Evaluation of heavy metal (As, Hg, Zn, Cu and Se) levels in wild birds of prey and aquatic habitats

• Zozan Garip Harran University, Faculty of Veterinary Medicine, Department of Pharmacology and Toxicology. Sanlıurfa, Türkiye
• Reşat Ektiren Harran University, Faculty of Veterinary Medicine, Department of Pharmacology and Toxicology. Sanlıurfa, Türkiye
• Füsun Temamoğulları Harran University, Faculty of Veterinary Medicine, Department of Pharmacology and Toxicology. Sanlıurfa, Türkiye
• Anıl Karakaş Harran University, Faculty of Veterinary Medicine, Department of Pharmacology and Toxicology. Sanlıurfa, Türkiye

DOI: https://doi.org/10.52973/rcfcv-e34319

Keywords: Wild bird, indicator, metal, ICP–MS

Abstract

Birds are used as bioindicators to determine the negative effects of environmental pollution on human, animal, and environmental health. Among the terrestrial bird species in the study are: the common buzzard (Buteo buteo); black kite (Milvus migrans), common kestrel (Falco tinnunculus); among the aquatic bird species, marsh harrier (Circus aeruginosus), white stork (Ciconia ciconia), gray heron (Ardea cinerea) were used. Heavy metals As, Hg, Zn, Cu, and Se were analysed in blood samples by inductively coupled plasma mass spectrometry (ICP–MS). In the study, Hg and Se concentrations were generally higher and As concentrations were generally lower than those reported in the literature. In black kites, which are vulnerable to environmental contamination and pollution has serious effects on population numbers, it was observed that heavy metals other than As metal were generally higher than the values determined in the studies. Pollutants in nature need to be evaluated by taking into account species–specific differences, age, gender, habitats, migration periods, biomass and feeding habits.

References

Baos R, Blas J, Bortolotti GR, Marchant, TA, Hiraldo F. Adrenocortical response to stress and thyroid hormone status in free–living nestling white storks (Ciconia ciconia) exposed to heavy metal and arsenic contamination. Environ. Health Perspect. [Internet]. 2006; 114(10):1497–1501. doi: https://doi.org/cwqz77

de la Casa–Resino I, Hernández–Moreno D, Castellano A, Soler–Rodríguez F, Pérez–López M. Biomarkers of oxidative status associated with metal pollution in the blood of the white stork (Ciconia ciconia) in Spain. Toxicol. Environ. Chem. [Internet]. 2015; 97(5):588–598. doi: https://doi.org/mg34

Baos R, Jovani R, Pastor N, Tella JL, Begona J, Gomez G, Gonzalez MJ, Hiraldo, F. Evaluation of genotoxic effects of heavy metals and arsenic in wild nestling white storks (Ciconia ciconia) and black kites (Milvus migrans) from southwestern Spain after a mining accident. Environ. Toxicol. Chem. [Internet]. 2006; 25(10):2794–2803. doi: https://doi.org/d48bh2

Carneiro M, Colaço B, Brandão R, Ferreira C, Santos N, Soeiro V, Colaço A, Pires MJ, Oliveira PA, Lavín S. Biomonitoring of heavy metals (Cd, Hg, and Pb) and metalloid (As) with the Portuguese common buzzard (Buteo buteo). Environ. Monit. Assess. [Internet]. 2014; 186(11):7011–7021. doi: https://doi.org/f6kzv3

Manzano J, Méndez–Fernández P, Gil–Jiménez E, Romero D, Ferrer M. Temporal trends of inorganic elements in a common kestrel (Falco tinnunculus) population from southwest Spain. Environ. Pollut. [Internet]. 2021; 274:116447. doi: https://doi.org/mg36

Kitowski I, Kowalski R, Komosa A, Sujak A. Total mercury concentration in the kidneys of birds from Poland. Turk. J. Zool. [Internet]. 2015; 39(4):693–701. doi: https://doi.org/mg37

Blanco G, Frías O, Jiménez B, Gómez G. Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid–waste incinerator. Environ. Toxicol. Chem. [Internet]. 2003; 22(11):2711–2718. doi: https://doi.org/dgr7z7

Fox GA. Wildlife as Sentinels of Human Health Effects in the Great Lakes. St. Lawrence Basin. Environ. Health Perspect. [Internet]. 2001; 109(6):853–861. doi: https://doi.org/d4xpjv

Pérez–López M, Hermoso de M. M, López–Beceiro A, Soler–Rodríguez F. Heavy metal (Cd, Pb, Zn) and metalloid (As) content in raptor species from Galicia (NW Spain). Ecotoxicol. Environ. Saf. [Internet]. 2008; 70(1):154–162. doi: https://doi.org/bksxfr

Pérez–López M, Cid F, Oropesa AL, Fidalgo LE, López–Beceiro A, Soler F. Heavy metal and arsenic content in seabirds affected by the Prestige oil spill on the Galician coast (NW Spain). Sci. Total Environ. [Internet]. 2006; 359(1–3):209–220. doi: https://doi.org/fcwp8h

Ütme Ö, Temamoǧullari F. Analysis of some heavy metals (Cd and Pb) in the Şanlıurfa province using Feral pigeon blood samples. Turkish J. Vet. Anim. Sci. [Internet]. 2021; 45(2):311–317. doi: https://doi.org/mg38

Grúz A, Mackle O, Bartha A, Szabó R, Déri J, Budai P, Lehel J. Biomonitoring of toxic metals in feathers of predatory birds from eastern regions of Hungary. Environ. Sci. Pollut. Res. [Internet]. 2019; 26(25):26324–26331. doi: https://doi.org/mg39

Kitowski I, Jakubas D, Wiącek D, Sujak A, Pitucha G. Trace element concentrations in livers of Common Buzzards Buteo buteo from eastern Poland. Environ. Monit. Assess. [Internet]. 2017; 189(8):421. doi: https://doi.org/mg4b

Ding J, Yang W, Yang Y, Ai S, Bai X, Zhang Y. Variations in tree sparrow (Passer montanus) egg characteristics under environmental metal pollution. Sci. Total Environ. [Internet]. 2019; 687:946–955. do: https://doi.org/mg4c

Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L. A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ. Sci. Pollut. Res. [Internet]. 2016; 23(9):8244–8259. doi: https://doi.org/ghw7vj

Malvandi H, Shamabadi MH. Use of Feathers from Birds that Collided with Vehicles to Monitor Heavy Metal Contamination in Western Khorasan Razavi, Iran. Bull. Environ. Contam. Toxicol. [Internet]. 2022; 109(3):495–501. doi: https://doi.org/mg4d

Kamiński P, Kurhalyuk N, Kasprzak M, Jerzak L, Tkachenko H, Szady–Grad M, Klawe JJ, Koim B. The impact of element–element interactions on antioxidant enzymatic activity in the blood of white stork (Ciconia ciconia) chicks. Arch. Environ. Contam. Toxicol. [Internet]. 2009; 56(2):325–337. doi: https://doi.org/chgb7q

Montañez JC, Arribére MA, Rizzo A, Arcagni M, Campbell L, Ribeiro–Guevara S. Zinc in an ultraoligotrophic lake food web. Environ. Sci. Pollut. Res. [Internet]. 2018; 25(16):15422–15435. doi: https://doi.org/gdwkc5

Xu EG, Lin N, Cheong RS, Ridsdale C, Tahara R, Du TY, Das D, Zhu J, Silva LP, Azimzada A, Larsson HCE, Tufenkji N. Artificial turf infill associated with systematic toxicity in an amniote vertebrate. Proc. Natl. Acad. Sci. U.S.A. [Internet]. 2019; 116(50):25156–25161. doi: https://doi.org/gq2jf3

Kierczak J, Potysz A, Pietranik A, Tyszka R, Modelska M, Néel C, Ettler V, Mihaljevič M. Environmental impact of the historical Cu smelting in the Rudawy Janowickie Mountains (south–western Poland). J. Geochem. Explor. [Internet]. 2013; 124:183–194. doi: https://doi.org/mg4f

Baos R, Jovani R, Forero MG, Tella JL, Gómez G, Jiménez B, González MJ, Hiraldo F. Relationships between T–cell–mediated immune response and Pb, Zn, Cu, Cd, and as concentrations in blood of nestling white storks (Ciconia ciconia) and black kites (Milvus migrans) from Doñana (southwestern Spain) after the Aznalcóllar toxic spill. Environ. Toxicol. Chem. [Internet]. 2006; 25(4):1153–1159. doi: https://doi.org/bv267z

Zhang HH, Wu ZF, Yang CL, Xia B, Xu DR, Yuan HX. Spatial Distributions and Potential Risk Analysis of Total Soil Selenium in Guangdong Province, China. J. Environ. Qual. [Internet]. 2008; 37(3):780–787. doi: https://doi.org/bc87gv

Alvárez CR, Moreno MJ, Alonso LL, Gómara B, Bernardo FJG, Martín–Doimeadios RCR, González MJ. Mercury, methylmercury, and selenium in blood of bird species from Doñana National Park (Southwestern Spain) after a mining accident. Environ. Sci. Pollut. Res. [Internet]. 2013; 20(8):5361–5372. doi: https://doi.org/f5bjd3

Ackerman JT, Herzog MP, Evers DC, Cristol DA, Kenow KP, Heinz, G. H., Lavoie, RA, Brasso, RL, Mallory, ML, Provencher, JF, Braune, BM, Matz A, Schmutz JA, Eagles–Smith CA, Savoy LJ, Meyer MW, Hartman CA. Synthesis of Maternal Transfer of Mercury in Birds: Implications for Altered Toxicity Risk. Environ. Sci. Technol. [Internet]. 2020; 54(5):2878–2891. doi: https://doi.org/ghkcg9

He C, Su T, Liu S, Jiang A, Goodale E, Qiu G.Heavy Metal, Arsenic, and Selenium Concentrations in Bird Feathers from a Region in Southern China Impacted by Intensive Mining of Nonferrous Metals. Environ. Toxicol. Chem. [Internet]. 2020; 39(2):371–380. doi: https://doi.org/mg4g

Benito V, Devesa V, Muñoz O, Suñer MA, Montoro R, Baos R, Hiraldo F, Ferrer M, Fernández MA, González MJ. Trace elements in blood collected from birds feeding in the area around Donana National Park affected by the toxic spill from the Aznalcollar mine. Sci. Total Environ. [Internet]. 1999; 242(1–3):309–323. doi: https://doi.org/dj7w8z

Bjedov D, Mikuška A, Velki M, Lončarić Z, Mikuška T. The first analysis of heavy metals in the Grey Heron Ardea cinerea feathers from the Croatian colonies. Larus–Hrvat. Akad. Znan. i Umjet. [Internet]. 2020; 55(1):7–25. doi: https://doi.org/mg4j

Pérez–López M, De la Casa–Resino I, Hernández–Moreno D, Galeano J, Míguez–Santiyán MP, de Castro–Lorenzo A, Otero–Filgueiras M, Rivas–López O, Soler F. Concentrations of Metals, Metalloids, and Chlorinated Pollutants in Blood and Plasma of White Stork (Ciconia ciconia) Nestlings From Spain. Arch. Environ. Contam. Toxicol. [Internet]. 2016; 71(3):313–321. doi: https://doi.org/f83989

Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA. Mercury Exposure Affects the Reproductive Success of a Free–Living Terrestrial Songbird, the Carolina Wren (Thryothorus ludovicianus). The Auk. 2011; 128(4):759–769. doi: https://doi.org/fh32h6

Beyer WN, Meador JP, editors. Environmental Contaminants in Biota: Interpreting Tissue Concentrations. 2nd. ed. Boca Raton, Florida, USA: CRC Press. 2011. p. 669–696

Carneiro M, Oliveira P, Brandão R, Soeiro V, Pires MJ, Lavin S, Colaço B. Assessment of the exposure to heavy metals and arsenic in captive and free–living black kites (Milvus migrans) nesting in Portugal. Ecotoxicol. Environ. Saf. [Internet]. 2018; 160(6):191–196. doi: https://doi.org/mg5k

Maia AR, Soler–Rodriguez F, Pérez–López M. Concentration of 12 Metals and Metalloids in the Blood of White Stork (Ciconia ciconia): Basal Values and Influence of Age and Gender. Arch. Environ. Contam. Toxicol. [Internet]. 2017; 73(4):522–532. doi: https://doi.org/mg5m

Kamiński P, Kurhalyuk N, Jerzak L, Kasprzak M, Tkachenko H, Klawe JJ, Szady–Grad M, Koim B, Wiśniewska E. Ecophysiological determinations of antioxidant enzymes and lipoperoxidation in the blood of White Stork Ciconia ciconia from Poland. Environ. Res. [Internet]. 2009; 109(1):29–39. doi: https://doi.org/bzc36v

Eagles–Smith CA, Ackerman JT, De La Cruz SEW, Takekawa JY. Mercury bioaccumulation and risk to three waterbird foraging guilds is influenced by foraging ecology and breeding stage. Environ. Pollut. [Internet]. 2009; 157(7):1993–2002. doi: https://doi.org/cd6db8

Borgå K, Campbell L, Gabrielsen GW, Norstrom RJ, Muir DCG, Fisk AT. Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds. Environ. Toxicol. Chem. [Internet]. 2006; 25(11):2927–2936. doi: https://doi.org/dhvhf4

Temamoğullari F, Dinçoğlu AH. Şanlıurfa ve Çevresindeki Kuyu Sularında Çinko ve Selenyum Düzeyleri. Kafkas Univ. Vet. Fak. Derg. [Internet]. 2020; 16(2):199–203. doi: https://doi.org/mg5p

Tokatli C. Drinking water quality assessment of ergene river basin (Turkey) by water quality index: Essential and toxic elements. Sains Malays. [Internet]. 2019; 48(10):2071–2081. doi: https://doi.org/mg5q

Yabanli M, Tay S. Selenium and mercury balance in sea bream obtained from different living environments in Turkey: a risk assessment for the consumer health. Environ. Sci. Pollut. Res. [Internet]. 2021; 28(27):36069–36075. doi: https://doi.org/gmpnk7