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Concentration of Selected Trace Elements in the Golden Jackal (Canis aureus L., 1758) Population from

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Concentration of Selected Trace Elements in the Golden Jackal (Canis aureus L., 1758) Population from Serbia

Duško Ćirović1,*, Aleksandra Gizejewska2, Vladimir Jovanović3, Aleksandra Penezić1, Miroljub Milenković3, Mladen Vujošević3, Jelena Blagojević3

1 Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia 2 Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Oczapow- skiego 2, Olsztyn, Poland 3 Institute for Biological Research “Siniša Stanković”, University of Belgrade, Bulevar Despota Stefana 142, Belgrade, Serbia

Abstract: Golden jackal is considered a top predator in many human dominated landscapes of South-eastern Europe. Concentrations of seven trace elements (Pb, Cd, Zn, Cu, Fe, Mn, and Ni) in livers of 129 specimens of golden jackals (Canis aureus) from six localities from Serbia were analysed. Both, sex and localities had no significant effects on concentrations of any metals. Lead concentrations, both average (9.59 mg/kg) and maximal values (23.00 mg/kg), were higher than those found in other mammal predator species. Fur- thermore, concentrations of essential trace elements (copper, iron and manganese) were also significantly higher than those reported by other researchers. Only zinc had significantly lower concentration (66.36 mg/kg), while cadmium was similar (14.89 mg/kg) with those reported in the literature. The jackal, be- ing a wild omnivorous mammal at the top of the food chain with high adaptability and other supportive ecological features, is a good bioindicator of environmental contamination.

Key words: Canis aureus, golden jackal, trace elements, Serbia

Introduction Industrial development leads to emissions of vari- ing. Cadmium concentrations in the environment ous pollutants, such as heavy metals (Fr i t s c h et al. increased due to industrial contamination, result- 2010). Heavy metals occur naturally but increased ing from waste incineration and fertilizer produc- metal contents in the environmental can be attrib- tion, often at a local scale. Others metals (e.g. cop- uted to atmospheric deposition from anthropogenic per, zinc, iron) are essential for various life forms at sources as well as mobilisation from soils, bottom low levels, but in higher concentrations can disturb sediments of lakes, and rivers. They persist in the en- metabolism and growth of organisms (Bi l a n d ž i ć et vironment and animal tissues over prolonged time. al. 2012). Regular exposure to toxic metals results Some metals, like lead and cadmium can cause toxic in chronic poisoning and poses serious threats, for effects even in small doses (Sc h e u h a m m e r 1987, instance nephrotoxic and hepatotoxic effects, which Bu r g e r 2008). The main sources of lead contami- can produce remote effects manifested in successive nation are industrial plants, coal combustion, auto- generations (Pi s k o r o v a et al. 2003) and influence motive industry and wastewater treatment plants. entire populations (La n s z k i et al. 2009). Long-term exposure to lead contributes to non-toxic High level of pollution in altered environments phosphates accumulation of lead in bones, but in pe- demand careful biomonitoring of soil, air, water, liv- riods of increased demand of minerals lead can be ing organisms and food products (Kr a m a r o v a et al. released from bones leading to secondary poison- 2005). Animals respond differently to environmental

*Corresponding author: [email protected]

409 Ćirović D., A. Gizejewska, V. Jovanović, A. Penezić, M. Milenković, M. Vujošević, J. Blagojević contamination, and the presence of toxic substances (Surčin) to 23% () of the study areas. Alluvial in the environment and their accumulation in animal willow (Salix sp.) and white poplar (Populus alba) tissues need to be studied for a better understanding forests were present along the rivers. Away from the of the effects of pollutants on every element of the rivers, mixed forests consisted predominantly of oak environment. (Quercus sp.), narrow leaved ash (Fraxinus angus- Golden jackal (Canis aureus L., 1758) is the tifolia), and common hornbeam (Carpinus betulus). largest and the only jackal outside Africa. It is the Agriculture is the dominant economic activity at all most widely distributed canid species, occurring in chosen localities with small amount of pesticides used Northern and Eastern Africa, Asia Minor, Middle during production. There are no large industrial facili- East, Central and Southern Asia, and South-eastern ties, except in (steelworks) and a chemical Europe (Jh a l a & Mo e h l m a n 2004). Golden jackal factory in Negotin which was closed 20 years ago. is believed to be a highly adaptable species due to In Serbia the main areas of the golden jackal’s its omnivorous diet consisted mainly of small mam- distribution are along the north-eastern border with mals (La n s z k i et al. 2010, Ma r k o v & La n s z k i 2012), Bulgaria, and the Plain of Srem. In the northeast of livestock remains and carcasses (La n s z k i et al. 2010, the country large populations are present in the vicin- Ći r o v i ć et al. 2014), and human refuse (Ja e g e r et ity of Negotin and Bela Palanka (Šá l e k et al. 2014). al. 2007). Due to theirs opportunistic foraging be- From the surroundings of Negotin jackals have haviour, jackals are capable to survive in different spread into Velika Morava River valley. Population environments, with high local densities (Jh a l a & from the Plain of Srem expanded along the banks of Mo e h l m a n 2004, Šá l e k et al. 2014). river Sava up to the slopes of Fruška Gora mountain. The aim of this study was to (i) determine the (Mi l e n k o v i ć & Pa u n o v i ć 2003). concentrations of lead (Pb), cadmium (Cd), zinc (Zn), copper (Cu), iron (Fe), manganese (Mn) and nickel Collected material (Ni) in livers of golden jackals from various areas Bodies of 129 specimens of golden jackals were of Serbia; (ii); estimate the degree of environmental collected in cooperation with local hunting organi- pollution in the examined area; and (iii) determine zations. Most of these animals were legally hunted that golden jackal tissues can serve as bioindicator of metal pollution.

Material and Methods Study area This study was conducted on liver tissue sam- ples obtained from six distinct areas in Serbia (Fig. 1). Localities where jackal carcasses were collected were along the rivers: Veliko Gradište – the Danube River, Negotin – the confluence of the Timok River with the Danube River, – the Resava River, – the Morava River, Smederevo – the conflu- ence of the Morava River with the Danube River, Surčin – the Sava River. Surčin and Smederevo were located in the alluvial plains only, while the other lo- calities (Veliko Gradište, Velika Plana, Svilajnac, and Negotin) extended to the surrounding foothills. The size of the area where jackals’ carcasses were collected varied from 50 km2 (Smederevo) to 197 km2 (Veliko Gradište). Predominantly the land was used for agriculture in all six areas, with crops (grain, maize, sunflower, soy bean) covering from 50% (Negotin) to 82% (Surčin) of the area. Meadows/pastures (1-13%) and orchards/vineyards (2-15%) were also present. Fig. 1. Location of the six sampling sites for analysis of Forests were represented by small fragments trace elements concentration in the liver of golden jackals within the agricultural matrix and covered from 6% in Serbia

410 Concentration of Selected Trace Elements in the Golden Jackal (Canis aureus L., 1758) Population from Serbia...

(n=124), while the rest were collected as road kills comparisons between localities. Significant differ- (n=5). Samples were collected during the winter of ences were accepted at level of probability p < 0.05. 2009/2010 (December-January). Since jackals give Statistical analyses were conducted using Statistica birth during spring, in this part of the year there are 5.1 software (Statsoft, Tulsa, OK, USA). no more pups in the population. After all the mor- phological measurements were taken skulls were Results cleaned and the shape and wear of maxillary incisors Average concentrations of Pb and Cd in golden were examined (following Lo m b a a r d 1971), we de- termined that all the jackals were adults specimens. jackal liver samples at the six localities were 9.59 Livers were removed in the field, and frozen at -20°C mg/kg and 14.89 mg/kg, respectively (Table 1). The for later analysis. highest Pb concentration was recorded from female jackals from Negotin (23.00 mg/kg). This group was Determination of trace elements also characterised by the highest concentration of Cd Trace element contents were determined by (37.67 mg/kg). No traces of Pb were found at Surčin, atomic absorption spectrometry (Thermo Scientific and the lowest Pb concentrations were detected from Solaar S Series AA) (REF). All liver samples were male jackals from Negotin (3.46 mg/kg). Cadmium dried using a Freeze Dryers Rotational-Vacuum- concentrations were the lowest at Veliko Gradište, Concentrator (GAMMA 1–16 LSC, Germany). both from males and females (1.75 mg/kg and 1.65 From each jackal a sample of 50 mg of dry liver was mg/kg, respectively, Table 1). taken. Furthermore, samples of dry livers from each Average concentration of Zn was 66.36 mg/ locality were pooled by sex. Samples were ground kg. Female jackals from Negotin had the highest Zn using porcelain mortar and a pestle and digested in concentrations (107.00 mg/kg), while the lowest was recorded in female jackals from Svilajnac (49.56 10 ml of a 2:1 mixture of concentrated HNO3 and mg/kg, Table 1). HClO4 (Merck, Germany). Samples were heated un- til perchloric acid white fumes were no longer vis- The average concentration of Cu was 57.85 mg/ ible and the solution became clear. Samples were kg. The highest Cu level of 104.33 mg/kg was found filtered after digestion and 50 ml of deionised water from female group inhabiting the area of Negotin, was added. The concentrations of the analysed met- while the lowest was reached in male jackals harvested als were expressed in mg/kg dry weight. in Svilajnac (39.63 mg/kg). The highest average con- centration in general was determined for Fe (1017.27 Statistical analyses mg/kg) with highest levels found in females inhabiting As the heavy metals concentrations were not the area of Negotin (1546.67 mg/kg; Table 1). normally distributed, the nonparametric Mann- The Mn concentrations were highest in female Whitney U-test was used for statistical compari- jackals from Negotin area (28.67 mg/kg). Average sons between genders and Kruskal-Wallis test for levels of Mn and Ni were 16.93 mg/kg and 13.43

Table 1. Mean concentrations of seven trace elements (mg/kg) in the liver of golden jackals at six study sites in Serbia, 2009-2010 (N - sample size; F – female, M -male)

Study site Sex N Pb Cd Zn Cu Fe Mn Ni F 5 - 15.71 54.88 70.38 1361.09 17.75 14.69 Surčin M 15 5.93 6.53 59.07 46.33 882.13 14.60 7.27 F 3 23.00 37.67 107.00 104.33 1546.67 28.67 40.67 Negotin M 13 3.46 9.23 52.23 48.92 560.08 15.39 7.08 F 5 19.00 30.00 82.8 91.2 1612.6 25.40 35.80 Velika Plana M 12 6.08 12.5 50.17 41.58 1294.5 16.17 10.58 F 9 5.33 18.22 49.56 47.78 760.00 17.33 11.33 Svilainac M 8 7.75 21.25 51.12 39.63 1042.5 18.13 14.13 F 15 4.40 12.07 53.07 54.27 886.6 15.33 8.73 Smederevo M 15 5.87 12.13 59.67 44.07 843.6 18.27 10.93 F 17 15.06 1.65 62.47 41.35 437.18 4.77 - Veliko Gradište M 12 19.25 1.75 114.33 64.33 980.33 11.33 - Average 129 9.59 14.89 66.36 57.85 1017.27 16.93 13.43

411 Ćirović D., A. Gizejewska, V. Jovanović, A. Penezić, M. Milenković, M. Vujošević, J. Blagojević mg/kg, respectively. The lowest Mn level of 4.77 increases (Pr a t e r 1980). Thus, males as heavier and mg/kg was registered for the female group harvested more mobile are more susceptible to accumulating in Veliko Gradište. Female jackals from Negotin pollutants, including heavy metals. Although vari- had the highest Ni concentrations (40.67 mg/kg) ation in concentration of different metals between and the lowest was found from males from Negotin gender exists, we found no significant sex-related (7.08 mg/kg). Traces of Ni were not found in Veliko differences in heavy metal accumulation, as opposed Gradište. to results of similar studies by Pa s s l a c k et al. (2014) Statistical analysis showed no significant dif- in horses and Va h t e r et al. (2007) in humans. ference between the sexes (Pb: U=18, p=0.963; Similar environmental conditions of human Cd: U=11, p=0.262; Zn: U=15, p=0.631; Cu: U=8, modified habitats were present at all the analysed p=0.109; Fe: U=16, p=0.749; Mn: U=14, p=0.522; localities and that could be the cause of the lack of Ni: U=6, p=0.065). Significant statistical differ- statistical difference in concentrations of analysed ences in concentrations of analysed metals were not metals among localities. Main source of pollution present among localities either. were agricultural chemicals which were widely used at all the localities. Although the steelwork near Discussion Smederevo and chemical industry near Negotin were not working during this study period, it is known that Both mammalian and avian wild predators’ high posi- most metals do not undergo microbial or chemical tion in food chain and wide-ranging behaviour make degradation and their total concentration in soils per- them prone to accumulate pollutants from wider are- sists for a long time after their introduction (Ad r i a n o as. Common wild birds are also a potential source of 2003). Moreover, heavy metals can be carried by air contamination, in particular with Pb (Ga s p a r i k et al. and water across significant distances, and they are 2010). Wild animals, mostly carnivores and omni- found even in regions that are situated remotely from vores, adapt to habitats near human settlements. This sources of industrial pollution. strategy provides them with additional food sources, Golden jackals were characterised by high Cd but it also exposes animals to anthropogenic pollut- and Pb levels which could affect zinc metabolism. ants such as pesticides, effluents and fluel gas emis- Diets deficient in Fe, Zn and Cu intensify Cd absorp- sions (Bi l a n d ž i ć et al. 2010). tion (Bu r g e r 2008) and accumulation in bodily tis- The group of trace elements whose presence sues (Ch r o b a c z y ń s k a et al. 2011). Diet rich in Cu was investigated in this study contains both highly reduced resorption of Pb from the digestive system toxic non-essential metals such as Cd and Pb, as well (Ch r o b a c z y ń s k a et al. 2011). as essential metals which are characterised by dose- Small mammals preyed upon golden jackals dependent toxicity. Essential trace elements, such as absorb trace elements, including highly toxic met- Cu, Zn, Fe and Mn, are required for growth and de- als, from soil, water, plants and air, and they are a velopment and have to be supplied with food. Their potential source of contamination for predatory ani- absorption is determined by the body’s nutritional mals inhabiting natural and agricultural ecosystems demand, physiological condition and the availabil- (Fr i t s c h et al. 2010). ity of food which is a rich source of those elements Although metal concentrations in food sources (Cz a j k o w s k a et al. 2011). typically consumed by golden jackals (e.g. small It is known that significant differences in metal mammals) were not examined at the six study sites, concentrations in animal tissues could occur between heavy metals concentrations in the bones of black- individuals of the same species (Di p et al. 2001, striped field mouse (Apodemus agrarius) in two ar- He l t a i & Ma r k o v 2012), as well as in different spe- eas in Serbia showed similar concentrations of Cu cies inhabiting the same region (Fr i e l et al. 1987). (54.118 mg/kg) and Zn (74.256 mg/kg) (Bl a g o j e v i ć Gender effect in heavy metals accumulation in this et al. 2012) as compared to our study. In the same study is determined most probably by the biology of study concentrations of Fe (5.629 mg/kg), Mn (1.129 the species. The size of golden jackal`s home range mg/kg) and Cd (0.213 mg/kg) were lower, while Pb depends on resource distribution, extent of human (25.965 mg/kg) and Ni (28.677 mg/kg) concentra- pressure, type of ecosystem, and is estimated to be tions were higher than in this study. In toxicologi- in the range from 1.1 to 20 km2 (Jh a l a & Mo e h l m a n cal study on hare (Lepus europaeus) from Serbia the 2004). In general, male jackals have wider home concentrations Cd and Zn were lower than in golden ranges than females (Gi a n n a t o s , 2004). Additionally jackal (Pe t r o v i ć et al. 2013). High levels of trace ele- the elimination rate of foreign compounds per unit ments in jackal livers could be attributed to the trans- body weight in mammals decreases as body weight fer of heavy metals from the food chain, in particular

412 Concentration of Selected Trace Elements in the Golden Jackal (Canis aureus L., 1758) Population from Serbia... for animals inhabiting polluted regions or feeding on conclusion about specific pollution at the studied the dumps in vicinity of human settlements (Ći r o v i ć locations. Due to commensalism with humans, om- et al. 2014). Mammals inhabiting suburban habitats nivorous diet and high position in food chain, golden are already recognised as good bioindicators of envi- jackal could be an appropriate bioindicator for envi- ronmental pollution (Bi l a n d ž i ć et al. 2012). ronmental pollution. It is known that if food resources are abun- dant enough, golden jackals can survive in habitats Acknowledgments: This work was supported by the Ministry of that are highly altered, including large urban areas Science and Technological Development of the Republic of Ser- (Ja e g e r et al. 2007). Currently, jackals are spreading bia (TR 31009 and 173003 grants), and BAN and SANU bilater- al project. We wish to express our gratitude to Petnica Research r n o l d across the European continent (A et al. 2012), Station which kindly allowed us the use of their equipment and reaching high local densities (Šá l e k et al. 2014). As especially to Ljubica Perić for technical assistance and all col- a wild omnivorous mammal at the top of the food laborators in the field who helped in collecting the material for chain which is characterised by high adaptability this study: Goran Blagojević (Surčin), Zoran Gubin, (Smeder- and other supportive ecological features, the jackal evo), Nenad Mirković, Slađan Marković, Goran Cvetković, is a good bioindicator of environmental contamina- Mladen Bogdanović (Veliko Gradište), Predrag Živanović (Velika Plana), Borko Dimitrijević, Boriša Dimitrijević, Bata tion (Bi l a n d ž i ć et al. 2010). However, we acknowl- Dimitrijević (Svilajnac), Zoran Tufarević-Moce and Slobodan edge that the great mobility of golden jackal hamper Kastratović (Negotin).

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