Environmental Science and Pollution Research

, Volume 23, Issue 7, pp 6074–6081 | Cite as

Mercury species accumulation and trophic transfer in biological systems using the Almadén mining district (Ciudad Real, Spain) as a case of study

  • M. J. Patiño Ropero
  • N. Rodríguez Fariñas
  • R. Mateo
  • J. J. Berzas Nevado
  • R. C. Rodríguez Martín-Doimeadios
Contamination related to anthropic activities. Characterization and remediation


The impact of mercury (Hg) pollution in the terrestrial environments and the terrestrial food chains including the impact on human food consumption is still greatly under-investigated. In particular, studies including Hg speciation and detoxification strategies in terrestrial animals are almost non-existing, but these are key information with important implications for human beings. Therefore, in this work, we report on Hg species (inorganic mercury, iHg, and monomethylmercury, MeHg) distribution among terrestrial animal tissues obtained from a real-world Hg exposure scenario (Almadén mining district, Spain). Thus, we studied Hg species (iHg and MeHg) and total selenium (Se) content in liver and kidney of red deer (Cervus elaphus; n = 41) and wild boar (Sus scrofa; n = 16). Similar mercury species distribution was found for both red deer and wild boar. Major differences were found between tissues; thus, in kidney, iHg was clearly the predominant species (more than 81 %), while in liver, the species distribution was less homogeneous with a percentage of MeHg up to 46 % in some cases. Therefore, Hg accumulation and MeHg transfer were evident in terrestrial ecosystems. The interaction between total Se and Hg species has been evaluated by tissue and by animal species. Similar relationships were found in kidney for both Hg species in red deer and wild boar. However, in liver, there were differences between animals. The possible underlying mechanisms are discussed.


Mercury Speciation Selenium Terrestrial animal Tissues Pollution 


  1. Bårregard L, Sällsten G, Conradi N (1999) Tissue levels on mercury determined in a deceased worker after occupational exposure. Int Arch Occup Environ Health 72:169–173CrossRefGoogle Scholar
  2. Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC, Krupp EM, Guzmán Bernardo FJ, Rodríguez Fariñas N, Jiménez Moreno M, Wallace D, Patiño Ropero MJ (2011) Comparison of gas chromatography hyphenated techniques for mercury speciation analysis. J Chromatogr A 1218:4545–4551Google Scholar
  3. Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC, Mateo R, Rodríguez Fariñas N, Rodríguez-Estival J, Patiño-Ropero MJ (2012a) 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
  4. Berzas Nevado JJ, Rodríguez Martín-Doimeadios RC, Guzmán Bernardo FJ, Rodríguez Fariñas N, Patiño Ropero MJ (2012b) Mercury speciation analysis in terrestrial animal tissues. Talanta 99:859–864Google Scholar
  5. BerzasNevado JJ, García Bermejo LF, Rodríguez Martín-Doimeadios RC (2003) Distribution of mercury in the aquatic environment at Almadén, Spain. Environ Pollut 122:261–271CrossRefGoogle Scholar
  6. BerzasNevado JJ, Rodríguez Martín-Doimeadios RC, Jiménez Moreno M (2009) Mercury speciation in the Valdeazogues River–La Serena reservoir system: influence of Almadén (Spain) historic mining activities. Sci Total Environ 407:2372–2382CrossRefGoogle Scholar
  7. Cabañero AI, Madrid Y, Cámara C (2005) Effect of animal feed enriched with Se and clays on Hg bioaccumulation in chickens: in vivo experimental study. J Agric Food Chem 53:2125–2132Google Scholar
  8. Clarkson TW, Magos L, Gary JM (2003) The toxicology of mercury — current exposures and clinical manifestations. N Engl J Med 349:1731–1737CrossRefGoogle Scholar
  9. Cornelis R, Caruso J, Crews H, Heuman K (2005) Handbook of elemental speciation. II, Species in the environment, food, medicine and occupational health. Wiley, ChichesterCrossRefGoogle Scholar
  10. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Halliger KK, Moroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335CrossRefGoogle Scholar
  11. Dröge S, Limper U, Emtiazi F, Schönig I, Pavlus N, Drzyzga O, Fischer U, König H (2005) In vitro and in vivo sulfate reduction in the gut contents of the termite Mastotermes darwiniensis and the rose-chafer Pachnoda marginata. J Gen Appl Microbiol 51:57–64Google Scholar
  12. Fitzgerald WF, Mason RP (1996) In: Baeyens V, Ebinghaus R, Vasiliev O (eds) Global and regional cycles: sources, fluxes and mass balances. Kluwer Academic Publishers, Dordrecht, pp 85–108CrossRefGoogle Scholar
  13. FrØslie A, Siverstsen T, Lochmiller R (2001) Perissodactyla and artiodactyla. In: Shore RF, Rattner BA (eds) Ecotoxicology of wild mammals. Wiley, Chichester, pp 497–550Google Scholar
  14. Gailer J (2007) Arsenic–selenium and mercury–selenium bonds in biology. Coord Chem Rev 251:234–254CrossRefGoogle Scholar
  15. Gailer J, George GN, Pickering IJ, Madden S, Prince RC, Yu EY, Denton MB, Younis HS, Aposhian HV (2000) Structural basis of the antagonism between inorganic mercury and selenium in mammals. Chem Res Toxicol 13:1135–1142CrossRefGoogle Scholar
  16. Gnamus A, Horvat M (1999) Mercury contaminated sites: characterization, risk assessment and remediation. In: Ebinghaus R, Turner RR, de Lacerda LD, Vasiliev O, Salomons W (eds) Springer environmental book series. Springer-Verlag, Berlin, pp 281–320Google Scholar
  17. Gnamus A, Byrne AR, Horvat M (2000) Mercury in the soil-plant-deer-predator food chain of a temperate forest in Slovenia. Environ Sci Technol 34:3337–3345CrossRefGoogle Scholar
  18. Gray JE, Hines ME, Higueras PL, Adatto I, Lasorsa BK (2004) Mercury speciation and microbial transformations in mine waters, stream sediments and surface waters at the Almadén mining district, Spain. Environ Sci Technol 38:4285–4292Google Scholar
  19. Hintelmann H (2010) Organomercurials. Their Formation and Pathways in the Environment. In: Sigel A, Sigel H, Sigel RKO (eds) Organometallics in environment and toxicology: volume 7 of metal ions in life sciences, volume 7. Royal Society of Chemistry, Cambridge, pp 365–401CrossRefGoogle Scholar
  20. 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) capture on Amamioshima Island, Japan. Chemosphere 65:657–665Google Scholar
  21. Kaschak E, Knopf B, Petersen JH, Bings NH, König H (2014) Biotic methylation of mercury by intestinal and sulfate-reducing bacteria and their potential role in mercury accumulation in the tissue of the soil-living Eisenia foetida. Soil Biol Biochem 69:202–211CrossRefGoogle Scholar
  22. Khan MAK, Wang F (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem 28:1567–1577CrossRefGoogle Scholar
  23. Klevezal' GA, Kleinenberg SE (1969) Age determination of mammals from annual layers in teeth and bones. Israel Program for Scientific Translations, Jerusalem, IsraelGoogle Scholar
  24. Lobinski R, Becker JS, Haraguchi H, Sarkar B (2010) Metallomics: guidelines for terminology and critical evaluation of analytical chemistry approaches (IUPAC Technical Report). Pure Appl Chem 82:493–504CrossRefGoogle Scholar
  25. Millán R, Gamarra R, Schmid T, Sierra MJ, Quejido AJ, Sánchez DM, Cardona AI, Fernández M, Vera R (2006) Mercury content in vegetation and soils of the Almadén mining area (Spain). Sci Total Environ 368:79–87CrossRefGoogle Scholar
  26. Millán J, Mateo R, Taggart MA, López-Bao JV, Viota M, Monsalve L, Camarero PR, Blázquez 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 399:193–201CrossRefGoogle Scholar
  27. Millán R, Lominchar MA, López-Tejedor I, Rodríguez-Alonso J, Schmid T, Sierra MJ (2012) Behaviour of mercury in the Valdeazogues riverbank soil and transfer to Nerium oleander L. J Geochem Explor 123:136–142CrossRefGoogle Scholar
  28. Millán R, Lominchar MA, Rodríguez-Alonso J, Schmid T, Sierra MJ (2014) Riparian vegetation role in mercury uptake (Valdeazogues River, Almadén, Spain). J Geochem Explor 140:104–110CrossRefGoogle Scholar
  29. Parks JM, Johs A, Podar M, Bridou R, Hurt JRA, Smith SD, Tomanicek SJ, Qian Y, Brown SD, Brandt CC, Palumbo AV, Smith JC, Wall JD, Elias DA, Liang L (2013) The genetic basis for bacterial mercury methylation. Science 339:1332–1335CrossRefGoogle Scholar
  30. 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 157:1388–1395CrossRefGoogle Scholar
  31. Rieder SR, Brunner I, Daniel O, Liu B, Frey B (2013) Methylation of mercury in earthworms and the effect of mercury on the associated bacterial communities. PLoS One 8(4):e61215CrossRefGoogle Scholar
  32. Rodríguez Martin-Doimeadios RC, Wasserman JC, García Bermejo LF, Amouroux D, BerzasNevado JJ, Donard OFX (2000) Chemical availability of mercury in stream sediments from the Almadén area, Spain. J Environ Monit 2:360–366CrossRefGoogle Scholar
  33. Sáenz de Buruaga M, Lucio AJ, Purroy FJ (1991) Reconocimiento de sexo y edad en especies cinegéticas. Diputación Foral de Álava, VitoriaGoogle Scholar
  34. Watras CJ, Huckabee JW (1992) Mercury pollution: integration and synthesis. Lewis Publishers, Boca RatonGoogle Scholar
  35. WHO (2011) Evaluation of certain food additives and contaminants. Seventy-second report of the Joint FAO/WHO Expert Committee on Food Additives. WHO technical report series No. 959Google Scholar
  36. Yannone SM, Hartung S, Menon AL, Adams MWW, Tainer JA (2012) Metals in biology: defining metalloproteomes. Curr Opin Biotechnol 23:89–95CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • M. J. Patiño Ropero
    • 1
  • N. Rodríguez Fariñas
    • 1
  • R. Mateo
    • 2
  • J. J. Berzas Nevado
    • 1
  • R. C. Rodríguez Martín-Doimeadios
    • 1
  1. 1.Facultad de Ciencias Ambientales y BioquímicaUniversidad de Castilla-La ManchaToledoSpain
  2. 2.Instituto de Recursos Cinegéticos IREC-CSIC-UCLMCiudad RealSpain

Personalised recommendations