Biological Trace Element Research

, Volume 185, Issue 1, pp 98–105 | Cite as

Serum Concentration of Macro-, Micro-, and Trace Elements in Silver Fox (Vulpes vulpes) and Their Interrelationships with Morphometric, Densitometric, and Mechanical Properties of the Mandible

  • Marcin R. TataraEmail author
  • Iwona Łuszczewska-Sierakowska
  • Witold Krupski


The optimal content of macro-, micro-, and trace elements in tissues ensures proper systemic growth and development and optimal health status in animals and humans. However, very little is known on the elemental content in the plasma compartment in Silver fox. The aim of this study was to determine the content of selected elements in serum obtained from 8-month-old female (N = 8) and male (N = 7) silver foxes. Moreover, relationships of the evaluated elements with the morphological, densitometric, and mechanical parameters of the mandible were determined. Serum content of 12 different elements was measured using inductively coupled plasma-atomic emission spectrometry. The morphometric and densitometric properties of the mandible were determined using quantitative computed tomography method, while mechanical endurance was tested using a three-point bending test. Serum concentration of calcium was significantly higher by 20% in male foxes (P = 0.01), while manganese concentration was significantly lower in males by over 17% (P = 0.03). Positive correlations of serum concentration of calcium, phosphorus, and magnesium with the morphological traits of the mandible such as weight, length, and bone volume were stated (P < 0.05). In the group of elements playing regulatory functions, the positive relationships between serum concentrations of selenium, chromium, manganese, copper, and cobalt were found (P < 0.05). The elaborated experimental model may serve for further studies on foxes, especially focused on nutritional factors affecting elemental homeostasis, whole-body metabolism, and systemic growth and development. Daily diet formulation and precise delivery for farm foxes, together with relatively large animal population maintained at the same environmental conditions, regularly subjected to slaughter procedure, enable economical experimentation with various dietary and pharmacological manipulations.


Dual-energy X-ray absorptiometry (DEXA) Macroelements Mandible Microelements Quantitative computed tomography (QCT) Silver fox (Vulpes vulpes


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable international, national and institutional guidelines for the care and use of animals were followed. The study protocol was approved by the Local Ethics Committee on Animal Experimentation of the University of Life Sciences in Lublin, Poland—permission number 20/2015.


  1. 1.
    Studziński T, Matras J, Grela ER, Valverde Pietra JL, Truchliński J, Tatara MR (2006) Minerals: functions, requirements, excessive intake and toxicity. In: Mosenthin R, Zentec J, Żebrowska T (eds) Biology of growing animals, 1st edn. Elsevier, New York, pp 467–509. CrossRefGoogle Scholar
  2. 2.
    Fantuz F, Ferraro S, Todini L, Mariani P, Piloni R, Salimei E (2013) Essential trace elements in milk and blood serum of lactating donkeys as affected by lactation stage and dietary supplementation with trace elements. Animal 7(11):1893–1899. CrossRefPubMedGoogle Scholar
  3. 3.
    Pereira PC (2014) Milk nutritional composition and its role in human health. Nutrition 30(6):619–627. CrossRefPubMedGoogle Scholar
  4. 4.
    Prado EL, Dewey KG (2014) Nutrition and brain development in early life. Nutr Rev 72(4):267–284. CrossRefPubMedGoogle Scholar
  5. 5.
    Sobczak M, Jabłoński E (2007) Mineral elements in diet of pregnant and breast-feeding women. Part I. Macro minerals: calcium, magnesium, phosphorus, sodium, potassium, chloride. Przegl Lek 64(3):165–169PubMedGoogle Scholar
  6. 6.
    Sobczak M, Jabłoński E (2007) Mineral elements in diet of pregnant and breast-feeding women. Part II. Micro minerals: iron, zinc, copper, selenium, iodine, fluorine, manganese, molybdenium, chromium. Przegl Lek 64:170–174PubMedGoogle Scholar
  7. 7.
    Paolisso G, Barbagallo M (1997) Hypertension, diabetes mellitus, and insulin resistance: the role of intracellular magnesium. Am J Hypertens 10(3):346–355. CrossRefPubMedGoogle Scholar
  8. 8.
    Williams RJ (1998) Calcium: outside/inside homeostasis and signalling. Biochim Biophys Acta 1448(2):153–165. CrossRefPubMedGoogle Scholar
  9. 9.
    Bennett MR (1999) The concept of a calcium sensor in transmitter release. Prog Neurobiol 59(3):243–277. CrossRefPubMedGoogle Scholar
  10. 10.
    Laroche M (2001) Phosphate, the renal tubule, and the musculoskeletal system. Joint Bone Spine 68(3):211–215. CrossRefPubMedGoogle Scholar
  11. 11.
    Burjonrappa SC, Miller M (2012) Role of trace elements in parenteral nutrition support of the surgical neonate. J Pediatr Surg 47(4):760–771. CrossRefPubMedGoogle Scholar
  12. 12.
    Tatara MR (2016) Physiological function of magnesium in maintenance of optimal health status in animals. In: Maj-Żurawska M, Pyrzyńska T (eds) Magnesium. Element of life, 1st edn. Wydawnictwo MALAMUT, Warsaw, pp 229–248Google Scholar
  13. 13.
    Lieu PT, Heiskala M, Peterson PA, Yang Y (2001) The roles of iron in health and disease. Mol Asp Med 22(1-2):1–87. CrossRefGoogle Scholar
  14. 14.
    Aschner JL, Aschner M (2005) Nutritional aspects of manganese homeostasis. Mol Asp Med 26(4-5):353–362. CrossRefGoogle Scholar
  15. 15.
    Jeejeebhoy KN, Chu RC, Marliss EB, Greenberg GR, Bruce-Robertson A (1977) Chromium deficiency, glucose intolerance, and neuropathy reversed by chromium supplementation, in a patient receiving long-term total parenteral nutrition. Am J Clin Nutr 30(4):531–538CrossRefPubMedGoogle Scholar
  16. 16.
    Abraham AS, Brooks BA, Eylath U (1992) The effects of chromium supplementation on serum glucose and lipids in patients with and without non-insulin-dependent diabetes. Metabolism 41(7):768–771. CrossRefPubMedGoogle Scholar
  17. 17.
    Tomza-Marciniak A, Pilarczyk B, Bakowska M, Ligocki M, Gaik M (2012) Lead, cadmium and other metals in serum of pet dogs from an urban area of NW Poland. Biol Trace Elem Res 149(3):345–351. CrossRefPubMedGoogle Scholar
  18. 18.
    Tymczyna B, Tatara MR, Krupski W, Tymczyna-Sobotka M, Łuszczewska-Sierakowska I, Bachanek T (2012) Relationships between biochemical bone metabolism indices and morphometric, densitometric and mechanical properties of mandible in 6-month-old pigs. Ann Agric Environ Med 19(3):535–539PubMedGoogle Scholar
  19. 19.
    Szabelska A, Tatara MR, Krupski W (2017) Morphological, densitometric and mechanical properties of mandible in 5-month-old Polish Merino sheep. BMC Vet Res 13(1):12. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Szabelska A, Tatara MR, Krupski W (2017) Interrelationships between bone metabolism markers and deciduous teeth and mandible properties in Polish Merino sheep. J Hard Tissue Biol 26(3):249–256. CrossRefGoogle Scholar
  21. 21.
    Piotrowska A, Szymeczko R, Ozgo M, Bogusławska-Tryk M, Burlikowska K (2008) Morphological and mineral characteristics of peripheral blood in female polar fox in relation to age. Folia Biol (Kraków) 56(3):263–267. CrossRefGoogle Scholar
  22. 22.
    Benn DM, McKeown DB, Lumsden JH (1986) Hematology and biochemistry reference values for the ranch fox. Can J Vet Res 50(1):54–58PubMedPubMedCentralGoogle Scholar
  23. 23.
    Mainka SA (1988) Hematology and serum biochemistry of captive swift foxes (Vulpes velox). J Wildl Dis 24(1):71–74. CrossRefPubMedGoogle Scholar
  24. 24.
    Rubio AV, Hidalgo-Hermoso E, Bonacic C (2014) Hematology and serum biochemistry values of Culpeo foxes (Lycalopex culpaeus) from central Chile. J Zoo Wildl Med 45(3):589–593. CrossRefPubMedGoogle Scholar
  25. 25.
    Winnicka A (2004) Reference values of the basic laboratory examinations in veterinary medicine. Wydawnictwo SGGW, WarsawGoogle Scholar
  26. 26.
    Cybulski W, Jarosz L, Chałabis-Mazurek A, Jakubczak A, Kostro K, Kursa K (2009) Contents of zinc, copper, chromium and manganese in silver foxes according to their age and mineral supplementation. Pol J Vet Sci 12(3):339–345PubMedGoogle Scholar
  27. 27.
    Gudmundsson TV, Woodhouse NJ (1971) Regulation of plasma calcium in man: the influence of parathyroid hormone and calcitonin. Hormones 2(1):26–39PubMedGoogle Scholar
  28. 28.
    Wendelaar Bonga SE, Pang PK (1991) Control of calcium regulating hormones in the vertebrates: parathyroid hormone, calcitonin, prolactin, and stanniocalcin. Int Rev Cytol 128:139–213. CrossRefPubMedGoogle Scholar
  29. 29.
    Underwood EJ, Suttle NF (1999) Manganese. In: Underwood EJ, Suttle NF (eds) The mineral nutrition of livestock, 3rd edn. CABI Publishing, Oxon, pp 397–420. CrossRefGoogle Scholar
  30. 30.
    Hodgkinson A, Marshall DH, Nordin BE (1979) Vitamin D and magnesium absorption in man. Clin Sci 57(1):121–123. CrossRefPubMedGoogle Scholar
  31. 31.
    Krejs GJ, Nicar MJ, Zerwekh JE, Norman DA, Kane MG, Pak CY (1983) Effect of 1,25-dihydroxyvitamin D3 on calcium and magnesium absorption in the healthy human jejunum and ileum. Am J Med 75(6):973–976. CrossRefPubMedGoogle Scholar
  32. 32.
    Hardwick LL, Jones MR, Brautbar N, Lee DB (1991) Magnesium absorption: mechanisms and the influence of vitamin D, calcium and phosphate. J Nutr 121(1):13–23CrossRefPubMedGoogle Scholar
  33. 33.
    Razzaque MS (2009) The FGF23-Klotho axis: endocrine regulation of phosphate homeostasis. Nat Rev Endocrinol 5(11):611–619. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Fleet JC (2017) The role of vitamin D in the endocrinology controlling calcium homeostasis. Mol Cell Endocrinol 453:36–45. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Barceloux DG (1999) Cobalt. J Toxicol Clin Toxicol 37(2):201–206. CrossRefPubMedGoogle Scholar
  36. 36.
    Goullé JP, Mahieu L, Castermant J, Neveu N, Bonneau L, Lainé G, Bouige D, Lacroix C (2005) Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair. Reference values. Forensic Sci Int 153(1):39–44. CrossRefPubMedGoogle Scholar
  37. 37.
    Binkowski ŁJ, Merta D, Przystupińska A, Sołtysiak Z, Pacoń J, Stawarz R (2016) Levels of metals in kidney, liver and muscle tissue and their relation to the occurrence of parasites in the red fox in the Lower Silesian Forest in Europe. Chemosphere 149:161–167. CrossRefPubMedGoogle Scholar
  38. 38.
    Lanocha N, Kalisinska E, Kosik-Bogacka DI, Budis H, Noga-Deren K (2012) Trace metals and micronutrients in bone tissues of the red fox Vulpes vulpes (L., 1758). Acta Theriol 57(3):233–244. CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Budis H, Kalisinska E, Lanocha N, Kosik-Bogacka DI (2013) The concentration of manganese, iron and strontium in bone of red fox Vulpes vulpes (L. 1758). Biol Trace Elem Res 155(3):361–369. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Prestrud P, Norheim G, Sivertsen T, Daae HL (1994) Levels of toxic and essential elements in arctic fox in Svalbard. Polar Biol 14:155–159CrossRefGoogle Scholar
  41. 41.
    Hoekstra PF, Braune BM, Elkin B, Armstrong FA, Muir DC (2003) Concentrations of selected essential and non-essential elements in arctic fox (Alopex lagopus) and wolverines (Gulo gulo) from the Canadian Arctic. Sci Total Environ 309(1-3):81–92. CrossRefPubMedGoogle Scholar
  42. 42.
    Massányi P, Trandzik J, Nad P, Skalická M, Koréneková B, Lukac N, Fabis M, Toman R (2005) Seminal concentration of trace elements in fox and relationships to spermatozoa quality. J Environ Sci Health A Tox Hazard Subst Environ Eng 40(5):1097–1105. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Marcin R. Tatara
    • 1
    • 2
    Email author
  • Iwona Łuszczewska-Sierakowska
    • 3
  • Witold Krupski
    • 2
  1. 1.Department of Animal PhysiologyUniversity of Life Sciences in LublinLublinPoland
  2. 2.II Department of RadiologyMedical University in LublinLublinPoland
  3. 3.Department of Normal AnatomyMedical University in LublinLublinPoland

Personalised recommendations