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Metal interactions within and between tissues of nestling rooks Corvus frugilegus

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Abstract

We analyzed interactions of concentrations of 11 essential and nonessential elements, including toxic metals within and between internal organs (liver, kidney and lung), muscles and bones of nestling rooks Corvus frugilegus with acute cadmium contamination and elevated level of lead. The number of statistically significant (P ≤ 0.05) metal-metal relationships (positive/negative) within particular tissues was the highest in the kidney (7/6), following in the bone (9/2), liver (6/4), lung (5/2) and muscle (5/2). We found eight significant interactions of lead with other metals, and only two of cadmium (only with lead and cobalt, which probably mirrored a greater ability of lead (than in the case of cadmium) to functional and kinetic interaction with other metals, and/or inhibiting effect of lead or cadmium in co-accumulation. Furthermore, a positive relationship between concentration of cadmium and lead in the kidney could hint at the key importance of this organ in detoxification of both toxic metals. Analyses of relationships of individual metals between examined tissues show only positive results in the case of copper (n = 8), following potassium (n = 3), zinc and iron (in both cases n = 2) and a single ones for calcium and magnesium. We concluded that the lack of significant relationships of individual toxic metals (cadmium or lead) between analyzed tissues could result from high levels of these metals, which destroyed detoxifying capacity of kidney, and ultimately enabled a rapid bioaccumulation of these inorganic contaminations in all tissues of examined nestlings. An explanation of concentration of toxic metals in tissues of animals, especially in the case of their high level, require an identification of the actual level of essential elements associated with physiological status of organism.

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References

  • Alonso M.L., Montana F.P., Miranda M., Castillo C., Hernandez J. & Benedito J.L. 2004. Interactions between toxic (As, Cd, Hg and Pb) and nutritional essential (Ca, Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Zn) elements in the tissues of cattle from NW Spain. BioMetals 17(4): 389–397. DOI: 10.1023/B:BIOM.0000029434.89679.a2

    Article  CAS  Google Scholar 

  • Bilby L.W. & Widdowson E.M. 1971. Chemical composition of growth in nestling blackbirds and thrushes. Br. J. Nutr. 25(1): 127–134. DOI: 10.1079/BJN19710070

    Article  PubMed  CAS  Google Scholar 

  • Blanco G., Jimenez B., Frias O., Millan J. & Davila J.A. 2004. Contamination with nonessential metals from a solid-waste incinerator correlates with nutritional and immunological stress in prefledgling black kites (Milvus migrans). Environ. Res. 94(1): 94–101. DOI: 10.1016/S0013-9351(03)00120-8

    Article  PubMed  CAS  Google Scholar 

  • Blanco-Penedo I., Cruz J.M., López-Alonso M., Miranda M., Castillo C., Hernández J. & Benedito J.L. 2006. Influence of copper status on the accumulation of toxic and essential metals in cattle. Environ. Int. 32(7): 901–906. DOI: 10.1016/j.envint.2006.05.012

    Article  PubMed  CAS  Google Scholar 

  • Burger J. & Gochfeld M. 2000. Metals in albatross feathers from Midway Atoll: influence of species, age, and nests location. Environ. Res. A 82(3): 207–221. DOI: 10.1006/enrs.1999.4015

    Article  CAS  Google Scholar 

  • Chandler C.R. 1995. Practical considerations in the use of simultaneous inference for multiple tests. Anim. Behav. 49(2): 524–527. DOI:10.1006/anbe.1995.0069

    Article  Google Scholar 

  • Cosson R.P., Amiard J.C. & Amiard-Triquet C. 1988a. Trace elements in little egrets and flamingos of Camargue, France. Ecotoxicol. Environ. Safe. 15(1): 107–116. PMID: 3359952

    Article  CAS  Google Scholar 

  • Cosson R.P., Amiard-Triquet C. & Amiard J.C. 1988b. Utilisation des plumes dans la recherche des sources de contamination des oiseaux par les elements traces: Cd, Cu, Hg, Pb, Se et Zn chez les flamants de Camargue, France. Water, Air Soil Pollut. 42(1–2): 103–115. DOI: 10.1007/BF00282394

    CAS  Google Scholar 

  • Dauwe T., Snoeijs T., Bervoets L., Blust R. & Eens M. 2006. Calcium availability influences lead accumulation in a passerine bird. Anim. Biol. 56(3): 289–298. DOI: 10.1163/157075606778441822.

    Article  Google Scholar 

  • Davis C.D., Ney D.M. & Greger J.L. 1990. Manganese, iron and lipid interactions. J. Nutr. 120(5): 507–513. PMID: 2341915

    PubMed  CAS  Google Scholar 

  • Frieden E. 1974. The evolution of metals as essential elements. Adv. Exp. Med. 48(1): 1–32. PMID: 4611156

    Article  CAS  Google Scholar 

  • Goyer R.A. 1997. Toxic and essential metal interactions. Ann. Rev. Nutr. 17(1): 37–50. DOI: 10.1146/annurev.nutr.17.1.37

    Article  CAS  Google Scholar 

  • Hagen J., Hagen E., Ostbye E. & Skar H.J. 1976. Some chemical elements in the body of the Meadow Pipit, Anthus pratensis (L.). Norw. J. Zool. 24: 279–289.

    CAS  Google Scholar 

  • Hawaria A.H. & Mulligan C.N. 2007. Effect of the presence of lead on the biosorption of copper, cadmium and nickel by anaerobic biomass. Proc. Biochem. 42(11): 1546–1552. DOI: 10.1016/j.procbio.2007.08.009

    Article  Google Scholar 

  • Irato P., Santon A., Ossi E. & Albergoni V. 2001. Interactions between metals in rat liver and kidney: Localization of metallothionein. Histochem J. 33(2): 79–86. DOI: 10.1023/A:1017944129801

    Article  PubMed  CAS  Google Scholar 

  • Kalavrouziotis I.K., Koukolakis P.H., Manouris G. & Papadopoulos A.H. 2009. Interactions between cadmium, lead, cobalt, and nickel in broccoli, irrigated with treated municipal wastewater. Eur. Water 25/26: 13–23.

    Google Scholar 

  • Kalisińska E., Salicki W., Kavetska K.M. & Ligocki M. 2007. Trace metal concentrations are higher in cartilage than in bones of scaup and pochard wintering in Poland. Sci. Tot. Environ. 388(1–3): 90–103. DOI: 10.1016/j.scitotenv.2007.07. 050

    Google Scholar 

  • Kalisińska E., Salicki W., Mysłek P., Kavetska K.M. & Jackowski A. 2004. Using the Mallard to biomonitor heavy metal contamination of wetlands in north-western Poland. Sci. Tot. Environ. 320(2–3): 145–161. DOI: 10.1016/j.scitotenv.2003.08.014

    Google Scholar 

  • Kamiński P. 1998. The Impact of Calcium and Heavy Metals Upon the Nest Development of the Tree Sparrow (Passer montanus). Wyd. UMK, Toruń, 140 pp. ISBN: 8323109710, 9788323109716

    Google Scholar 

  • Kamiński P., Choiński A. & Wołosiuk B. 1993. Dynamics of the content of selected elements in the nestling development of the House Martin Delichon urbica in a rural landscape. Acta Ornithol. 28(1): 23–37.

    Google Scholar 

  • Kamiński P. & Matus A. 1998. The impact of urban environments on the growth and histopathological changes of tree sparrow (Passer montanus) nestlings. Pol. J. Environ. Stud. 7(3): 131–150.

    Google Scholar 

  • Kamiński P. & Warot L. 2005a. [Chemical element interactions in Jackdaw Corvus monedula nestlings], pp. 173–184. In: Jerzak L., Kavanagh B.P. & Tryjanowski P. (eds), Ptaki krukowate Polski [Corvids of Poland], Bogucki Wyd. Nauk., Poznań. 679 pp. ISBN: 8389290928

    Google Scholar 

  • Kamiński P. & Warot L. 2005b. [Dynamics of physiological elements in the Jackdaw Corvus monedula during nesting development in an agricultural landscape], pp. 155–172. In: Jerzak L., Kavanagh B.P. & Tryjanowski P. (eds), Ptaki krukowate Polski [Corvids of Poland], Bogucki Wyd. Nauk., Poznań. 679 pp. ISBN: 8389290928

    Google Scholar 

  • Kasprzykowski Z. 2001. Niekorzystne warunki pogodowe przyczyna strat w legach gawrona Corvus frugilegus [Unfavourable weather conditions the cause of the rook Corvus frugilegus brood losses]. Notatki Ornitologiczne 41: 255–256.

    Google Scholar 

  • Kasprzykowski Z. 2002. Biologia rozrodu gawrona Corvus frugilegus w krajobrazie rolniczym wschodniej Polski [Reproductive biology of the rook Corvus frugilegus in the agricultural landscape of eastern Poland]. Notatki Ornitologiczne 43: 219–226.

    Google Scholar 

  • Kasprzykowski Z. 2003. Habitat preferences of foraging Rooks Corvus frugilegus during the breeding period in the agricultural landscape of eastern Poland. Acta Ornithol. 38(1): 27–31.

    Google Scholar 

  • Kasprzykowski Z. 2007. Reproduction of the rook, Corvus frugilegus in relation to the colony size and foraging habitats. Folia Zool. 56(2): 186–193.

    Google Scholar 

  • Kasprzykowski Z. 2008. Nest location within the tree and breeding parameters of Rooks Corvus frugilegus. Bird Study 55(1): 59–65. DOI: 10.1080/00063650809461505

    Article  Google Scholar 

  • Larison J.R. 2002. Effects of cadmium on white-tailed ptarmigan in Colorado. Utah Divison of Oil, Gas and Mining OGM File Services. pp. 188–197. In: 2002 NAAMLP 24th Annual Conference Proceedings Technical paper session 5 — Biology / Vegetation, 578 pp. http://fs.ogm.utah.gov/pub/MINES/AMRRelated/NAAMLP/BioVeg/Larison.pdf (accessed 23.03.2010)

  • Larison J.R., Likens G.E., Fitzpatrick J.W. & Crock J.G. 2000. Cadmium toxicity among wildlife in the Colorado Rocky Mountains. Nature 406(6792): 181–183. DOI: 10.1038/35018068

    Article  PubMed  CAS  Google Scholar 

  • 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(1–3): 35–49. DOI: 10.1007/s10661-007-9727-x

    Article  PubMed  CAS  Google Scholar 

  • Morgan J.E. & Morgan A.J. 1988. Calcium-lead interactions involving earthworms. Part 1: The effect of exogenous calcium on lead accumulation by earthworms under field and laboratory conditions. Environ. Pollut. 54(1): 41–53. DOI: 10.1016/0269-7491(88)90174-1

    Article  PubMed  CAS  Google Scholar 

  • Nagy N.N. & 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. Colloids and Surfaces A: Physicochemical and Engineering Aspects 137(1–3): 231–242. DOI:10.1016/S0927-7757(97)00381-6

    Article  CAS  Google Scholar 

  • Orłowski G., Kamiński P., Kasprzykowski Z., Zawada Z., Koim-Puchowska B., Szady-Grad M. & Klawe J.J. 2012. 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. DOI: 10.1007/s00244-012-9794-z

  • Orłowski G., Kasprzykowski Z., Zawada Z. & Kopij G. 2009. Stomach content and grit ingestion by Rook Corvus frugilegus nestlings. Ornis Fenn 86: 117–122.

    Google Scholar 

  • Petering H.G. 1974. The effect of cadmium and lead on copper and zinc metabolism, pp. 311–325. In: Hoekstra W.G., Suttie J.W., Ganther H.E. & Mertz W. (eds), Trace Element Metabolism in Animals-II, University Park Press, Baltimore. 760 pp.

    Google Scholar 

  • Pinowski J., Pinowska B., Kraśnicki K. & Tomek T. 1983. Chemical composition of growth in nestling Rooks Corvus frugilegus. Ornis Scand. 14: 289–298.

    Article  Google Scholar 

  • Pinowski J., Barkowska M. & Pinowska B. 1995. Interaction of microorganisms, heavy metals and pesticides from liver and their effect on the development and mortality of Passer spp. nestlings, pp. 307–338. In: Pinowski J., Kavanagh B.P. & Pinowska B. (eds), Nestling Mortality of Granivorous Birds due to Microorganisms and Toxic Substances: Synthesis, PWN, Warszawa, 437 pp. ISBN: 8301116749, 9788301116743

  • Prasada Rao P.V.V., Jordan S.A. & Bhatnagar M.K. 1989. Combined nephrotoxicity of methylmercury, lead, and cadmium in pekin ducks: Metallothionein, metal interactions, and histopathology. J. Toxicol. Environ. Health 26(3): 327–348. DOI: 10.1080/15287398909531257

    Article  PubMed  CAS  Google Scholar 

  • Rucker R.B., O’Dell B.L., Parker H.E. & Rogler J.C. 1970. The role of copper in crosslinking of collagen and elastin. Trace Subs. Envir. Health 4: 255–259.

    Google Scholar 

  • Scheuhammer A.M. 1996. Influence of reduced dietary calcium on the accumulation and effects of lead, cadmium, and aluminum in birds. Environ. Poll. 94(3): 337–343. DOI: 10.1016/S0269-7491(96)00084-X

    Article  CAS  Google Scholar 

  • StatSoft, 2006. Statistica© (Data Analysis Software System), Version 7.1., Tulsa, USA.

  • Terelak H., Stuczyński T., Motowicka-Terelak T., Maliszewska-Kordybach B & Pietruch C. 2008. Monitoring Chemizmu Gleb Ornych Polskiwlatach 2005–2007. Instytut Uprawy Nawożenia i Gleboznawstwa. National Research Institute in Puławy. Puławy, Poland, 205 pp. ISBN: 978-83-7217-319-5

    Google Scholar 

  • Wayland M., Neugebauer E. & Bollinger T. 1999. Concentrations of lead in liver, kidney, and bone of bald and golden eagles. Arch. Environ. Contam. Toxicol. 37(2): 267–272. DOI: 10.1007/s002449900514

    Article  PubMed  CAS  Google Scholar 

  • Weltz B. 1985. Atomic Absorption Spectrometry, Second Completely Revised Edition VCH Veincheim, Berlin, Germany, 965 pp. ISBN: 3527285717, 9783527285716

    Google Scholar 

  • Wenzel C., Adelung D. & Theede H. 1996. Distribution and agerelated changes of trace elements in kittiwake Rissa tridactyla nestlings from a isolated colony in the German Bight, North Sea. Sci. Tot. Environ. 193(1): 13–26. DOI: 10.1016/S0048-9697(96)05320-X

    Article  CAS  Google Scholar 

  • Woshner V.M., O’Hara T.M., Bratton G.R., Suydam R.S. & Beasley V.R. 2001. Concentrations and interactions of selected essential and non-essential elements in bowhead and beluga whales of arctic Alaska. J. Wild. Dis. 37(4): 693–710. PMID: 11763733

    CAS  Google Scholar 

  • Woshner V.M., O’Hara T.M., Bratton G.R. & Beasley V.R. 2001. Concentrations and interactions of selected essential and nonessential elements in ringed seals and polar bears of arctic Alaska. J. Wildl. Dis. 37(4): 711–721. PMID: 11763734

    PubMed  CAS  Google Scholar 

  • Young C.Y., Sang K.L., Ja Y.Y., Ki W.K., Lee S.-Y., Seung M.O. & Chung K.H. 2002. Interrelationship between the concentration of toxic and essential elements in Korean tissues. J. Health Sci. 48(2): 195–200.

    Article  Google Scholar 

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Orłowski, G., Kamiński, P., Kasprzykowski, Z. et al. Metal interactions within and between tissues of nestling rooks Corvus frugilegus . Biologia 67, 1211–1219 (2012). https://doi.org/10.2478/s11756-012-0108-8

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