Barbary sheep tissues as bioindicators of radionuclide and stabile element contamination in Croatia: exposure assessment for consumers

  • Maja Lazarus
  • Pavao Gančević
  • Tatjana Orct
  • Delko Barišić
  • Klemen Jerina
  • Nikica ŠpremEmail author
Research Article


Muscle, liver and kidney of 21 Barbary sheep (Ammotragus lervia) from Mosor Mountain, Croatia, were sampled to quantify the activity of caesium and potassium radionuclides and five toxic and ten essential stabile elements in order to establish reference values for this species and to evaluate the potential of Barbary sheep tissues to reflect environmental pollution. We also assessed seasonal diet (botanical composition and dry matter content) of Barbary sheep based on analyses of a rumen content of culled animals. None of the 19 plant species (mostly grasses) identified as part of the Barbary sheep diet is known as a stabile element or radionuclide hyperaccumulator. Measured levels reflected low environmental pollution with arsenic, cadmium, mercury and lead, with levels generally less than those reported for wild herbivorous ungulates. Methodological differences (detection limit of elements in muscle) were shown to hamper interpretation and comparison of the Toxic Contamination Index (TCI) values with those published for other species. There was no homeostasis disturbance of trace elements in Barbary sheep, either due to inadequate intake via food or as an adverse effect due to a high toxic metal(loid) burden. Consumption of the muscle and liver of wild Barbary sheep can be considered safe for the health of adult consumers regarding toxic metal(loid)s and radioactive caesium, though the liver should be avoided as a food item in vulnerable population groups due to the possible adverse effects of cadmium and lead. Otherwise, muscle and liver are a rich source of copper, iron, selenium and zinc for consumers and, as such, can benefit the overall dietary intake of essential elements.


Ammotragus lervia Exotic species Toxic Contamination Index Environmental pollution Ungulate Metal accumulation 



We would like to thank Mr. Miro Olujić (Dalmacijalov Ltd.) for his invaluable assistance in providing the samples and in the field work, Ms. Brankica Šošić and Ms. Tija Mlinac for their botanical assistance and Mr. Erich Klansek (Research Institute of Wildlife Ecology, Vienna) for the diet analysis.

Funding information

Financial support for the chemical analyses carried out in this study was made by the Ministry of Science and Education of the Republic of Croatia through Institutional Funding made available to the Institute for Medical Research and Occupational Health is acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11356_2019_4507_MOESM1_ESM.docx (27 kb)
ESM 1 (DOCX 26 kb)


  1. Anonymous (2012) Izvješće o stanju okoliša u Splitsko–dalmatinskoj županiji za razdoblje od 2008. do 2011. godine. Splitsko – dalmatinska županija, Upravni odjel za graditeljstvo, komunalne poslove, infrastrukturu i zaštitu okoliša, Split, p 398 [in Croatian]Google Scholar
  2. Assenova B, Okuskhanova E, Rebezov M, Korzhikenova N, Yessimbekov Z, Dragoev S (2016) Trace and toxic elements in meat of maral (red deer) grazing in Kazakhstan. Res J Pharm, Biol Chem Sci 7(1):1425–1433Google Scholar
  3. Bąkowska M, Pilarczyk B, Tomza-Marciniak A, Udała J, Pilarczyk R (2016) The bioaccumulation of lead in the organs of roe deer (Capreolus capreolus L.), red deer (Cervus elaphus L.), and wild boar (Sus scrofa L.) from Poland. Environ Sci Pollut Res Int 23(14):14373–14382CrossRefGoogle Scholar
  4. Bartoš L, Kotrba R, Pintíř J (2010) Ungulate and their management in the Czech Republic. In: Apollonio M, Andersen R, Putman R (eds) European ungulates and their management in the 21st century. Cambridge University Press, Cambridge, pp 243–261Google Scholar
  5. Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC, Mateo R, Rodríguez Fariñas N, Rodríguez-Estival J, Patiño Ropero MJ (2012) Mercury exposure and mechanism of response in large game using the Almadén mercury mining area (Spain) as a case study. Environ Res 112:58–66CrossRefGoogle Scholar
  6. Bilandžić N, Đokić M, Sedak M (2010) Survey of arsenic, cadmium, copper, mercury and lead in kidney of cattle, horse, sheep and pigs from rural areas in Croatia. Food Addit Contam Part B Surveill 3(3):172–177CrossRefGoogle Scholar
  7. Bilandžić N, Sedak M, Đokić M, Varenina I, Solomun-Kolanović B, Božić Đ, Brstilo M, Sokolić-Mihalak D, Jurković Z (2013) Comparative study of iron, magnesium and zinc and daily intakes in certain meats and meat products. Slov Vet Res 50(3):103–110Google Scholar
  8. Bilandžić N, Sedak M, Đokić M, Solomun-Kolanović B, Božić Đ, Brstilo M, Šimić B (2014) Determination of zinc concentrations in foods of animal origin, fish and shellfish from Croatia and assessment of their contribution to dietary intake. J Food Compos Anal 35(2):61–66CrossRefGoogle Scholar
  9. Bjorå R, Falch JA, Staaland H, Nordsletten L, Gjengedal E (2001) Osteoporosis in the Norwegian moose. Bone 29(1):70–73CrossRefGoogle Scholar
  10. Carpio A, Guerrero-Casado J, Barasona J, Tortosa F, Vicente J, Hillström L, Delibes-Mateos M (2017) Hunting as a source of alien species: a European review. Biol Invasions 19:1197–1211CrossRefGoogle Scholar
  11. Cassinelo J (1998) Ammotragus lervia: a review on systematics, biology, ecology and distribution. Ann Zool Fenn 35:149–162Google Scholar
  12. Cassinello J (2012) The Mediterranean’s mosaic landscape and its survival: from pastoralism to the role of exotic species. Lychnos 9:48–55Google Scholar
  13. Cassinello J (2018) Misconception and mismanagement of invasive species: the paradoxical case of an alien ungulate in Spain. Conserv Lett 11:e12440CrossRefGoogle Scholar
  14. Cassinello J, Cuzin F, Jdeidi T, Masseti M, Nader I, De Smet K (2008) Ammotragus lervia. The IUCN Red List of threatened species 2008: e.T1151A3288917., Accessed 5 April 2018
  15. Census (2012) Census of population, households and dwellings 2011. Croatian Bureau of Statistics, Zagreb, Accessed 20 March 2018Google Scholar
  16. Chiari M, Cortinovis C, Bertoletti M, Alborali L, Zanoni M, Ferretti E, Caloni F (2015) Lead, cadmium and organochlorine pesticide residues in hunted red deer and wild boar from northern Italy. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32(11):1867–1874CrossRefGoogle Scholar
  17. Dannenberger D, Nuernberg G, Nuernberg K, Hagemann E (2013) The effects of gender, age and region on macro- and micronutrient contents and fatty acid profiles in the muscles of roe deer and wild boar in Mecklenburg-Western Pomerania (Germany). Meat Sci 94(1):39–46CrossRefGoogle Scholar
  18. Davis GK, Mertz W (1986) Copper. In: Mertz W (ed) Trace elements in human and animal nutrition, vol 1, 5th edn. Academic, Orlando, pp 301–364Google Scholar
  19. Długaszek M, Kopczyński K (2013) Elemental composition of muscle tissue of wild animals from central region of Poland. Int J Environ Res 7(4):973–978Google Scholar
  20. Durkalec M, Nawrocka A, Krzysiak M, Larska M, Kmiecik M, Posyniak A (2018) Trace elements in the liver of captive and free-ranging European bison (Bison bonasus L.). Chemosphere 193:454–463CrossRefGoogle Scholar
  21. EC (2006) Commission Regulation (EC) No. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union 364:5–24Google Scholar
  22. EFSA (2010) Scientific opinion on lead in food. European Food Safety Authority (EFSA) Panel on Contaminants in the Food Chain (CONTAM). EFSA J 8(4):1570CrossRefGoogle Scholar
  23. EFSA (2011) Statement on tolerable weekly intake for cadmium. European Food Safety Authority (EFSA) Panel on Contaminants in the Food Chain (CONTAM). EFSA J 9(2):1975Google Scholar
  24. EFSA (2012) Scientific opinion on the risk for public health related to the presence of mercury and methylmercury in food. European Food Safety Authority (EFSA) Panel on Contaminants in the Food Chain (CONTAM). EFSA J 10(12):2985Google Scholar
  25. EFSA (2014) Dietary exposure to inorganic arsenic in the European population. European Food Safety Authority (EFSA). EFSA J 12(3):3597Google Scholar
  26. EFSA (2017) Dietary reference values for nutrients. Summary report. European Food Safety Authority (EFSA) supporting publication 2017:e15121, pp. 92Google Scholar
  27. Ertl K, Kitzer R, Goessler W (2016) Elemental composition of game meat from Austria. Food Addit Contam Part B Surveill 9(2):120–126CrossRefGoogle Scholar
  28. Ferri M, Baldi L, Cavallo S, Pellicanò R, Brambilla G (2017) Wild game consumption habits among Italian shooters: relevance for intakes of cadmium, perfluorooctanesulphonic acid, and 137cesium as priority contaminants. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 34(5):832–841Google Scholar
  29. Flueck WT, Smith-Flueck JM, Mionczynski J, Mincher BJ (2012) The implications of selenium deficiency for wild herbivore conservation, a review. Eur J Wildl Res 58(5):761–780CrossRefGoogle Scholar
  30. Forte G, Bocca B (2007) Quantification of cadmium and lead in offal by SF-ICP-MS: method development and uncertainty estimate. Food Chem 105(4):1591–1598CrossRefGoogle Scholar
  31. Frank A (2004) A review of the “mysterious” wasting disease in Swedish moose (Alces alces L.) related to molybdenosis and disturbances in copper metabolism. Biol Trace Elem Res 102(1–3):143–159CrossRefGoogle Scholar
  32. French AS, Shaw D, Gibb SW, Taggart MA (2017) Geochemical landscapes as drivers of trace and toxic element profiles in wild red deer (Cervus elaphus). Sci Total Environ 601–602:1606–1618CrossRefGoogle Scholar
  33. Gančević P, Šprem N, Jerina K (2016) Space use and activity patterns of introduced Barbary sheep (Ammotragus lervia) in southern Dinarides, Croatia. In: Hadjisterkotis, E. (Ed.), Abstract book of 6th world congress on mountain ungulates and 5th international symposium on mouflon, Nicosia, Cyprus, pp. 41Google Scholar
  34. Goretti E, Pallottini M, Cenci Goga BT, Selvaggi R, Petroselli C, Vercillo F, Cappelletti D (2018) Mustelids as bioindicators of the environmental contamination by heavy metals. Ecol Indic 94(1):320–327CrossRefGoogle Scholar
  35. Gray GG (1980) Aspects of Barbary sheep (Ammotragus lervia): biology in Palo Duro Canyon, Texas [Ph.D. thesis]. Texas Tech University, Lubbock, pp. 175Google Scholar
  36. Halamić J, Miko S (2009) Geochemical atlas of the Republic of Croatia. Croatian Geological Survey, Zagreb, p 87 [in Croatian]Google Scholar
  37. Hermoso de Mendoza García M, Hernández Moreno D, Soler Rodríguez F, López Beceiro A, Fidalgo Alvarez LE, Pérez López M (2011) Sex- and age-dependent accumulation of heavy metals (Cd, Pb and Zn) in liver, kidney and muscle of roe deer (Capreolus capreolus) from NW Spain. J Environ Sci Health A Tox Hazard Subst Environ Eng 46(2):109–116CrossRefGoogle Scholar
  38. IAEA (1996) International Atomic Energy Agency safety standards series. Safety series no. 115. IAEA, ViennaGoogle Scholar
  39. Jarzyńska G, Falandysz J (2011) Selenium and 17 other largely essential and toxic metals in muscle and organ meats of red deer (Cervus elaphus)—consequences to human health. Environ Int 37(5):882–888CrossRefGoogle Scholar
  40. Klansek E, Vavra I, Onderscheka K (1995) Die Äsungszusammensetzung des Alpensteinwildes (Capra i. ibex L.) in Abhängigkeit von Jahreszeit, Alter und Äsungsangebot in Graubünden. Z Jagdwiss 41:171–181Google Scholar
  41. Kośla T, Skibniewski M, Skibniewska E, Urbańska-Słomka G (2013) The iron content in organs of free ranging European bison from the Białowieża herd. Ann Anim Sci 13(2):357–364CrossRefGoogle Scholar
  42. Kramárová M, Massányi P, Slamecka J, Tataruch F, Jancová A, Gasparik J, Fabis M, Kovacik J, Toman R, Galová J, Jurcik R (2005) Concentration of cadmium in liver and kidneys of some wild and farm animals. Bull Vet Inst Pulawy 49(4):465–469Google Scholar
  43. Krysl LJ, Simpson CD, Gray GG (1980) Dietary overlap of sympatric Barbary sheep and mule deer in Palo Duro Canyon, Texas. In: Simpson CD (ed) Proceedings of the symposium on ecology and management of Barbary sheep. Texas Tech University Press, LubbockGoogle Scholar
  44. Kudrnáčová E, Bartoň L, Bureš D, Hoffman LC (2018) Carcass and meat characteristics from farm-raised and wild fallow deer (Dama dama) and red deer (Cervus elaphus): a review. Meat Sci 141:9–27CrossRefGoogle Scholar
  45. Larter NC, Macdonald CR, Elkin BT, Wang X, Harms NJ, Gamberg M, Muir DC (2016) Cadmium and other elements in tissues from four ungulate species from the Mackenzie Mountain region of the Northwest Territories, Canada. Ecotoxicol Environ Saf 132:9–17CrossRefGoogle Scholar
  46. Lazarus M, Orct T, Blanuša M, Vicković I, Šoštarić B (2008) Toxic and essential metal concentrations in four tissues of red deer (Cervus elaphus) from Baranja, Croatia. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25(3):270–283CrossRefGoogle Scholar
  47. Lazarus M, Prevendar Crnić A, Bilandžić N, Kusak J, Reljić S (2014) Cadmium, lead, and mercury exposure assessment among Croatian consumers of free-living game. Arh Hig Rada Toksikol 65:281–292CrossRefGoogle Scholar
  48. Lehel J, Zwillinger D, Bartha A, Lányi K, Laczay P (2017) Food safety aspects of primary environmental contaminants in the edible tissues of roe deer (Capreolus capreolus). Environ Sci Pollut Res Int 24(32):25372–25382CrossRefGoogle Scholar
  49. Ma WC (1996) Lead in mammals. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue residues. CRC Press Inc, Boca Raton, pp 281–296Google Scholar
  50. Mimoun JB, Nouira S (2015) Food habits of the aoudad Ammotragus lervia in the Bou Hedma mountains, Tunisia. S Afr J Sci 111:11–12Google Scholar
  51. Miranda M, Sicilia M, Bartolomé J, Molina-Alcaide E, Gálvez-Bravo L, Cassinello J (2012) Contrasting feeding patterns of native red deer and two exotic ungulates in a Mediterranean ecosystem. Wildl Res 39:171–182CrossRefGoogle Scholar
  52. Mori E, Mazza G, Saggiomo L, Sommese A, Esattore B (2017) Strangers coming from the Sahara: an update of the worldwide distribution, potential impacts and conservation opportunities of alien aoudad. Ann Zool Fenn 54(5–6):373–386CrossRefGoogle Scholar
  53. Nordberg GF, Nogawa K, Nordberg M (2015) 32. Cadmium. In: Nordberg GF, Fowler BA, Nordberg M (eds) Handbook on the toxicology of metals, vol 2, 4th edn. Academic, Amsterdam, pp 667–716CrossRefGoogle Scholar
  54. Patiño Ropero MJ, Rodríguez Fariñas N, Mateo R, Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC (2016) Mercury species accumulation and trophic transfer in biological systems using the Almadén mining district (Ciudad Real, Spain) as a case of study. Environ Sci Pollut Res Int 23(7):6074–6081CrossRefGoogle Scholar
  55. Pourcelot L, Renaud P, Louvat D, Gurriaran R, Richon P (2003) Influence of hot spots on cesium-137 contamination of an alpine food chain and doses associated with it. Environ Risque Santé 2:112–120Google Scholar
  56. Puls R (1994) Mineral levels in animal health. Diagnostic data. Sherpa International, ClearbrookGoogle Scholar
  57. Ramanzin M, Amici A, Casoli C, Esposito L, Lupi P, Marsico G, Mattiello S, Olivieri O, Ponzetta MP, Russo C, Trabalza M (2010) Meat from wild ungulates: ensuring quality and hygiene of an increasing resource. Ital J Anim Sci 9(3):318–331Google Scholar
  58. Redžić S (2011) Phytogeographic and syntaxonomic diversity of high mountain vegetation in Dinaric Alps (Western Balkan, SE Europe). J Mt Sci 8:767–786CrossRefGoogle Scholar
  59. Reglero MM, Taggart MA, Monsalve-González L, Mateo R (2009) Heavy metal exposure in large game from a lead mining area: effects on oxidative stress and fatty acid composition in liver. Environ Pollut 157(4):1388–1395CrossRefGoogle Scholar
  60. Rodríguez Piñero JC, Rodríguez Luengo JL (1992) Autumn food habits of the Barbary sheep (Ammotragus lervia Pallas, 1772) on La Palma Island (Canary Islands). Mammalia 56:385–392CrossRefGoogle Scholar
  61. Scheuhammer AM (1991) Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ Pollut 71(2–4):329–375CrossRefGoogle Scholar
  62. Skibniewski M, Skibniewska EM, Kośla T, Olbrych K (2016) The content of copper and molybdenum in the liver, kidneys, and skeletal muscles of elk (Alces alces) from North-Eastern Poland. Biol Trace Elem Res 169:204–210CrossRefGoogle Scholar
  63. Skibniewski M, Skibniewska EM, Kośla T, Olbrych K (2017) Relationship between Cd and Zn concentration in the kidneys, liver, and muscles of moose (Alces alces) from North-Eastern Poland. Environ Sci Pollut Res Int 24(1):598–604CrossRefGoogle Scholar
  64. Šoštarić M (2017) Radiological properties of soil in the Republic of Croatia, [Ph.D. thesis]. Faculty of Science, University of Zagreb, Zagreb. [in Croatian]Google Scholar
  65. Šprem N, Babić I, Barišić D, Barišić D (2013) Concentration of 137Cs and 40K in meat of omnivore and herbivore game species in mountain forest ecosystems of Gorski Kotar, Croatia. J Radioanal Nucl Chem 298:513–517CrossRefGoogle Scholar
  66. Šprem N, Piria M, Barišić D, Kusak J, Barišić D (2016) Dietary items as possible sources of 137Cs in large carnivores in the Gorski Kotar forest ecosystem, Western Croatia. Sci Total Environ 542A:826–832Google Scholar
  67. Thijs S, Langill T, Vangronsveld J (2017) The bacterial and fungal microbiota of hyperaccumulator plants: small organisms, large influence. Adv Bot Res 83:43–86CrossRefGoogle Scholar
  68. Thompson DR (1996) Mercury in birds and terrestrial mammals. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue residues. CRC Press Inc, Boca Raton, pp 341–356Google Scholar
  69. Tsuji LJ, Wainman BC, Jayasinghe RK, VanSpronsen EP, Liberda EN (2009) Determining tissue-lead levels in large game mammals harvested with lead bullets: human health concerns. Bull Environ Contam Toxicol 82(4):435–439CrossRefGoogle Scholar
  70. Vihnanek Lazarus M, Sekovanić A, Kljaković-Gašpić Z, Orct T, Jurasović J, Kusak J, Reljić S, Huber Đ (2013) Cadmium and lead in grey wolf liver samples: optimization of a microwave-assisted digestion method. Arh Hig Rada Toksikol 64:395–403CrossRefGoogle Scholar
  71. Vladović D, Ilijanić LJ (1992) A contribution to the flora of Mosor Mountain (Croatia). Acta Bot Croat 51:143–150 [in Croatian with English abstract]Google Scholar
  72. Vukšić N, Šperanda M, Lončarić Z, Đidara M, Ludek E, Budor I (2018) The effect of dietary selenium addition on the concentrations of heavy metals in the tissues of fallow deer (Dama dama L.) in Croatia. Environ Sci Pollut Res Int 25(11):11023–11033CrossRefGoogle Scholar
  73. Wieczorek-Dąbrowska M, Tomza-Marciniak A, Pilarczyk B, Balicka-Ramisz A (2013) Roe and red deer as bioindicators of heavy metals contamination in North-Western Poland. Chem Ecol 29(2):100–110CrossRefGoogle Scholar
  74. Wilson PR, Grace ND (2001) A review of tissue reference values used to assess the trace element status of farmed red deer (Cervus elaphus). N Z Vet J 49(4):126–132CrossRefGoogle Scholar
  75. Zacs D, Rjabova J, Ikkere LE, Bavrins K, Bartkevics V (2018) Brominated flame retardants and toxic elements in the meat and liver of red deer (Cervus elaphus), wild boar (Sus scrofa), and moose (Alces alces) from Latvian wildlife. Sci Total Environ 621:308–316CrossRefGoogle Scholar
  76. Zaninović K, Gajić-Čapka M, Perčec Tadić M, Vučetić M, Milković J, Bajić A, Cindrić K, Cvitan L, Katušin Z, Kaučić D, Likso T, Lončar E, Lončar Ž, Mihajlović D, Pandžić K, Patarčić M, Smec L, Vučetić V (2008) Klimatski atlas Hrvatske / Climate atlas of Croatia 1961–1990, 1971–2000. Državni hidrometeorološki zavod, Zagreb [in Croatian]Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Maja Lazarus
    • 1
  • Pavao Gančević
    • 2
  • Tatjana Orct
    • 1
  • Delko Barišić
    • 3
  • Klemen Jerina
    • 4
  • Nikica Šprem
    • 2
    Email author
  1. 1.Analytical Toxicology and Mineral Metabolism UnitInstitute for Medical Research and Occupational HealthZagrebCroatia
  2. 2.Department of Fisheries, Beekeeping, Game Management and Special Zoology, Faculty of AgricultureUniversity of ZagrebZagrebCroatia
  3. 3.Laboratory for Radioecology, Centre for Marine and Environmental ResearchRuđer Bošković InstituteZagrebCroatia
  4. 4.Department of Forestry, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia

Personalised recommendations