Skip to main content
Log in

Assessment of Heavy Metal Accumulation in the Golden Jackal (Canis aureus) as a Possible Bioindicator in an Agricultural Environment in Bulgaria

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

Abstract

The aim of this study was to evaluate the residues of heavy metals as an indicator of environmental pollution in internal organs of golden jackal (Canis aureus) from an agricultural region in Bulgaria. It was demonstrated that the golden jackal has high potential for specific accumulation of heavy metals, thus implying that this species may serve as a biological indicator of their presence in the agricultural regions, which it inhabits. The concentrations of the targeted elements (mean [mg/kg of dried tissue] ± SD) were respectively: Cu—57.62 ± 10.76; Zn—141.45 ± 11.33; Ni—0.28 ± 0.19; Co—0.46 ± 0.30; Pb—6.88 ± 1.67 and Cd—0.58 ± 0.16 in liver and Cu—17.67 ± 5.01; Zn—58.28 ± 10.81; Ni—0.51 ± 0.4; Co—0.52 ± 0.29; Pb—4.03 ± 1.32 and Cd—1.41 ± 0.22 in kidney samples. The concentrations we found revealed the specific accumulation of these metals in golden jackal and provide values, within which negative effects on the advancement of its populations should not be expected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • AEFA (2014) Game numbers in Bulgaria. Archive of the Executive Forest Agency of Ministry of Agriculture and Foods of R. Bulgaria, Sofia

  • Ansorge HK, Graeser H, Fink G (1993) Schwermetallruckstande beim Rotfuchs (Vulpes vulpes). Beitr Jagd-Wildforsch 18:79–82

    Google Scholar 

  • Arnold J, Humer A, Heltai M, Murariu D, Spassov N, Hackländer K (2012) Current status and distribution of golden jackals Canis aureus in Europe. Mammal Rev 42:1–11

    Article  Google Scholar 

  • Bilandžić N, Dezdek D, Sedak M, Dokić M, Solomun B, Varenina I, Knežević Z, Slavica A (2010) Concentration of trace elements in tissues of red fox (Vulpes vulpes) and stone marten (Martes foina) from suburban and rural areas in Croatia. Bull Environ Contam Toxicol 85:486–491

    Article  Google Scholar 

  • Brunn H, Georgii S, Bachour G, Elmadfa I (1991) Free-living animals as an indicator of environmental contamination. Tierärztl Umschau 46:549–553

    Google Scholar 

  • Bukovjan K (1997) Concentration of selected foreign substances in the tissues of fox Vulpes vulpes L. Folia Venatoria 26(27):107–112

    Google Scholar 

  • Chang LW, Magos L, Suzuki T (eds) (1996) Toxicology of metals. CRC Press, Boca Raton

    Google Scholar 

  • Ćirović D, Gizejewska A, Jovanović V, Penezić A, Milenković M, Vujošević M, Blagojević J (2015) Concentration of selected trace elements in the golden jackal (Canis aureus L., 1758) population from Serbia. Acta Zool Bulg 67(3):409–414

    Google Scholar 

  • Corbet G, Harris V (1991) The handbook of British mammals, 3rd edn. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Corsolini S, Focardi S, Leonzio S, Lovari S, Monaci F, Romeo G (1999) Heavy metals and chlorinated hydrocarbon concentrations in the red fox in relation to some biological parameters. Environ Monit Assess 54:87–100

    Article  CAS  Google Scholar 

  • Dehn LA, Follmann EH, Thomas DL, Sheffield GG, Rosa C, Duffy LK, O’Hara TM (2006) Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci Total Environ 362:103–123

    Article  CAS  Google Scholar 

  • Dip R, Stieger C, Deplazes P, Hegglin D, Muller U, Dafflon O, Koch H, Naegeli H (2001) Comparison of heavy metal concentration in tissues of red foxes from adjacent urban, suburban and rural areas. Arch Environ Contam Toxicol 40:551–556

    Article  CAS  Google Scholar 

  • Donchev D, Karakashev H (2004) Physical and socio-economical geography of Bulgaria. Slovo, Veliko Tarnovo

    Google Scholar 

  • Driscoll CT, Han YJ, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the northwestern United States. Bioscience 57:17–28

    Article  Google Scholar 

  • E-PRTR, European Pollutant Release and Transfer Register (2010) http://prtr.ec.europa.eu/Home.aspx

  • Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187(4):201. doi:10.1007/s10661-015-4436-3

    Article  Google Scholar 

  • Genov P, Vassilev K (1991) Density and damages caused by jackal (Canis aureus L.) to livestock in Southern Bulgaria. Ecologia Bulg Acad Sci 24:58–65

    Google Scholar 

  • Gimeno-García E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25

    Article  Google Scholar 

  • Goyer RA (1986) Toxic effects of metals. In: Klaassen CD, Amdur M, Doull J (eds) Casarett and Doull’s toxicology. The basic science of poisons, 3rd edn. Macmillan Publishing Company, New York, pp 582–635

    Google Scholar 

  • Heltai M, Markov G (2012) Red fox (Vulpes vulpes Linnaeus, 1758) as biological indicator for environmental pollution in Hungary. Bull Environ Contam Toxicol 89:910–914

    Article  CAS  Google Scholar 

  • Horai S, Minagawa M, Ozaki H, Watanabe I, Takeda Y, Yamada K, Ando T, Akiba S, Abe S, Kuno K (2006) Accumulation of Hg and other heavy metals in the Javan mongoose (Herpestes javanicus) captured on Amamioshima Island, Japan. Chemosphere 65:657–665

    Article  CAS  Google Scholar 

  • Jhala YU, Moehlman PD (2004) Golden jackal. In: Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) Canids, foxes, wolves, jackals and dogs. International Union for Conservation of Nature and Natural Resources, Gland, pp 156–161

    Google Scholar 

  • Jhala Y, Moehlman P (2008) Canis aureus. In: IUCN red list of threatened species. Version 2010.4. www.iucnredlist.org

  • Kryštufek B, Murariu D, Kurtonur C (1997) Present distribution of the golden jackal Canis aureus in the Balkans and adjacent regions. Mammal Rev 27:109–114

    Article  Google Scholar 

  • Lanocha N, Kalisinska E, Kosik-Bogacka DI, Budis H, Sokolowski S, Bohatyrewicz A (2013) Comparison of metal concentrations in bones of long-living mammals. Biol Trace Elem Res 152(2):195–203. doi:10.1007/s12011-013-9615-x

    Article  CAS  Google Scholar 

  • Lanszki J, Heltai M (2002) Feeding habits of golden jackal and red fox in southwestern Hungary during winter and spring. Mamm Biol 67:129–136. doi:10.1078/1616-5047-00020

    Google Scholar 

  • Lanszki J, Kurys A, Heltai M, Csányi S, Ács K (2015) Diet composition of the golden jackal in an area of intensive big game management. Ann Zool Fenn 52(4):243–255. doi:10.5735/086.052.0403

    Article  Google Scholar 

  • Lombaard D (1971) Age determination and growth curves in the black-backed jackal. Ann Transv Mus 27:135–169

    Google Scholar 

  • Luckey T, Venugopal B (1977) Metal toxicity in mammals. I. Plenum Press, New York

    Google Scholar 

  • Malvandi H, Ghasempouri SM, Esmaili-Sari A, Bahramifar N (2010) Evaluation of the suitability of application of golden jackal (Canis aureus) hair as a noninvasive technique for determination of body burden mercury. Ecotoxicology 19(6):997–1002

    Article  CAS  Google Scholar 

  • Markov G (2012a) Jackal (Canis aureus L.) in Bulgaria: What is going on? Acta Zool Bulg Suppl 4:67–71

    Google Scholar 

  • Markov G (2012b) Residual heavy metal concentrations in the fat dormouse (Glis glis) in an agricultural region of Bulgaria. Peckiana 8:229–234

    Google Scholar 

  • Markov G, Dekov O (2008) Actual numbers of main pest rodent species in Bulgarian agricultural ecosystems in 2004–2008. Ann Konstantin Preslavski Univ Shumen XIX(B6):73–82

    Google Scholar 

  • Markov G, Gospodinova M (2006) Residuals of heavy metals in the red fox (Vulpes vulpes) from agricultural region. In: Proceedings of Second Scientific Conference with International Participation, “Space, ecology, safety” SENS2006, Varna, pp. 1–5

  • Markov G, Lanszki J (2012) Diet composition of the golden jackal, Canis aureus in an agricultural environment. Folia Zool 61(1):44–48

    Google Scholar 

  • Markov G, Dekov O, Kocheva M (2009) Risk assessment of outbreak of rodents as main pests in agricultural crops in Bulgaria in 2009. In: Proceedings of Fifth Scientific Conference with International Participation, “Space, ecology, nanotechnology, safety”, Sofia, pp. 286–293

  • Millán J, Mateo R, Taggart MA, Lñpez-Bao JV, Viota M, Monsalve L, Camarero PR, Blézquez E, Jiménez B (2008) Levels of heavy metals and metalloids in critically endangered Iberian lynx and other wild carnivores from Southern Spain. Sci Total Environ 399:193–201

    Article  Google Scholar 

  • Morris P (1997) The edible dormouse (Glis glis). The Mammal Society, London, pp 1–20

    Google Scholar 

  • Nowak R (1999) Walker’s mammals of the world, 6th edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • OSHA (2004) Safety and health topics: toxic metals. US Dept. of Labor, Occupational Safety and Health (OSHA)

  • OSMH (2015) Official site of the municipality of Hissar. http://hisar.bg

  • Parker S (1990) Grzimek’s encyclopedia of mammals (English Language Edition). McGraw Hill Publishing Company, New York

    Google Scholar 

  • Penezić A, Ćirović D (2015) Seasonal variation in diet of the golden jackal (Canis aureus) in Serbia. Mammal Res 60(4):309–317

    Article  Google Scholar 

  • Reynolds J, Trapper SC (1995) The ecology of the red fox Vulpes vulpes in relation to small game in rural southern England. Wildl Biol 1:105–119

    Google Scholar 

  • Sawicka-Kapusta K (1979) Roe deer antlers as bioindicators of environmental pollution in Southern Poland. Environ Pollut 19:283–293

    Article  CAS  Google Scholar 

  • Spassov N (2007) The jackal, Canis aureus (Linnaeus 17Б8). In: Miteva S, Mihova B, Georgiev K, Petrov B, Vansink D (eds) The mammals, important for conservation in bulgaria, vol 6. Dutch Mammal Society VZZ, Arnhem, pp 234–238

    Google Scholar 

  • STATISTICA (data analysis software system) (2008) StatSoft, Inc. version 8.0. www.statsoft.com

  • Stenin G, Kolev N, Mitov I (1983) Some aspects of jackal’s dispersion. Hunt Fish Econ 7:28–30

    Google Scholar 

  • Talmage S, Walton B (1991) Small mammals as monitors of environmental contaminants. Rev Environ Contam Toxicol 119:47–108

    CAS  Google Scholar 

  • Tataruch F, Kierdorf H (2003) Mammals as biomonitors, Chapter 20. In: Markert BA, Breure AM, Zechmeister HG (eds) Trace metals and other contaminants in the environment, vol 6. Elsevier, Amsterdam, pp 737–772

    Google Scholar 

  • Tchounwou P, Newsome C, Williams J, Glass K (2008) Copper-induced cytotoxicity and transcriptional activation of stress genes in human liver carcinoma cells. Metal Ions Biol Med 10:285–290

    Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. EXS 101:133–164. doi:10.1007/978-3-7643-8340-4_6

    Google Scholar 

  • Varsha G (2013) Mammalian feces as bio-indicator of heavy metal contamination in Bikaner Zoological Garden, Rajasthan. Res J Anim Vet Fish Sci 1(5):10–15

    Google Scholar 

  • WHO/FAO/IAEA (1996) Trace elements in human nutrition and health. World Health Organization, Geneva

    Google Scholar 

  • Wren D (1986) Mammals as biological monitors of environmental metal levels. Environ Monit Assess 6(2):127–144

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We wish to express our gratitude to all collaborators in the field who helped in collecting the material for this study. Thanks to the reviewers for their helpful comments. This work was supported by BAN and SANU bilateral project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgi Markov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Markov, G., Kocheva, M. & Gospodinova, M. Assessment of Heavy Metal Accumulation in the Golden Jackal (Canis aureus) as a Possible Bioindicator in an Agricultural Environment in Bulgaria. Bull Environ Contam Toxicol 96, 458–464 (2016). https://doi.org/10.1007/s00128-016-1754-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-016-1754-2

Keywords

Navigation