Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bioaccumulation of Trace and Non-trace Elements in Blood and Fibers of Alpacas (Vicugna pacos) that Graze in Italian Pastures

  • 151 Accesses


The concentrations of trace and non-trace elements were determined in blood and fibers of alpacas (Vicugna pacos) from a north Italian area, as well as in their pasture forages. This is the first investigation regarding this species in Italy, and the first considering alpaca’s fiber as bioindicator worldwide. Metal contents in blood were in the decreasing order: copper > zinc > aluminum > selenium > lead > nickel > manganese > chromium > arsenic and cadmium, while in fiber, metal levels were in the following order: aluminum > zinc > copper > manganese > chromium > nickel > selenium > lead > arsenic and cadmium. Antimony, beryllium, mercury, tin, and thallium were below the limit of quantification (0.010 mg kg−1). The analysis of the alpacas’ forage confirmed the same trend found in fiber, suggesting that metal bioaccumulation was affected by diet. These preliminary results have shown that all the trace elements studied bioaccumulated to a greater extent in the fibers of the alpaca than in the blood. Accordingly, we may suggest that alpaca fibers could be used for monitoring exposure especially to non-essential metals like aluminum, cadmium, and lead, and could constitute a suitable non-invasive method for measuring trace and non-trace element exposure in camelids.

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

Fig. 1
Fig. 2


  1. Agency for Toxic Substances and Disease Registry (ATSDR). (2008). Toxicological Profile for Aluminum. U.S. Public Health Service. Atlanta: Agency for Toxic Substances and Disease Registry.

  2. Barton, C. C., & Schmitz, S. C. (2009). Environmental toxicology: wildlife. In P. Wexler (Ed.), Information resources in toxicology (pp. 251–254). New York: Academic Press.

  3. Bates, D. M., Mächler, M., & Bolker, B. M., Walker, S. C.. (2014) lme4: linear mixed-effects models using eigen and S4 R package. Version 11–7. Available: http://CRANR-projectorg/package=lme4

  4. Beernaert, J., Scheirs, J., Leirs, H., Blust, R., & Verhagen, R. (2007). Nondestructive pollution exposure assessment by means of wood mice hair. Environmental Pollution, 145(2), 443–451.

  5. Budtz-Jorgensen, E., Grandjean, P., Jorgensen, P. J., Weihe, P., & Keiding, N. (2004). Association between mercury concentrations in blood and hair in methylmercury-exposed subjects at different ages. Environmental Research, 95, 385–393.

  6. Burger, J., Gochfeld, M., Sullivan, K., Irons, D., & McKnight, A. (2008). Arsenic, cadmium, chromium, lead, manganese, mercury, and selenium in feathers of black-legged kittiwake (Rissa tridactyla) and black oystercatcher (Haematopus bachmani) from Prince William Sound, Alaska. The Science of the Total Environment, 398, 20–25.

  7. Burger, J., & Gochfeld, M. (2000). Effects of lead on birds (Laridae): a review of laboratory and field studies. Journal of Toxicology & Environmental Health Part B: Critical Reviews, 3, 59–78.

  8. Burger, J., Marquez, M., & Gochfeld, M. (1994). Heavy metals in hair of opossum from Palo Verde, Costa Rica. Archives of Environmental Contamination and Toxicology, 27, 472–476.

  9. Carmalt, J. L., Baptiste, K. E., & Blakley, B. (2001). Suspect copper toxicity in an alpaca. The Canadian Veterinary Journal, 42, 554–556.

  10. Caroli, S., Alimonti, A., Coni, E., Petrucci, F., Senofonte, O., Violante, N. (1994). The assessment of reference values for elements in human biological tissues, fluids: A systematic review. Critical Reviews in Analytical Chemistry, 24, 363–398.

  11. Clauss, M., Lendl, C., Schramel, P., & Streich, W. J. (2004). Skin lesions in alpacas and llamas with low zinc and copper status—a preliminary report. Veterinary Journal, 167(3), 302–305.

  12. Das, K. K., Das, S., & Dhundasi, S. (2008). Nickel, its adverse health effects & oxidative stress. The Indian Journal of Medical Research, 128, 412–425.

  13. de Almeida Curi, N. H., Hoff Brait, C. H., Filho, N. H. A., & Talamoni, S. A. (2012). Heavy metals in hair of wild canids from the Brazilian Cerrado. Biological Trace Element Research, 147, 97–102.

  14. Degeratu, C. N., Mabilleau, G., Cincu, C., & Chappard, D. (2005). Aluminum inhibits the growth of hydroxy apatite crystals developed on a biomimetic methacrylic polymer. Journal of Trace Elements in Medicine and Biology: Organ of the Society for Minerals and Trace Elements (GMS), 27, 346–351.

  15. D’Have, H., Scheirs, J., Kayawe Mubiana, V., Verhagen, R., Blust, R., & De Coen, W. (2006). Nondestructive pollution exposure assessment in the European hedgehog (Erinaceus europaeus): II: Hair and spines as indicators of endogenous metal and As concentrations. Environmental Pollution, 142, 438–448.

  16. Dunnet, M., & Lees, P. (2003). Trace element, toxin and drug elimination in hair with particular reference to the horse. Research in Veterinary Science, 75, 89–101.

  17. EFSA (2009) Cadmium in food. Scientific opinion of the Panel on Contaminants in the Food Chain. The EFSA J 980: 1–139 Available online: www.efsa.europa.eu.

  18. Eisler, R. (1985) Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 2; (1.2) 30 pp.

  19. Eisler, R. (1988) Nickel hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 34, 1998 (1.2) 30 pp.

  20. Erry, B. V., Macnair, M. R., Meharg, A. A., & Shore, R. F. (2005). The distribution of arsenic in the body tissues of wood mice and bank voles. Archives of Environmental Contamination and Toxicology, 49(4), 569–576.

  21. Faye, B., Seboussi, R., Askar, M. (2008) Trace elements and heavy metals status in Arabian camel. In: Impact of pollution on animal products, part of the series NATO Science for Peace and Security Series C: Environmental Security, Springer, pp 97–106.

  22. Herdt, T. H., & Hoff, B. (2011) The Use of Blood Analysis to Evaluate Trace Mineral Status in Ruminant Livestock. Veterinary Clinics of North America: Food Animal Practice, 27 (2), 255–283.

  23. Judson, G. J., McGregor, B. A., & Howse, A. M. (2000). Trace elements and vitamins in blood of alpacas (Lama pacos) and sheep grazing the same pasture. In A. M. Roussel, R. A. Anderson, & A. E. Favrier (Eds.), Trace elements in man and animals 10 (pp. 737–740). New York: Kluwer Academic/Plenum Publishers.

  24. Kosla, T., Skibniewska, E. M., & Skibniewski, M. (2004). Contamination with aluminum of cats free living in Warsaw agglomeration and its effect on hematologic and biochemical indexes of blood as compared to cats kept in flats. Macro and Trace elements. Jena: Friedrich-Schiller-University, 22, 280–285.

  25. Kosla, T., Skibniewski, M., Skibniewska, E. M., & Urbanska-Slomka, G. (2006). Aluminum status in free living European bisons from Bialowieza primeval forest. Polish Journal of Environmental Studies, 15, 374–377.

  26. Kosla, T., & Skibniewska, E. M. (2010). The content of aluminum in the hair of Yorkshire terrier dogs from the Warsaw area depending on sex, age and keeping conditions. Trace Elements and Electrolytes, 27(4), 209–213.

  27. Kosla, T., Skibniewska, E. M., & Skibniewski, M. (2011). The state of bioelements in the hair of free-ranging European bisons from Białowieża Primeval Forest. Polish Journal of Veterinary Sciences, 14(1), 81–86.

  28. Kucharzak, E., Moryl, A., Szyoiszynski, K., & Jopek, Z. (2005). Influence of environment on aluminum content in game animal tissues. Medycyna Weterynaryjna, 61(11), 1277–1279.

  29. Lamand, M. (1987). Place du laboratoire dans le diagnostic des carences en oligo-éléments. Record of Medicine Veterinary, 163, 1071–1082.

  30. Liu, Z. P. (2003). Lead poisoning combined with cadmium in sheep and horses in the vicinity of non-ferrous metal smelters. The Science of The Total Environment, 309(1-3), 117–126.

  31. McLean, C. M., Koller, C. E., Rodger, J. C., & MacFarlane, G. R. (2009). Mammalian hair as an accumulative bioindicator of metal bioavail ability in Australian terrestrial environments. The Science of the Total Environment, 407, 3588–3596.

  32. Metcheva, R., Yurukova, L., Teodorova, S., & Nikolova, E. (2006). The penguin feathers as bioindicator of Antarctica environmental state. The Science of the Total Environment, 362, 259–265.

  33. Milton, A., & Johnson, M. S. (2002). Food chain transfer of zinc within the ecosystem of old and modern metalliferous mine wastes. Environmental Technology, 23, 525–536.

  34. National Research Council. (2007). Nutrient requirements of small ruminants, sheep, goats, cervids, and new world camelids (p. 362). Washington, D.C.: National Academy Press.

  35. Ohlendorf, H. M., & Heinz, G. H. (2009). Selenium in Birds. In W. N. Beyer & J. P. Meador (Eds.), Environmental contaminants in biota: interpreting tissue concentrations. Boca Raton, FL: Taylor and Francis.

  36. Osweiler, G. D., Carson, T. L., Buck, W. B., & Van Gelder, G. A. (Eds.). (1985). Clinical and diagnostic veterinary toxicology, 3rd ed., pp. 107–120. Kendall/Hunt. IA: Dubuque.

  37. Pragst, F., & Balikova, M. A. (2006). State of the art in hair analysis for detection of drug and alcohol abuse. Clinica Chimica Acta, 370(1–2), 17–49.

  38. Pearce, D. C., Dowling, K., Gerson, A. R., Sim, M. R., Sutton, S. R., Newville, M., Russell, R., & McOrist, G. (2010). Arsenic microdistribution and speciation in toenail clippings of children living in a historic gold mining area. The Science of the Total Environment, 408, 2590–2599.

  39. Pérez-Granados, A. M., & Vaquero, M. P. (2002). Silicon, aluminium, arsenic and lithium: Essentiality and human health implications. The Journal of Nutrition Health and Aging, 6, 154–162.

  40. Pugh, D. G. (1993). Copper nutrition in llamas. Llamas, 7(2), 77–79.

  41. Ralston, N. V. C., & Raymond, L. J. (2010). Dietary selenium’s protective effects against methylmercury toxicity. Toxicology, 278, 112–123.

  42. R Core Team. (2015). R: a language and environment lfor statistical computing. Vienna: R Foundation for Statistical Computing Available: http://www.R-projectorg/

  43. Rosychuk, R. A. W. (1994). Llama dermatology. The Veterinary Clinics of North America. Food Animal Practice, 10, 228–239.

  44. Spahn, S. A., & Sherry, T. W. (1999). Cadmium and lead exposure associated with reduced growth rates, poorer fledging success of little blue heron chicks (Egretta caerulea) in South Louisiana wetlands. Archives of Environmental Contamination and Toxicology, 37, 377–384.

  45. Smedley, P. L., & Kinniburgh, D. G. (2002). A review of the source, behavior and distribution of arsenic in natural waters. Applied Geochemistry, 17, 517–568.

  46. Squadrone, S., Abete, M. C., Brizio, P., Monaco, G., Colussi, S., Biolatti, C., Modesto, P., Acutis, P. L., Pessani, D., & Favaro, L. (2016). Sex- and age-related variation in metal content of penguin feathers. Ecotoxicology, 25(2), 431–438.

  47. U. S. Environmental Protection Agency (USEPA). (1986). Health assessment document for nickel and nickel compounds. EPA Report 600/8-83/012FF. 460 pp. Washington, DC: US EPA.

  48. U. S. Environmental Protection Agency (USEPA). 1980. Ambient water quality criteria for nickel. EPA Report 440/5-80-060. 206 pp. Washington, DC: US EPA.

  49. Van Saun, R. J. (2006). Nutritional diseases of South American camelids. Small Ruminant Research, 61, 153–164.

  50. Van Saun, R. J. (2009a). Nutritional diseases of llama and alpacas. The Veterinary Clinics of North America. Food Animal Practice, 25, 797–810.

  51. Van Saun, R. J. (2009b). Nutritional requirements and assessing nutritional status in camelids. The Veterinary Clinics of North America. Food Animal Practice, 25, 265–279.

  52. Vaughan, J. (2007). Ovarian synchronization and induction of ovulation in llamas and alpacas. In Current therapy in large animal theriogenology (second edition) (pp. 884–889).

  53. Vermeulen, F., Van den Brink, N. W., D'Havé, H., Mubiana, V. K., Blust, R., Bervoets, L., & De Coen, W. (2009). Habitat type-based bioaccumulation and risk assessment of metal and As contamination in earthworms, beetles and woodlice. Environmental Pollution, 157, 3098–3105.

  54. Ward, N. I., & Savage, J. M. (1994). Elemental status of grazing animals located adjacent to the London Orbital (M25) motorway. The Science of the Total Environment, 146, 185–189.

  55. Weaver, D. M., Tyler, J. W., Marion, R. S., et al. (1999). Subclinical copper accumulation in llamas. The Canadian Veterinary Journal, 40, 422–424.

  56. Yokel, R. A. (1982). Hair as an indicator of excessive aluminum exposure. Clinical Chemistry, 28, 662–665.

Download references


The authors would like to thank the alpaca farmer Pasquale Scognamiglio from “Il Quadrifoglio Alpaca farm” (Quargnento, AL, Italy) for his help in collecting and providing samples, and for his support and cooperation in this research.

Author information

Correspondence to Stefania Squadrone.

Ethics declarations

Conflict of Interest

All authors declare that they have no conflict of interest.

Ethical Approval

We received blood and fiber samples from an alpaca’s herd. The samples were collected by the local veterinarian for a routine check to determine the nutritional state of the animals and sent to the chemical laboratory. We did not aim to perform any animal research and that nobody of my institution has personally viewed as samples have been collected. Only the private veterinarian who is taking care of the farm directly managed the samples, together with the farmer, but all applicable international, national, and/or institutional guidelines for the care and use of animals were followed. After evaluating the results, we decided in agreement with the alpaca’s farmer, who is also member of the Italian National Association of alpacas and lamas (SNAEL), that they could be of interest, being data about trace elements in alpacas scarce.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Squadrone, S., Abete, M.C., Rizzi, M. et al. Bioaccumulation of Trace and Non-trace Elements in Blood and Fibers of Alpacas (Vicugna pacos) that Graze in Italian Pastures. Water Air Soil Pollut 229, 41 (2018). https://doi.org/10.1007/s11270-018-3703-7

Download citation


  • Alpacas
  • Bio indicator
  • Trace elements
  • Fibers
  • Blood