Abstract
Concentration of minerals (sodium, potassium, calcium [Ca], magnesium, iron [Fe], copper, zinc [Zn], manganese [Mn], and cobalt) as well as toxic metals (cadmium [Cd], lead [Pb]) were determined in five tissues (liver, lung, kidney, muscle, and bone) of nestling rooks (Corvus frugilegus; 1 to 13 days old) found dead in seven breeding colonies in eastern Poland. Cd concentration in all analyzed tissues was in the narrow range of 17.0–17.2 mg/kg dry weight (dw) Cd, which in the light of the literature data indicates acute contamination by this toxic metal. Similarly, we found increased levels of Pb, which in all tissues ranged between 5.0 and 6.2 mg/kg dw. Results of multivariate general linear model (GLM) testing of the effect of three variables (tissue type, colony, and nestling age) on tissue concentrations of various metals showed significance for Fe, Cu, Zn, and Mn. Only concentrations of Ca, Fe, and Zn differed significantly between the analyzed tissues. GLM analysis did not show any statistically significant differences in tissue levels of minerals and both toxic metals among examined rookeries, which indicates the widespread presence of nonpoint Cd and Pb pollution linked to agricultural activity and similar levels of these inorganic contaminants on crop fields (feeding grounds) around breeding colonies. We concluded that high levels of both toxic metals, Cd and Pb, probably resulting from the diet of nestling rooks, are based mainly on a diet of ground-dwelling beetles gathered on crop fields.
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Agusa T, Matsumoto T, Ikemoto T, Anan Y, Kubota R, Yasunaga G et al (2005) Body distribution of trace elements in black-tailed gulls from Rishiri Island, Japan: Age-dependent accumulation and transfer to feathers and eggs. Environ Toxicol Chem 24:2107–2120
AP Berglund M, Akesson A, Bjellerup P, Vahter M (2000) Metal-bone interactions. Toxicol Lett 112–113:219–225
Beyerbach M, Büthe A, Heidmann WA, Dettmer R, Knüwer H (1987) Chlorierte Kohlenwasserstoffe in Eiern und Lebern von Saatkrähen (Corvus frugilegus) aus niedersächsichen Brutkolonien. J Ornithol 128:277–290
Blanco G, Frias O, Jimenez B, Gomez G (2003) Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid-waste incinerator. Environ Toxicol Chem 22:2711–2718
Blazka ME, Shaikh ZA (1992) Cadmium and mercury accumulation in rat hepatocytes: interactions with other metal ions. Toxicol Appl Pharmacol 113:112–118
Carpene E, Andreani G, Monari M, Castellani G, Isani G (2006) Distribution of Cd, Zn, Cu and Fe among selected tissues of the earthworm (Allobophora caliginosa) and Eurasian woodcock (Scolopax rusticola). Sci Total Environ 363:126–135
Cramp S (ed) (1998) The complete birds of the Western Palaearctic [on CD-ROM]. Oxford University Press, Oxford
Custer CM, Custer TW, Anteau MJ, Afton AD, Wooten DE (2003) Trace elements in lesser scaup (Aythya affinis) from the Mississippi flyway. Ecotoxicology 12:47–54
Dach J, Starmans D (2005) Heavy metals balance in Polish and Dutch agronomy: actual state and previsions for the future. Agric Ecosyst Environ 107:309–316
Dauwe T, Janssens E, Bervoets L, Blust R, Eens M (2004) Relationships between metal concentrations in great tit nestling and their environment and food. Environ Pollut 131:373–380
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
de Vries W, Römkens PF, van Leeuwen T, van Bronswijk JJ (2002) Heavy metals. In: Hagyart PM, Jarvis SC (eds) Agriculture, hydrology and water quality. CAB International Publishing, Oxfordshire, pp 107–132
Degernes LA (2008) Waterfowl toxicology: a review. Vet Clin North Am Exot Anim Pract 11:283–300
Di Giulio RT, Scanlon PF (1985) Environ Res 37:433–444
Esselink H, van der Geld F, Jager L, Posthuma-Trumpie G, Zoun P, Baars J (1995) Biomonitoring heavy metals using the Barn owl (Tyto alba guttata): Sources of variation especially relating to body condition. Arch Environ Contam Toxicol 28:471–486
Frieden E (1974) The evolution of metals as essential elements. Adv Exp Med 48:1–32
Fullmer CS, Edelstein S, Wasserman RH (1985) Lead-binding properties of intestinal calcium-binding proteins. J Biol Chem 260:6816–6819
Garcia-Fernandez AJ, Sanchez-Garcia JA, Gomez-Zapata M, Luna A (1996) Distribution of cadmium in blood and tissues of wild birds. Arch Environ Contam Toxicol 30:252–258
Goyer RA (1997) Toxic and essential metal interactions. Ann Rev Nutr 17:37–50
Graveland J, Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation an skeletal growth in passerines. Ardea 82:299–314
Hiller BJ, Barclay JS (2011) Concentrations of heavy metals in American Woodcock harvested in Connecticut. Arch Environ Contam Toxicol 60:156–164
Hogstad O (1996) Accumulation of cadmium, copper and zinc in the liver of some passerines species wintering in Central Norway. Sci Total Environ 183:187–194
Honda K, Min BY, Tatsukava R (1986) Distribution of heavy metals and their age-related changes in the eastern great white egret, Egretta alba modesta, in Korea. Arch Environ Contam Toxicol 15:185–197
Jager LP, Rijnierse F, Esselin H, Baars A (1996) Biomonitoring with the Buzzard Buteo buteo in The Netherlands: heavy metals and sources of variation. J Ornithol 137:295–318
Jerzak L, Kavanagh BP, Tryjanowski P (eds) (2005) Corvids of Poland. Bogucki Wyd Nauk, Poznań
Kalavrouziotis IK, Koukolakis PH, Manouris G, Papadopoulos AH (2009) Interactions between cadmium, lead, cobalt, and nickel in broccoli, irrigated with treated municipal wastewater. Eur Water 25(26):13–23
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
Kamiński P (1998) The impact of calcium and heavy metals upon the nest development of the tree sparrow (Passer montanus). Wyd UMK, Toruń, Poland, 140 pp
Kamiński P, Warot L (2005a) Dynamics of physiological elements in the Jackdaw Corvus monedula during nesting development in an agricultural landscape. In: Jerzak L, Kavanagh BP, Tryjanowski P (eds) Corvids of Poland (in Polish with English abstract) Bogucki Wyd Nauk. Poznań, Poland, pp 155–172
Kamiński P, Warot L (2005b) Chemical element interactions in Jackdaw Corvus monedula nestlings. In: Jerzak L, Kavanagh BP, Tryjanowski P (eds) Corvids of Poland [in Polish with English abstract]. Bogucki Wyd Nauk, Poznań, pp 173–184
Kamiński P, Warot L (2005c) Microelements and toxic heavy metals in nestlings Jackdaw Corvus monedula in agricultural landscape. In: Jerzak L, Kavanagh BP, Tryjanowski P (eds) Corvids of Poland [in Polish with English abstract]. Bogucki Wyd Nauk, Poznań, pp 185–205
Kamiński P, Kurhalyuk N, Kasprzak M, Jerzak L, Tkachenko H, Szady-Grad M et al (2009) The impact of element–element interactions on antioxidant enzymatic activity in the blood of white stork (Ciconia ciconia) chicks. Arch Environ Contam Toxicol 56:325–337
Kasprzykowski Z (2001) Unfavourable weather conditions the cause of the Rook Corvus frugilegus brood losses [in Polish]. Not Orn 41:255–256
Kasprzykowski Z (2002) Reproductive biology of the Rook Corvus frugilegus in the agricultural landscape of eastern Poland [in Polish]. Not Orn 43:219–226
Kasprzykowski Z (2003) Habitat preferences of foraging Rooks Corvus frugilegus during the breeding period in the agricultural landscape of eastern Poland. Acta Ornithol 38:27–31
Kasprzykowski Z (2007) Reproduction of the rook, Corvus frugilegus in relation to the colony size and foraging habitats. Folia Zool 56:186–193
Kasprzykowski Z (2008) Nest location within the tree and breeding parameters of Rooks Corvus frugilegus. Bird Study 54:59–65
Kim L, Koo T (2008) Heavy metal distribution in chicks of two heron species from Korea. Arch Environ Contam Toxicol 54:740–747
Kobayashi J (1973) Effect of cadmium on calcium metabolism of rats. Trace Subst Environ Health 7:295–304
Larison JR (2002) Effects of cadmium on white-tailed ptarmigan in Colorado. In: 2002 NAAMLP 24th Annual conference proceedings technical paper session 5-Biology/Vegetation. Utah Division of Oil, Gas and Mining OGM File Services, pp. 188–197. https://fs.ogm.utah.gov/pub/MINES/AMR_Related/NAAMLP/BioVeg/Larison.pdf. Accessed 23 Mar 2010
Levengood JM, Skowron LM (2007) Coaccumulation of cadmium and zinc in tissues of sentinel mallards (Anas platyrhynchos) using a former dredge-disposal impoundment. Arch Environ Contam Toxicol 53:281–286
Linden A, Olsson I, Oskarsson A (1999) Cadmium levels in feed components and kidneys of growing/finishing pigs. J AOAC Int 82:1288–1297
Linden A, Andersson K, Oskarsson A (2001) Cadmium in organic conventional pig production. Arch Environ Contam Toxicol 40:425–431
Louis VL, Breebaart L (1991) Calcium supplements in the diet of nestling tree swallows near sensitive lakes. Condor 93:286–294
Malmberg T (1973) Pesticides and the rook Corvus frugilegus in Scania, Sweden between 1955 and 1970. Oikos 24:377–387
Migula P, Augustyniak M, Szymczyk A, Kowalczyk K (2000) Heavy metals, resting metabolism rates and breeding parameters in two populations of Black-headed Gull Larus ridibundus from industrially polluted areas (Upper Silesia, Poland). Acta Ornithol 35:159–172
Mochizuki M, Mori M, Hondo R, Ueda F (2008) A new index for evaluation of cadmium pollution in birds and mammals. Environ Monit Assess 137:35–49
Mora M (2003) Heavy metals and metalloids in egg contents and eggshells of passerine birds from Arizona. Environ Pollut 125:393–400
Nagy NN, Konya J (1998) Ion-exchange process of lead and cobalt ions on the surface of calcium-montmorillonite in the presence of complex-forming agents. I. The effect of EDTA on the sorption of lead and cobalt ions on calcium-montmorillonite. Collo Surf A Phys Eng Asp 137:231–242
Orłowski G, Kasprzykowski Z, Zawada Z, Kopij G (2009) Stomach content and grit ingestion by Rook Corvus frugilegus nestlings. Ornis Fenn 86:117–122
Orłowski G, Kasprzykowski Z, Dobicki W, Pokorny P, Polechoński 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
Osborn D (1979) Seasonal changes in the fat, protein and metal content of the liver of the Starling Sturnus vulgaris. Environ Pollut 19:145–155
Peryea FL (1998) Historical use of lead arsenate insecticides, resulting soil contamination and implications for soil remediation [on CD-ROM]. In: Proceedings of the 16th world congress of soil science, Montpellier, France, August 20–26. http://soilstfrecwsuedu/leadhistoryhtm. Accessed 20 Feb 2010
Pinowska B, Kraśnicki K, Pinowski J (1981) Estimation of the degree of contamination of granivorous birds with heavy metals in agricultural and industrial landscape. Ekol Pol 29:137–149
Pinowski J, Pinowska B, Kraśnicki K, Tomek T (1983) Chemical composition of growth in nestling Rooks Corvus frugilegus. Ornis Scand 14:289–298
Prestt I, Jefferies DJ, More NW (1970) Polychlorinated biphenyls in wild birds in Britain and their avian toxicity. Environ Pollut 1:3–26
Purchart L, Kula E (2007) Content of heavy metals in bodies of field ground beetles (Coleoptera, Carabidae) with respect to selected ecological factors. Pol J Ecol 55:305–314
Ratcliffe DA (1965) Organo-chlorine residues in some raptor and corvid eggs from northern Britain. British Birds 58:65–81
Reddy C, Coburn J, Hartenbower D, Friedler RM, Brickman AS, Massry SG, Jowsey J (1973) Studies on mechanisms of hypocalcemia of magnesium-depletion. J Clin Invest 52:3000–3010
Roodbergen M, Klok C, van der Hout A (2008) Transfer of heavy metals in the food chain earthworm black-tailed godwit (Limosa limosa): comparison of a polluted and a reference site in The Netherlands. Sci Total Environ 406:407–412
Rosen JF (1983) The metabolism of lead in isolated bone cell populations: interactions between lead and calcium. Toxicol Appl Pharmacol 71:101–112
Rytkonen S, Koivula K, Lindgren W (1993) The population size and breeding biology of the Rook Corvus frugilegus in northern Finland. Ornis Fenn 70:202–212
Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295
Scheuhammer AM (1996) Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ Pollut 94:337–343
Schubert J (1973) Heavy metals—toxicity and environmental pollution. Adv Exp Med Biol 47:239–297
Smith JE, Bortolotti GR, Baos R, Blas J, Hiraldo F, Xie Q (2005) Skeletal pathology in white storks (Ciconia ciconia) associated with heavy metal contamination in southwestern Spain. Toxicol Pathol 33:441–448
Spahn SA, Sherry TW (1999) Cadmium and lead exposure associated with reduced growth rates, poorer fledging success of little blue heron chicks (Egretta caerulea) in South Louisiana Wetlands. Arch Environ Contam Toxicol 37:377–384
StatSoft (2006) Statistica (data analysis software system), version 71. StatSoft, Tulsa, OK
Stenström T, Vahter M (1974) Cadmium and lead in Swedish commercial fertilizers. Ambio 3:91–92
Stone D, Jepson P, Laskowski R (2002) Trends in detoxification enzymes and heavy metal accumulation in ground beetles (Coleoptera: Carabidae) inhabiting a gradient of pollution. Comp Biochem Physiol C Toxicicol Pharmacol 132:105–112
Taylor A, Brady J (1964) Chlorinated pesticide residues in wild bird eggs. Bird Study 11:192–197
Terelak H, Stuczyński T, Motowicka-Terelak T, Maliszewska-Kordybach B, Pietruch C (2008) Monitoring chemizmu gleb ornych polski w latach 2005-2007. Instytut Uprawy Nawożenia i Gleboznawstwa. National Research Institute in Puławy, Puławy
Thompson HM, Fernandes A, Rose M, White S, Blackburn A (2006) Possible chemical causes of skeletal deformities in the grey heron nestlings (Ardea cinerea) in North Nottinghamshire, UK. Chemosphere 65:400–409
Weltz B (1985) Atomic absorption spectrometry. VCH Veincheim, Berlin
Wenzel C, Adelung D, Theede H (1996) Distribution and age-related changes of trace elements in kittiwake Rissa tridactyla nestlings from a isolated colony in the German Bight, North Sea. Sci Total Environ 103:13–26
Wiemeyer SN, Withers D (2004) Metals and trace elements in livers of American white pelicans at Anaho Island, Nevada 2004 US Fish Wildl Service, p 14. http://wwwfwsgov/Nevada/ES/documents/contam/wiemeyer_and_withers_2004_metals_and_trace_elements_in_livers_of_american_white_pelicans_anaho_island_nevada_2004pdf. Accessed 20 Feb 2010
Williams CH, David DJ (1973) The effect of superphosphate on the cadmium content of soils and plants. Aust J Soil Res 11:43–56
Włostowski T, Dmowski K, Bonda-Ostaszewska E (2010) Cadmium accumulation, metallothionein and glutathione levels, and histopathological changes in the kidneys and liver of magpie (Pica pica) from a zinc smelter area. Ecotoxicology 19:1066–1073
Zaccaroni A, Andreani G, Ferrante M, Carpene E, Isani G, Lucisano A (2008) Metal concentrations in the liver and kidney of raptor species from the Calabria region, Italy. Acta Vet (Beogr) 58:315–324
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The authors are grateful to anonymous reviewers for constructive remarks and comments, which greatly improved the value of this manuscript. Responsibility for any errors, including chemical analyses, resides solely with the authors.
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Orłowski, G., Kamiński, P., Kasprzykowski, Z. et al. Essential and Nonessential Elements in Nestling Rooks Corvus frugilegus from Eastern Poland with a Special Emphasis on Their High Cadmium Contamination. Arch Environ Contam Toxicol 63, 601–611 (2012). https://doi.org/10.1007/s00244-012-9794-z
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DOI: https://doi.org/10.1007/s00244-012-9794-z