pathways and sources of entry for the elements are similar, and the pathways for accumulation of these elements, and the reactions of different organs of the body to these elements, are very similar. Also, 40% of gulls in Oman Sea coast had levels of lead in the brain (>5 μg g−1 −1 d.w) that were above the adverse effect levels, Ni concentrations in the liver of slender-billed gull in Oman Sea coast (100 %) and Chahnimeh water reservoirs (90 %) were above toxic levels (> 3 μg g−1 d.w), and 80% of Ni concentration in kidneys in gulls from the Oman Sea coast and Chahnimeh water reservoirs were higher than the toxicity levels (> 10 μg g−1 d.w).

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

Similar content being viewed by others

Data Availability

The authors declared that the data and materials for this work are available.

References

  • Agah H, Saleh A, Bastami KD, Fumani NS (2016) Ecological risk, source and preliminary assessment of metals in the surface sediments of Chabahar Bay, Oman Sea. Mar Pollut Bull 107:383–388. https://doi.org/10.1016/j.marpolbul.2016.03.042

    Article  CAS  Google Scholar 

  • Agusa T, Matsumoto T, Ikemoto T, Anan Y, Kubota R, Yasunaga G, Kunito T, Tanabe S, Ogi H, Shibata Y (2005) Body distribution of trace element in Black-Tailed gull from Rishiri island, Japan: age depended accumulation and transfer to feathers and eggs. Environ Toxicol Chem 24:2107–2120. https://doi.org/10.1897/04-617R.1

    Article  CAS  Google Scholar 

  • Alipour H, Solgi E, Majnouni F (2016) Concentrations of heavy metals in tissues of the Mallard Anas platyrhynchos in Kanibarazan, northwestern Iran. Podoces 11:35–42

    Google Scholar 

  • Amini-Ranjbar GH, Miraki GH (2006) Evaluation of quantity and quality of the Chabahar bay. Sistan Baluchestan Univ:7–9

  • Barbieri E, de Andrade PE, Filippini A et al (2010) Assessment of trace metal concentration in feathers of seabird (Larus dominicanus) sampled in the Florianópolis, SC, Brazilian coast. Environ Monit Assess 169:631–638

    Article  CAS  Google Scholar 

  • Behrooz RD, Sahebi S, Majnoni F, Ahmadpour M, Hoseini SH (2013) Mercury contamination in commercial fresh and salt water fish of the Zabol Chahnimeh reservoirs and the Gulf of Oman (Iran). Food Addit Contam Part B 6:175–180. https://doi.org/10.1080/19393210.2013.779322

    Article  Google Scholar 

  • Berny PJ, Cote LM, Buck WB (1994) Relationship between soil lead, dust lead, and blood lead concentrations in pets and their owners: evaluation of soil lead threshold values. Environ Res 67:84–97

    Article  CAS  Google Scholar 

  • Beyer WN, Dalgarn J, Dudding S, French JB, Mateo R, Miesner J, Sileo L, Spann J (2004) Zinc and lead poisoning in wild birds in the tri-state mining district (Oklahoma, Kansas, and Missouri). Arch Environ Contam Toxicol 48:108–117. https://doi.org/10.1007/s00244-004-0010-7

    Article  CAS  Google Scholar 

  • Beyer WN, Meador JP (2011) Environmental contaminants in biota: interpreting tissue concentrations. CRC Press

  • Braune BM, Scheuhammer MA (2008) Trace element and metallothionein concentrations in seabirds from the Canadian arctic. Environ Toxicol Chem 27:645–651. https://doi.org/10.1897/07-269.1

    Article  CAS  Google Scholar 

  • Braune BM, Simon M (2004) Trace elements and halogenated organic compounds in Canadian Arctic seabirds. Mar Pollut Bull 48:986–992

    Article  CAS  Google Scholar 

  • Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311

    Google Scholar 

  • Burger J, Gochfeld M (2016) Habitat, population dynamics, and metal levels in colonial waterbirds: a food chain approach. CRC Press

  • Carpenter JW, Andrews GA, Beyer WN (2004) Zinc toxicosis in a free-flying trumpeter swan (Cygnus buccinator). J Wildl Dis 40:769–774

    Article  Google Scholar 

  • Clark AJ, Scheuhammer AM (2003) Lead poisoning in upland-foraging birds of prey in Canada. Ecotoxicology 12:23–30

    Article  CAS  Google Scholar 

  • Dauwe T, Janssens E, Kempenaers B, Eens M (2004) The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environ Pollut 129:125–129

    Article  CAS  Google Scholar 

  • Degernes LA (2008) Waterfowl toxicology: a review. Vet Clin North Am Exot Anim Pract 11:283–300

    Article  Google Scholar 

  • Einollahi Peer F, Safahieh A, Sohrab DA, Pakzad Tochi S (2010) Heavy metal concentrations in rock oyster Socostrea cucullata from Iranian coasts of the Oman Sea. Trakia J Sci 8:79–86

    Google Scholar 

  • Eisler R (2000) Handbook of chemical risk assessment: health hazards to humans, plants, and animals, three volume set. CRC press

  • Elliott JE, Scheuhammer AM, Leighton FA, Pearce PA (1992) Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch Environ Contam Toxicol 22:63–73. https://doi.org/10.1007/BF00213303

    Article  CAS  Google Scholar 

  • Erwin RM, Custer TW (2000) Herons as indicators

  • Furness RW (1996) Cadmium in birds. Environ Contam Wildl Interpret tissue Conc Lewis, Boca Raton, pp 389–404

    Google Scholar 

  • Gochfeld M (1997) Factors influencing susceptibility to metals. Environ Health Perspect 105:817–822

    CAS  Google Scholar 

  • Gochfeld M, Belant JL, Shukla T, Benson T, Burger J (1996) Heavy metals in laughing gulls: gender, age and tissue differences. Environ Toxicol Chem 15:2275–2283

    Article  CAS  Google Scholar 

  • Gochfeld M, Burger J (1987) Heavy metal concentrations in the liver of three duck species: influence of species and sex. Environ Pollut 45:1–15

    Article  CAS  Google Scholar 

  • Gomez G, Baos R, Gomara B et al (2004) Influence of a mine tailing accident near Dooana National Park (Spain) on heavy metals and arsenic accumulation in 14 species of waterfowl (1998 to 2000). Arch Environ Contam Toxicol 47:521–529. https://doi.org/10.1007/s00244-004-0189-z

    Article  CAS  Google Scholar 

  • Grue CE, Hoffman DJ, Beyer WN, Franson LP (1986) Lead concentrations and reproductive success in European starlings Sturnus vulgaris nesting within highway roadside verges. Environ Pollut Ser A, Ecol Biol 42:157–182

    Article  CAS  Google Scholar 

  • Hamzeh MA, Shah-hosseini M, Naderi Beni A (2013) Effect of fishing vessels on trace metal contamination in sediments of three harbors along Iranian Oman Sea coast. Environ Monit Assess 185:1791–1807. https://doi.org/10.1007/s10661-012-2668-z

    Article  CAS  Google Scholar 

  • Havera SP, Wood SG, Georgi MM (1992) Blood and tissue parameters in wild mallards redosed with lead shot. Bull Environ Contam Toxicol 49:238–245

    Article  CAS  Google Scholar 

  • Hindell MA, Brothers N, Gales R (1999) Mercury and cadmium concentrations in the tissues of three species of southern albatrosses. Polar Biol 22:102–108

    Article  Google Scholar 

  • Hoshyari E, Pourkhabbaz A, Mansouri B (2012) Contaminations of metal in tissues of Siberian gull Larus heuglini: gender, age, and tissue differences. Bull Environ Contam Toxicol 89:102–106. https://doi.org/10.1007/s00128-012-0655-2

    Article  CAS  Google Scholar 

  • Hulse M, Mahoney JS, Schroder GD, Hacker CS, Pier SM (1980) Environmentally acquired lead, cadmium, and manganese in the cattle egret, Bubulcus ibis, and the laughing gull, Larus atricilla. Arch Environ Contam Toxicol 9:65–77

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kalisinska E (2000) Lead and other heavy metals in the brain of geese hunted in the vicinity of Slonsk, Poland. Biol Bull Poznań 37:273–286

    CAS  Google Scholar 

  • Kalisińska E, Salicki W, Kavetska KM, Ligocki M (2007) Trace metal concentrations are higher in cartilage than in bones of scaup and pochard wintering in Poland. Sci Total Environ 388:90–103

    Article  Google Scholar 

  • Kim E-Y, Ichihashi H, Saeki K, Atrashkevich G, Tanabe S, Tatsukawa R (1996) Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia. Environ Pollut 92:247–252. https://doi.org/10.1016/0269-7491(96)00007-3

    Article  CAS  Google Scholar 

  • Leonzio C, Fossi C, Focardi S (1986a) Lead, mercury, cadmium and selenium in two species of gull feeding on inland dumps , and in marine areas. Sci Total Environ 57:121–127

    Article  CAS  Google Scholar 

  • Leonzio C, Fossi C, Focardi S (1986b) Heavy metals and selenium variation in a migratory bird wintering in a mercurypolluted lagoon. Bull Environ Contam Toxicol 37(2):219–225

  • Lucia M, André J-MM, Gontier K, Diot N, Veiga J, Davail S (2010) Trace element concentrations (mercury, cadmium, copper, zinc, lead, aluminium, nickel, arsenic, and selenium) in some aquatic birds of the Southwest Atlantic Coast of France. Arch Environ Contam Toxicol 58:844–853. https://doi.org/10.1007/s00244-009-9393-9

    Article  CAS  Google Scholar 

  • Malinga M, Szefer P, Gabrielsen GW (2010) Age, sex and spatial dependent variations in heavy metals levels in the Glaucous Gulls (Larus hyperboreus) from the Bjørnøya and Jan Mayen, Arctic. Environ Monit Assess 169:407–416. https://doi.org/10.1007/s10661-009-1183-3

    Article  CAS  Google Scholar 

  • Mansouri B, Babaei H, Hoshyari E et al (2012a) Assessment of trace-metal concentrations in western reef heron (Egrettagularis) and Siberian gull (Larusheuglini) from southern Iran. Arch Environ Contam Toxicol 63:280–287

    Article  CAS  Google Scholar 

  • Mansouri B, Babaei H, Hoshyari E et al (2012b) Assessment of trace-metal concentrations in western reef heron (Egretta gularis) and Siberian gull (Larus heuglini) from Southern Iran. Arch Environ Contam Toxicol 63:280–287. https://doi.org/10.1007/s00244-012-9762-7

    Article  CAS  Google Scholar 

  • Martin MB, Reiter R, Pham T, Avellanet YR, Camara J, Lahm M, Pentecost E, Pratap K, Gilmore BA, Divekar S, Dagata RS, Bull JL, Stoica A (2003) Estrogen-like activity of metals in MCF-7 breast cancer cells. Endocrinology 144:2425–2436

    Article  CAS  Google Scholar 

  • Mateo R, Beyer WN, Spann J, Hoffman D, Ramis A (2003) Relationship between oxidative stress, pathology, and behavioral signs of lead poisoning in mallards. J Toxicol Environ Heal Part A 66:1371–1389

    Article  CAS  Google Scholar 

  • Morris CM, Candy JM, Oakley AE, Bloxham CA, Edwardson JA (1992) Histochemical distribution of non-haem iron in the human brain. Cells Tissues Organs 144:235–257

    Article  CAS  Google Scholar 

  • Nergiz H (2019) Assessment of heavy metal concentration in fathers of armenian gull (Larus armenicus buturlin, 1934) and water samples of Hazar lake, Turky. Appl Ecol Environ Res 17:10221–10227. https://doi.org/10.15666/aeer/1704_1022110227

    Article  Google Scholar 

  • Nicholson JK (1981) The comparative distribution of zinc, cadmium and mercury in selected tissues of the herring gull (Larus argentatus). Comp Biochem Physiol Part C Comp Pharmacol 68:91–94. https://doi.org/10.1016/0306-4492(81)90042-3

    Article  Google Scholar 

  • Orlić I, Tang SM (1999) Elemental depth profiles in marine sediments of Singapore coastal waters. Nucl Inst Methods Phys Res Sect B Beam Interact Mater Atoms 150:291–297

    Article  Google Scholar 

  • Orlowski G, Polechonski R, Dobicki W, Zawada Z (2008) Heavy metal concentrations in the tissues of the Black-Headed gull Larus Ridibundus L. Nesting in the Dam Reservoir in south-western Poland. Pol J Ecol 55:783–793

    Google Scholar 

  • Outridge PM, Scheuhammer AM (1993) Bioaccumulation and toxicology of nickel: implications for wild mammals and birds. Environ Rev 1:172–197

    Article  CAS  Google Scholar 

  • Rice DC (1992) Behavioral effects of lead in monkeys tested during infancy and adulthood. Neurotoxicol Teratol 14:235–245

    Article  CAS  Google Scholar 

  • Savinov VM, Gabrielsen GW, Savinova TN (2003) Cadmium, zinc, copper, arsenic, selenium and mercury in seabirds from the Barents Sea: levels, inter-specific and geographical differences. Sci Total Environ 306:133–158. https://doi.org/10.1016/S0048-9697(02)00489-8

    Article  CAS  Google Scholar 

  • Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295

    Article  CAS  Google Scholar 

  • Schummer ML, Petrie SA, Badzinski SS, Deming M, Chen YW, Belzile N (2011) Elemental contaminants in livers of mute swans on Lakes Erie and St. Clair. Arch Environ Contam Toxicol 61:677–687

    Article  CAS  Google Scholar 

  • Sileo L, Nelson Beyer W, Mateo R (2003) Pancreatitis in wild zinc-poisoned waterfowl. Avian Pathol 32:655–660

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Szefer P, Falandysz J (1987) Trace metals in the soft tissues of scaup ducks (Aythya marila L.) wintering in Gdańsk Bay, Baltic Sea. Sci Total Environ 65:203–213

    Article  CAS  Google Scholar 

  • Szymczyk K, Zalewski K (2003) Copper, zinc, lead and cadmium content in liver and muscles of mallards (Anas Platyrhychnos) and other hunting fowl species in Warmia and Mazury in 1999-2000. Pol J Environ Stud 12:381–386

    CAS  Google Scholar 

  • Taggart MA, Figuerola J, Green AJ, Mateo R, Deacon C, Osborn D, Meharg AA (2006) After the Aznalcóllar mine spill: arsenic, zinc, selenium, lead and copper levels in the livers and bones of five waterfowl species. Environ Res 100:349–361. https://doi.org/10.1016/j.envres.2005.07.009

    Article  CAS  Google Scholar 

  • 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 Saf 72:1–9. https://doi.org/10.1016/j.ecoenv.2008.07.015

    Article  CAS  Google Scholar 

  • Takekawa JY, Wainwright-De La Cruz SE, Hothem RL, Yee J (2002) Relating body condition to inorganic contaminant concentrations of diving ducks wintering in coastal California. Arch Environ Contam Toxicol 42:60–70

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vaneeden PH, Schoonbee HJ (1992) Concentrations of heavy metals in organs and tissues of the redknobbed coot. Ostrich 63:165–171

    Google Scholar 

  • Vizuete J, Pérez-López M, Míguez-Santiyán MP, Hernández-Moreno D (2018) Mercury (Hg), lead (Pb), cadmium (Cd), selenium (Se), and arsenic (As) in liver, kidney, and feathers of gulls: a review. In: Reviews of Environmental Contamination and Toxicology. pp 85–146

  • Zaccaroni A, Amorena M, Naso B, Castellani G, Lucisano A, Stracciari GL (2003) Cadmium, chromium and lead contamination of Athene noctua, the little owl, of Bologna and Parma, Italy. Chemosphere 52:1251–1258

    Article  CAS  Google Scholar 

  • Zhang J, Han L, Ji Y et al (2018) Heavy metal investigation and risk assessment along the Le’An River from non-ferrous metal mining and smelting activities in Poyang, China. J Environ Biol 39:536–545

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by the University of Zabol, Project code PR-UOZ 99-4.

Author information

Authors and Affiliations

  1. Department of Environmental Sciences, Faculty of Natural Resources, University of Zabol, Zabol, Sistan, Iran

    Reza Dahmardeh Behrooz

  2. Division of Life Sciences, Rutgers University, 604 Allison Road, Piscataway, NJ, 08854-8082, USA

    Joanna Burger

  3. Environmental and Occupational Health Sciences Institute, and NIEHS Center, Piscataway, NJ, 08854, USA

    Joanna Burger

Authors
  1. Reza Dahmardeh Behrooz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanna Burger
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, formal analysis, data curation, investigation, Reza Dahmardeh Behrooz; methodology, review and editing, Joanna Burger. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Reza Dahmardeh Behrooz.

Ethics declarations

Ethics approval and consent to participate

All procedures performed in studies involving collection of birds and people who participated in this study were in accordance with the ethical standards of the institutional and/or national research committee University of Zabol with reference number IR.UOZ.REC.1399.005.

Consent for publication

I understand that the text and any pictures published in the article will be freely available on the internet and may be seen by the general public. The pictures and text may also appear on other websites or in print and may be translated into other languages or used for commercial purposes.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: V.V.S.S. Sarma

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dahmardeh Behrooz, R., Burger, J. Heavy metals in liver, kidney, brain, and muscle slender-billed gull (Chroicocephalus genei) from south-eastern Iran. Environ Sci Pollut Res 29, 10319–10331 (2022). https://doi.org/10.1007/s11356-021-16029-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-16029-0

Keywords

Search

Navigation