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Proceedings of the 10th International Symposium

Modern Trends in Livestock Production, October 2-4, 2013

DETERMINATION OF TOXIC ELEMENTS IN WILD BIRDS FROM THE AREA OF VOJVODINA Ž. Mihaljev, M. Živkov-Baloš, M. Kapetanov, S. Jakšić

Scientific Veterinary Institute „Novi Sad“, Rumenački put 20, 21000 Novi Sad, Republic of Serbia Corresponding author: zeljko@niv.ns.ac.rs Original scientific paper

Abstract: Content of lead, cadmium, arsenic and mercury was examined in 24

samples obtained from the following wild birds: Swan (Cygnus), March hen (Gallinula choloropus), Little egret (Egretta garzetta), Buzzard eagle (Buteo buteo), White-tailed eagle (Haliaeetus albicilla), Seagull (Larus ridibundus), White stork (Ciconia ciconia), Wild mallard (Anas platyrhynchos), Grey heron (Ardea cinerea). The samples of muscle tissue, liver, kidneys and heart tissue were analyzed. The samples were prepared by wet digestion using Ethos, Labstation Microwave, Milestone. Lead, cadmium, arsenic and mercury were analyzed by the method of coupled plasma on the Agilent ICP-MS 7700. The highest lead contents were registered in the liver and kidneys of the examined birds, with average values of 0.372 ± 0.290 mg/kg and 0.384 ± 0.168 mg/kg, respectively. The highest cadmium concentrations were recorded in the same organs, being averagely 0.083 ± 0.077 mg/kg in the liver and 0.248 ± 0.052 mg/kg in the kidneys. The content of arsenic was very low in all investigated samples (< 0.10 mg/kg). In some samples, significantly increased mercury content was established. The levels of mercury in the meat of grey heron, liver of white-tailed eagle and kidney of white-tailed eagle were 0.717 mg/kg, 1.128 mg/kg and as much as 3.656 mg/kg, respectively.

Key words: lead, cadmium, arsenic, mercury, wild birds

Introduction

In order to fully understand the exposure of animals to the pollutants originating from the environment and to assess their harmful effects and estimate the risk, it is necessary to carry out a systematic study and collect data on the degree and type of pollution, as well as distribution of hazardous chemicals in the environment. Nowadays, a number of studies have been focused on determination of chemical contaminants in animal tissues and organs (Milošević and Vitorović, 1992). The obtained results enable the assessment of human exposure to negative effects of these pollutants.

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Many wild animals are exposed to different toxic substances by consuming contaminated plants and animals, water, soil and air (Saičić et al., 1995). Since animals can move freely and find their own food, the game (including wild birds) is a link in the chain that accumulates pollutants from the environment. Therefore, wildlife species in certain geographic areas may represent a good indicator of environmental pollution, especially certain chemical elements, as they eat unprocessed plants in a particular habitat (Mihaljev et al., 1990, 1991). It should be noted that the accumulation of chemical elements is affected by endogenous factors (age, sex, health status of animals) and exogenous factors (geography, hydrological conditions, soil, climate, plant life). The importance of this issue is proved by the fact that a completely new discipline is being developed - wildlife toxicology - which includes examining the effects of toxins on wildlife (Živanov, 2001). Recently, comprehensive analysis of the extent and structure of mortality in protected endangered wild animals was performed. The results of pathoanatomical and biological examination strongly suggested that man is directly or indirectly responsible for the mortality (Kapetanov et al., 2012). The consequence of technological development is general pollution of the environment resulting from a range of contaminants. Ingestion of small amounts of a toxic substance over a longer period results in its accumulation in various tissues, causing chronic poisoning and inducing different diseases and even death (Pavkov et al., 1993; Mašić et al., 2001). Thus, the main objective of this study was to determine the number and type of chemical elements accumulated in the samples of wild birds, and, based on these results, determine the sites with increased content of chemical contaminants. This would enable identification of increasing contaminant levels and determination of appropriate corrective aimed at reducing environmental contamination by chemical agents with the purpose of improving the environment protection and preserving protected and highly protected wild animals.

Material and Methods

A total of 24 samples were tested on the content of trace elements in wild birds: Swan (Cygnus), March hen (Gallinula choloropus), Little egret (Egretta garzetta), Buzzard eagle (Buteo buteo), White-tailed eagle (Haliaeetus albicilla), Seagull (Larus ridibundus), White stork (Ciconia ciconia), Wild mallard (Anas platyrhynchos), Grey heron (Ardea cinerea) (Wüst , 1970). Samples of muscle tissue, liver, kidneys and heart collected from wild birds were individually analyzed. The samples were prepared by wet digestion using Ethos, Labstation Microwave, Milestone. Manganese, iron, copper and zinc were determined using atomic absorption spectrophotometry on the Varian Spectraa-10. Nickel, cobalt and

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selenium were analyzed by a technique of coupled plasma on the Agilent ICP-MS 7700. Considering the lack of referent values for the maximum permissible levels of metals and non-metals in tissues of wild species, the obtained results were evaluated and compared applying the maximum permissible levels of particular contaminant in animal feed (Pravilnik, 2011). Results and Discussion The results of our research are presented in Tables 1 and 2. Table 1. Contents of toxic elements in the examined samples from wild birds

Analyzed elements No

Type of sample Pb

mg/kg Cd

mg/kg As

mg/kg Hg

mg/kg 1. Swan – meat 0.096 0.008 0.022 0.028 2. March hen – meat 0.083 0.006 0.063 0.014 3. Little egret - meat 0.078 0.003 0.006 0.717 4. Swan - meat 0.089 0.002 0.016 < 0.001 5. Swan - meat 0.066 0.008 0.016 < 0.001 6. Buzzard eagle male – meat 0.125 0.004 0.003 0.050 7. Buzzard eagle male - liver 0.888 0.047 0.003 0.119 8. Buzzard eagle male - kidney 0.629 0.328 0.005 0.113 9. Buzzard eagle female-meat (meat) 0.092 0.013 0.010 0.148 10. Buzzard eagle female - liver (liver) 0.262 0.201 0.008 0.418 11. Buzzard eagle female-kidney 0.402 0.238 0.003 0.089 12. White-tailed eagle – meat 0.108 0.007 0.003 0.450 13. White-tailed eagle – liver 0.265 0.024 0.002 1.128 14. White-tailed eagle – kidney 0.430 0.228 0.010 3.656 15. White stork – meat 0.100 0.003 0.008 0.179 16. White-tailed eagle – meat 0.075 0.001 0.022 0.437 17. White-tailed eagle – liver 0.200 0.023 0.013 0.824 18. White-tailed eagle – kidney 0.269 0.185 0.014 0.931 19. White-tailed eagle – heart 0.146 0.003 0.012 0.530 20. Seagull - muscle 0.075 0.013 0.058 0.136 21. Wild mallard - muscle 0.073 0.002 0.010 < 0.001 22. Grey heron – meat 0.077 0.008 0.004 0.426 23. Grey heron – liver 0.243 0.118 0.008 2.132 24. Grey heron - kidney 0.192 0.259 0.010 0.634

The contents of lead, cadmium, arsenic and mercury determined in the examined samples are displayed in Table 1. Notably high lead contents were observed in male Buzzard eagle, being 0.125 mg/kg in meat, 0.888 mg/kg in the liver and 0.629 mg/kg in the kidneys. Moreover, increased lead contents were

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found in the meat of White-tailed eagle, being 0.108 mg/kg. We used the maximum permissible levels of metals and non-metals in feed (Pravilnik, 2011) as the “guideline” permissible values, which imply maximum permitted contents of lead in meat and entrails of 0.10 mg/kg and 0.50 mg/kg, respectively. Maximum permissible content of cadmium in meat is 0.050 mg/kg, whereas contents in the entrails are 0.50 mg/kg and 1.0 mg/kg in liver and kidneys, respectively (Pravilnik, 2011). Data presented in Table 1 indicate that kidneys are critical organ in a view of cadmium content, as the highest cadmium level was determined in the kidney of Buzzard eagle, reaching as high as 0.328 mg/kg. A group of authors (Saičić et al., 1995) reported similar values of kidney cadmium obtained in their research. In all meat samples examined, the content of cadmium was significantly below the maximum permissible values, which corresponds with our former research (Kljajić et al., 1994). Highest arsenic contents were established in meat of March hen (0.063 mg/kg), Seagull muscle tissue (0.058 mg/kg) as well as in the meat of Swan (0.022 mg/kg) and White-tailed eagle (0.022 mg/kg). Arsenic contents determined in all other meat samples and all liver and kidney samples were very low, below 0.02 mg/kg. Since the maximum permissible contents of arsenic in meat and entrails (Pravilnik, 2011) are 0.1 mg/kg and 0.5 mg/kg, respectively, we may conclude that examined samples of wild birds did not manifest any significant arsenic contamination. This is in accordance with the results reported by other authors (Saičić et al., 1995). If maximum permissible levels of metals and non-metals in feed (Pravilnik, 2011) are considered the “guideline” permissible values, the maximum permissible mercury contents are 0.03 mg/kg in meat and 0.10 mg/kg in the entrails. According to data displayed in Table 1, highly increased mercury content was determined in 80% of examined samples. Only in five samples, the content of mercury was within the ranges that could be considered normal. It is important to emphasize that mercury levels measured in some samples exceed the established guideline values by several times. Thus, mercury content in Grey heron meat was 0.717 mg/kg, which is 24 times higher than the maximum permissible value. Mercury contents in the liver of Grey heron (2.132 mg/kg) and in kidneys of White-tailed eagle (3.656 mg/kg) were 21-fold and 37-fold higher than the maximum permissible guideline values, respectively.

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Table 2: Total number of analysed samples (n), the mean value of the elements in different sample types (σ) and the interval of measured values (Iv)

Analyzed elements No

Type of sample Pb

mg/kg Cd

mg/kg As

mg/kg Hg

mg/kg

1.

Meat n=13

σ=0.088 ± 0.016 Iv=0.073 - 0.125

n=13 σ=0.006 ± 0.004 Iv=0.001- 0.013

n=13 σ=0.018 ± 0.017 Iv=0.010 - 0.063

n=13 σ= 0.199

Iv=<0.001-0.717

2.

Liver

n=5 σ=0.372 ± 0.290 Iv=0.200 - 0.888

n=5 σ=0.083 ± 0.077 Iv=0.023 - 0.201

n=5 σ=0.007 ± 0.004 Iv=0.002 - 0.013

n=5 σ=0.924 ± 0.777 Iv=0.119 - 2.132

3.

Kidneys

n=5 σ=0.384 ± 0.168 Iv=0.192 - 0.629

n=5 σ=0.248 ± 0.052 Iv=0.185 - 0.328

n=5 σ=0.008 ± 0.004 Iv=0.010 - 0.014

n=5 σ= 1.085

Iv=0.089 – 3.656

4.

Heart

n=1 0.146

n=1 0.003

n=1 0.012

n=1 0.530

According to the results presented in Table 2, the highest contents of lead, cadmium and mercury were established in kidneys of examined wild species, with average values being: Pb = 0.384 mg/kg, Cd = 0.248 mg/kg and Hg = 1.085 mg/kg. The content of this contaminant was very high also in the liver, being: Pb=0.372 mg/kg, Cd=0.083 mg/kg and Hg=0.924 mg/kg that fully corresponds with the existing data on bioaccumulation of these toxic elements (Puls, 1990). Upon resorption into blood, these heavy metals are very quickly transported to tissue and organ cells (Kastori, 1997). They are not biogenic and their effects are exclusively toxic. Tolerance of the body to these metals is strongly dependant on their concentration, mutual relationship and presence of other microelements (Zn, Cu, Se, Fe) that may reduce or prevent their toxic effects and that positively affect the detoxification process (Šarkanj et al., 2010). Arsenic content that was determined in the analyzed samples of meat, liver, kidneys and heart muscle was very low, being averagely below 0.02 mg/kg in all sample types. Our analysis furthermore confirmed apparent presence of most toxic elements (Pb, Cd, As, Hg) at detectable levels in all types of investigated samples. Other authors (Mihaljev et al., 1997; Brajković et al., 2010) also reported presence of increased levels of heavy metals and other microelements as well as other chemical pollutants, e.g. pesticide carbofuran. The aforementioned results strongly indicate that establishing high levels of diverse residues in tissues of wild animals put forward not only the issue of animal health, but also a wider ecological aspects and potential threat for human health considering that wild birds represent an important and valuable bioindicator of environmental pollution. In that respect, results of analysis of meat, liver and kidney samples from Grey heron are particularly interesting, as they revealed particularly high contents

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of some microelements (Mihaljev et al., 2012),predominantly of mercury. Elevated levels of lead in meat and liver of examined eagles, as well as extremely high mercury content in all organs of these birds strongly suggest the contamination of the environment with these pollutants. Thus, it would be of great importance to perform the assessment of the area of origin of these wild birds and to determine the potential sources of such contamination. Increased concentrations of lead in samples of heart muscle, meat, liver and kidneys of examined eagles are noteworthy. The most important finding within this research is the awareness of massive mercury contamination within the population of protected endangered wild birds. After entering the body, mercury inhibits enzyme systems, provokes lysosomal damage and poisoning of the central nervous system. The highest amounts of mercury are accumulated by the proteins of brain, liver, kidneys and gastro intestinal system (Mihaljev et al., 2003). Mutagenic and teratogenic features and its well-established toxicity qualify mercury among the most dangerous environmental pollutants. Conclusion Results of our research indicated that samples obtained from wild birds revealed presence of toxic metals, above all the lead and mercury. Their highest average levels were determined in the liver and kidneys. Presence of detectable and measurable levels of cadmium and arsenic in all organs and tissues was surprising, and should be particularly emphasized. In that respect, further research should be focused on investigating causes and origin of these elements in the soil and plants. Our results suggest that pollution of the biosphere with chemical contaminants should be systematically monitored to identify potential increasing contamination tendencies and with an aim of producing healthy and safe food and environmental protection. Effective protection of wild birds against these dangerous agents requires comprehensive examination of largest possible number of samples in order to locate the pollution sources and obtain a more realistic picture of the investigated regions. Acknowledgment Research was financed by the Ministry of Education, Science and Technological Development, Republic of Serbia, project No TR 31084.

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Određivanje toksičnih elemenata kod divljih ptica sa područja Vojvodine

Ž. Mihaljev, M. Živkov-Baloš, M. Kapetanov, S. Jakšić Rezime Sadržaj olova, kadmijuma, arsena i žive ispitan je u 24 uzorka divljih ptica, i to: labud (Cygnus), barska koka (Gallinula choloropus), mala bela čaplja (Egretta garzetta), orao mišar (Buteo buteo), orao belorepan (Haliaeetus albicilla), galeb (Larus ridibundus), bela roda (Ciconia ciconia), divlja patka (Anas platyrhynchos), siva čaplja (Ardea cinerea). Od sakupljenih ptica posebno je analizirano mišićno tkivo, jetra, bubrezi i srce. Uzorci za merenje su pripremljeni metodom vlažne digestije u sistemu Ethos, Labstation Microwave, Milestone. Olovo, kadmijum, arsen i živa određeni su metodom induktivno spregnute plazme na instrumentu Agilent ICP-MS 7700. Najveći sadržaj olova izmeren je u jetri i bubrezima ispitivanih ptica i iznosio je u proseku 0,372 ± 0,290 mg/kg za jetru i 0,384 ± 0,168 mg/kg za bubrege. U jetri i bubrezima ispitivanih ptica takođe je izmeren i najveći sadržaj kadmijuma, koji je prosečno iznosio u jetri 0,083 ± 0,077 mg/kg, a u bubrezima 0,248 ± 0,052 mg/kg. Utvrđeni sadržaj arsena u svim ispitanim uzorcima je veoma nizak (< 0,10 mg/kg). U nekim ispitanim uzorcima utvrđeno je prisustvo žive u veoma povišenim koncentracijama. U uzorku mesa sive čaplje koncentracija žive iznosila je 0,717 mg/kg, u jetri orla belorepana 1,128 mg/kg a u bubregu orla belorepana čak 3,656 mg/kg. References BRAJKOVIĆ G., RANČIĆ D., JOVANOVIĆ M., KILIBARDA V. (2010): Analytical Confirmation of poisoning Carbofuran by HPLC-PDA Method. Medicinska revija, 2, 4, 381-384. KAPETANOV M., STOJANOV IĆ., MIHALJEV Ž. (2012): Analiza strukture mortaliteta zaštićenih i strogo zaštićenih divljih životinja na teritoriji AP Vojvodine u periodu od jedne godine. International Symposium on Hunting, „Savremeni aspekti održivog gazdovanja populacijama divljači“, Zbornik radova, Zemun-Beograd, Srbija, 98-102. KASTORI R. (1997): Heavy Metals in the Environment. Naučni institut za ratarstvo i povrtarstvo, Novi Sad, 261-297. KLJAJIĆ R., PAVKOV S., MAŠIĆ Z., MIHALJEV Ž., MITROVIĆ R., RADOŠEVIĆ P. (1994): Levels of Radionuclides, Toxic Metals and Organochlorine Insecticides in the meat of Hunting game. Archives of toxicology, kinetics and xenobiotic metabolism, 377-378.

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MAŠIĆ Z., KLJAJIĆ R., MIHALJEV Ž., ŽIVKOV-BALOŠ M., ĐILAS S. (2001): Teški metali u životnoj sredini kao faktor poremećaja zdravlja životinja. Zbornik radova 13. Savetovanje veterinara Srbije, Zlatibor, 115-126. MIHALJEV Ž., ĐURIĆ G., SLIVKA J. (1991): Ugroženost ždralova radionuklidima i toksičnim hemijskim materijama. Zbornik radova 4. Simpozijuma ″Divljač i priroda″, Brioni, Savez veterinara i veterinarskih tehničara Jugoslavije, 206-210. MIHALJEV Ž.,VESKOVIĆ M., ĐURIĆ G. (1990): Game as bioindicator of the radiocontamination. Acta Veterinaria, 40, 4, 229-234. MIHALJEV Ž., ŽIVKOV-BALOŠ M., KAPETANOV M., JAKŠIĆ S. (2012): Sadržaj mikroelemenata u divljim pticama sa područja Vojvodine. Zbornik radova International Symposium on Hunting, „Savremeni aspekti održivog gazdovanja populacijama divljači“, Zemun-Beograd, Srbija, 129-131. MIHALJEV Ž., ŽIVKOV M., PAVKOV S.,KLJAJIĆ R. (1997): The radioactiviti level of radionuclides and the content of pesticides and toxic metals in peasants. Abstracts XIth International Congress of the World Veterinary Poultry Association, Budapest, Hungarian Branch of the World Veterinary Poultry Association, 301. MIHALJEV Ž., ŽIVKOV-BALOŠ M., RATAJAC R. (2003): Rasprostranjenost žive u različitim uzorcima iz životne sredine. Monografija, Ekološki pokret grada Novog Sada, Novi Sad, 483-488. MILOŠEVIĆ M., VITOROVIĆ S. (1992): Osnovi toksikologije sa elementima ekotoksikologije, Naučna knjiga, Beograd, 151-156. PAVKOV S., MAŠIĆ Z., MIHALJEV Ž., KAPETANOV M., KAPETANOV R. (1993): Ispitivanje uticaja mikroelemenata i toksičnih metala iz hraniva na živinarsku proizvodnju. Zbornik kratkih sadržaja II Savetovanja živinara Jugoslavije, Tivat,7-9, 75-77. PULS R. (1990): Mineral levels in Animal Health. Published by Sherpa International, Clearbrook, Canada. SAIČIĆ S., BASTIĆ LJ., PEROVIĆ M., RISTIĆ S. (1995): Određivanje arsena i teških metala u mesu i organima divljači. Tehnologija mesa, 2-3, 223-226. SLUŽBENI GLASNIK REPUBLIKE SRBIJE, br. 28/2011: Pravilnik o dopuni Pravilnika o maksimalno dozvoljenim količinama ostataka sredstava za zaštitu bilja u hrani i hrani za životinje i o hrani i hrani za životinje za koju se utvrđuju maksimalno dozvoljene količine ostataka sredstava za zaštitu bilja (Prilog 5), 2011. ŠARKANJ B., KIPČIĆ D., VASIĆ-RAČKI Đ., DELAŠ F., GALIĆ K., KATALENIĆ M., DIMITROV N., KLAPEC T. (2010): Kemijske i fizikalne opasnosti u hrani. HAH, Osjek, 58-66. WÜST W.(1970): Die Brutvögel Mitteleuropas. Bayerischer Schulbuch-Verlag, München. ŽIVANOV D. (2001): Veterinarska toksikologija. Fakultet veterinarske medicine, Beograd,10-12.