Skip to main content
SpringerLink
Log in

The Impact of Element–Element Interactions on Antioxidant Enzymatic Activity in the Blood of White Stork (Ciconia ciconia) Chicks

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The aim of this work was to determine interrelationships among macroelements Na, K, Ca, Mg, and Fe, microelements Zn, Cu, Mn, and Co, and toxic heavy metals Pb and Cd in the blood of white stork Ciconia ciconia, during postnatal development, in different Polish environments, and their impact on the activity of antioxidant enzymes. We considered the content of thiobarbituric acid-reactive substances (TBARSs), i.e., malondialdehyde (MDA), and activity of superoxide dismutase (SOD), catalase (CAT), ceruloplasmine (CP), glutathione peroxidase (GPx), and glutathione reductase (GR). Blood samples were collected from storks developing at Odra meadows (Kłopot; southwestern Poland). They were compared with blood of chicks from several suburban sites located 20 km away from Zielona Góra (0.1 million inhabitants; southwestern Poland) and near Głogów, where a copper smelter is situated. We also conducted research in the Pomeranian region (Cecenowo; northern Poland). We collected blood samples via venipuncture of the brachial vein of chicks in 2005–2007. They were retrieved from the nest and placed in individual ventilated cotton sacks. The blood was collected using a 5-ml syringe washed with ethylenediaminetetraacetic acid (EDTA). We found significant interactions between macro- and microelements and enzymatic activity and TBARS products. We noticed the predominance of Cd and Pb participation in element–enzyme interactions. Simultaneously, we found interrelationships between cadmium and Na, K, Ca, Mg, and Fe and the activity of antioxidant enzymes SOD, CAT, CP, GR, and TBARS products in the blood of white stork chicks. In the case of lead these relationships were not numerous and they were significant for Ca, Mg, Cu, Mn, and Co. Correlations with enzymes were significant for Pb-CAT and Pb-TBARS. We noted that activities of most enzymes (SOD, CAT, CP, GR) and TBARS products are determined by their interactions with physiological elements Na, Ca, Mg, Fe, and Zn and toxic heavy metals. White stork chicks ranged in age from 17 to 59 days. Concentrations of elements in the blood were age related. Among enzymes, only SOD, CAT, and GPx were age related. Young storks differed in the case of element concentration (except for Ca, Zn, and Cd) and enzymatic activity. We found that significant element–element interaction/enzyme activity predominated in the case of physiological elements and toxic metals, which we explain by the intensive and prevailing access of toxic metals in redox reactions. This causes changes in the priority of these metals, reflected by their influence on the enzymatic activity of antioxidant enzymes. The content of Cd and Pb in blood of young storks from different regions tends to affect the lipid peroxidation process negatively. However, in many cases we observed an increase in enzymatic activity with an increase in heavy metals. This indicates the changes in oxidative stress intensity in chicks in response to environmental differentiation. The increase in lipoperoxidation modifies antioxidant enzyme activity and causes changes in SOD, CAT, CP, GPx, and GR activity in chicks from various regions, principally increases in enzyme activity in chicks from polluted environments and suburbs. We suggest that the source of heavy metals in chicks’ blood might be used as a biological test system of adaptation to oxidative stress. We also report that a high level of heavy metals is accompanied by increased lipid peroxidation. Thus young storks are probably significantly susceptible to environmental conditions. They demonstrated initiation of lipoperoxidation and oxidative modification of proteins that coincide with chemical elements, as a possible antioxidant defense system.

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
Fig. 5

Similar content being viewed by others

References

  • Aschoff J (1981) Frerunning and entrained circadian rhythms. In: Aschoff J (ed) Handbook of behavioural neurobiology, vol 4. Plenum, New York, London, pp 81–93

    Google Scholar 

  • Benito V, Devesa V, Munoz O, Suner MA, Montoro R, Baos R, Hiraldo F, Ferrer M, Fernandez M, Gonzalez MJ (1999) 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 242:309–323 (doi: 10.1016/s0048-9697(99)00398-8)

    Article  CAS  Google Scholar 

  • Chłopecka A, Bacon JR, Wilson MJ, Kay J (1996) Forms of cadmium, lead, and zinc in contaminated soils from southwest. Poland J Environ Qual 25:69–79

    Google Scholar 

  • Congiu L, Chicca M, Pilastro A, Turchetto M, Tallandini L (2000) Effects of chronic dietary cadmium on hepatic glutathione levels and glutathione peroxidase activity in starlings (Sturnus vulgaris). Arch Environ Contam Toxicol 38:357–361 (doi: 10.1007/s002449910047)

    Article  CAS  Google Scholar 

  • Daniluk J, Daniluk-Korbal A, Mitrus C (2006) Changes in population size, breeding success and nest location of a local white stork Ciconia ciconia population in eastern Poland. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 15–21

    Google Scholar 

  • Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress. Part I. Mechanisms involved in metal induced oxidative damage. Curr Top Med Chem 1:529–539 (doi: 102174/1568026013394831)

    Article  CAS  Google Scholar 

  • Ermak G, Davies KJ (2002) Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38(10):713–721 (doi: 101016/S0161-5890(01)00108-0)

    Article  CAS  Google Scholar 

  • Fergusson JE (1990) The heavy elements: chemistry, environmental impact and health effects. Pergamon Press, New York

    Google Scholar 

  • Giesy JP Jr (1980) Cadmium interactions with naturally occuring organic ligands. In: Nriagu JO (ed) Cadmium in the environment. Wiley, New York, pp 237–256

    Google Scholar 

  • Glatzle D, Vuilleumier JP, Weber F, Decker K (1974) Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in human. Experientia 30:665–667 (doi: 101007/BF01921531)

    Article  CAS  Google Scholar 

  • Hall CM, Higueras PL, Kesler SE, Lunar R, Dong H, Halliday AN (1997) Dating of alteration episodes related to mercury mineralization in the Almadén district, Spain. Earth Planet Sci Lett 148(1–2):287–298

    Article  CAS  Google Scholar 

  • Hardeland R, Balzer I, Poeggeler B (1995) On the primary function of melatonin in evolution: mediation of photoperiodic signals in a unicell, photooxidation, and scavenging of free radicals. J Pineal Res 18:104–111

    Article  CAS  Google Scholar 

  • Hoffman DJ (2002) Role of selenium toxicity and oxidative stress in aquatic birds. Aquat Toxicol 57:11–26

    Article  CAS  Google Scholar 

  • Hoffman DJ, Franson JC, Pattee OH, Bunck CM, Murray HC (1985) Biochemical and hematological effects of lead ingestion in nestling American kestrels (Falco sparverius). Comp Biochem Physiol 80C:431–439

    CAS  Google Scholar 

  • Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier Applied Sciences, New York

    Google Scholar 

  • Jakubiec Z (ed) (1985) Population of white stork Ciconia ciconia L. in Poland. PWN, Warszawa-Kraków

  • Kabata-Pendias A, Pendias H (1984) Trace elements in soils and plants. CRC Press, Boca Raton, FL

    Google Scholar 

  • Kaługa I (2006) Protection of the white stork Ciconia ciconia in the Mazovian lowland. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 449–458

    Google Scholar 

  • Kamiński P, Warot L (2005) Chemical element interactions in jackdaw Corvus monedula nestlings. In: Jerzak L, Kavanagh BP, Tryjanowski P (eds) Corvids of Poland. Bogucki Wyd Nauk, Poznań, pp173–184

    Google Scholar 

  • Kamiński P, Kurhalyuk N, Szady-Grad M, Tkachenko H, Kasprzak M, Jerzak L (2007) Chemical elements in the blood of white stork Ciconia ciconia chicks in differential Poland regions. Med Biol Sci (in prep.)

  • Korolyuk MA, Ivanova LI, Majorova IT (1988) Methods of definition of catalase activity. Lab Manuals 1:16–19

    Google Scholar 

  • Kostyuk VA, Potapovich AI, Kovaleva JI (1990) Simple and sensitive method of definition of superoxidedismutase, based on reaction of oxidation of kvercetine. Questions Med Chem 2:88–91

    Google Scholar 

  • Kurhalyuk N, Kamiński P, Kasprzak M, Jerzak L (2006) Antioxidant enzymes activity and lipid peroxidation processes in the blood of white stork (Ciconia ciconia) chicks from W Poland. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 482–498

    Google Scholar 

  • Lack D (1973) Population studies of birds. Oxford Press, Clarendon, UK

    Google Scholar 

  • Lanzarot MP, Barahona MV, Andres MIS, Fernandez-Garcia M, Rodriguez C (2005) Hematologic, protein electrophoresis, biochemistry, and cholinesterase values of free-living black stork nestlings (Ciconia nigra). J Wildl Dis 41(2):379–386

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Merian E (ed) (1991) Metals and their compounds in the environment. VCH, New York

    Google Scholar 

  • Moin VM (1986) Simple and specific method of measurement of glutathione peroxidase activity in the erythrocytes. Lab Manuals 12:724–727

    Google Scholar 

  • Möller G (1995) Biogeochemical interactions affecting hepatic trace element levels in aquatic birds. Pharmacol Exp Ther 272:264–274

    Google Scholar 

  • Nielsen FH (1988) Nutritional significance of the ultratrace elements. Nutr Rev 46:337–341

    Article  CAS  Google Scholar 

  • Patrick L (2003) Toxic metals and antioxidants. Part II. The role of antioxidants in arsenic and cadmium toxicity. Altern Med Rev 8(2):106–128

    Google Scholar 

  • Peterson U, Jakubiec Z (2006) Long-term studies of population dynamics and reproduction of the white stork Ciconia ciconia in the region of its highest density. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 35–46

    Google Scholar 

  • Profus P (2006) Population changes and breeding ecology of the white stork Ciconia ciconia L. in Poland against a background of the European population. Synth Studia Nat 50, 155 pp

  • Quig D (1998) Cysteine metabolism and metal toxicity. Altern Med Rev 3(4):262–270

    CAS  Google Scholar 

  • Ravin HA (1961) An improved colorimetric enzymatic assay of ceruloplasmin. J Lab Clin Med 58:161–168

    CAS  Google Scholar 

  • Reiter RJ, Melchiorri D, Sewerynek E (1995) A review of the evidence supporting melatonin’s role as an antioxidant. J Pineal Res 18:1–11 (doi: 101111/j1600-079X1995tb00133x)

    Article  CAS  Google Scholar 

  • Rubacha S, Jerzak L (2006) Changes in the white stork Ciconia ciconia population number, density and breeding places in Zielona Góra region 1926–2004. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 47–54

    Google Scholar 

  • Sewerynek E, Melchiorri D, Ortiz GG (1995) Melatonin reduces H2O2-induced lipid peroxidation in homogenates of different rat brain regions. J Pineal Res 19:51–56 (doi: 101111/j1600-079X1995tb00170x)

    Article  CAS  Google Scholar 

  • Shmueli M, Izhaki I, Zinder O, Arad Z (2000) The physiological state of captive and migrating great white pelicans (Pelecanus onocrotalus) revealed by their blood chemistry. Comp Biochem Physiol A 125:25–32 (doi: 101016/s1095-6433(99)00162-2)

    Article  CAS  Google Scholar 

  • Simkiss K (1975) Calcium and avian reproduction. Symp Zool Soc Lond 35. In: Peaker M (ed) Avian physiology. Academic Press, London, pp 307–337

    Google Scholar 

  • Smith K (1988) Calcium and trace mineral interactions. Cereal Foods World 33:775–782

    Google Scholar 

  • Stajn A, Zhikić RV, Ognjanović B, Saićić ZS, Pavlović SZ, Kostić MM, Petrović VM (1997) Effect of cadmium and selenium on the antioxidant defense system in rat kidneys. Comp Biochem Physiol 117C(2):167–172

    CAS  Google Scholar 

  • Szulc-Guziak D (2006) Natural history education based on white stork Ciconia ciconia observation and protection. In: Tryjanowski P, Sparks TH, Jerzak L (eds) The white stork in Poland: studies in biology, ecology and conservation. Bogucki Wyd Nauk, Poznań, pp 459–476

    Google Scholar 

  • Tan DX, Manchester LC, Reiter RJ (2000) Melatonin directly scavengers hydrogen peroxide: a potentially new metabolic pathway of melatonin biotransformation. Free Radical Biol Med 29:1177–1185 (doi: 101016/s0891-5849(00)00435-4)

    Article  CAS  Google Scholar 

  • Timirbulatov RA, Selezniev EI (1981) Method for increasing intensity of free radical oxydation of blood lipid containing components and its diagnosis value. Lab Manuals 4:209–211

    Google Scholar 

  • Tomiałojć L, Stawarczyk T (2003) The avifauna of Poland: distribution, numbers and trends. PTPP, Wrocńaw

    Google Scholar 

  • Tryjanowski P, Jerzak L, Radkiewicz J (2005) Effect of water level and livestock on the productivity and numbers of breeding white storks waterbirds. 28(3):378–382 (doi: 101675/1524-4695(2005)028[0378:EOWLAL]20CO;2)

  • Uchida M, Teranishi H, Aoshima K, Katoh T, Kasuya M, Inadera H (2004) Reduction of erythrocyte catalase and superoxide dismutase activities in male inhabitants of a cadmium-polluted area in Jinzu river basin. Jpn Toxicol Lett 151:451–457 (doi: 101016/jtoxlet200403009)

    Article  CAS  Google Scholar 

  • Underwood EJ (1966) The mineral nutrition of livestock. Academic Press, New York

    Google Scholar 

  • Underwood EJ (1977) Trace elements in human and animal nutrition, 4th edn. Academic Press, New York

    Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208 (doi: 102174/0929867053764635)

    Article  CAS  Google Scholar 

  • Volesky B (1990) Biosorption of heavy metals. CRC Press, Boca Raton, FL

    Google Scholar 

  • Weltz B (1985) Atomic absorption spectrometry. VCH Veincheim, Berlin

    Google Scholar 

  • Zar JH (1998) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Zhikic RV, Stajn AS, Pavlović SZ, Ognjanović BI, Saićić ZS (2001) Activities of superoxide dismutase and catalase in erythrocytes and plasma transaminases of goldfish (Carassius auratus gibelio Bloch) exposed to cadmium. Physiol Res 50:105–111

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ecology and Environmental Protection, Nicolaus Copernicus University, Collegium Medicum in Bydgoszcz, Skłodowska-Curie St. 9, PL 85-094, Bydgoszcz, Poland

    Piotr Kamiński & Beata Koim

  2. Department of Animal Physiology, Pomeranian Academy, Institute of Biology and Environmental Protection, Arciszewski St. 22 B, PL 76-200, Slupsk, Poland

    Nataliya Kurhalyuk & Mariusz Kasprzak

  3. Faculty of Biological Sciences, University of Zielona Góra, Institute of Biotechnology and Environment Protection, Prof. Szafran St. 1, PL 65-516, Zielona Góra, Poland

    Leszek Jerzak

  4. Department of Hygiene and Toxicology, Danylo Halytskiy Lviv National Medical University, Pekarska St. 69, 79010, Lviv, Ukraine

    Halyna Tkachenko

  5. Department of Hygiene and Epidemiology, Nicolaus Copernicus University, Collegium Medicum in Bydgoszcz, Skłodowska-Curie St. 9, PL 85-094, Bydgoszcz, Poland

    Małgorzata Szady-Grad & Jacek J. Klawe

Authors
  1. Piotr Kamiński
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nataliya Kurhalyuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariusz Kasprzak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leszek Jerzak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Halyna Tkachenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Małgorzata Szady-Grad
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jacek J. Klawe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Beata Koim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Piotr Kamiński.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kamiński, P., Kurhalyuk, N., Kasprzak, M. et al. 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 (2009). https://doi.org/10.1007/s00244-008-9178-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-008-9178-6

Keywords

Search

Navigation