Skip to main content

Advertisement

Log in

Bioaccumulation of Heavy Metals in the Lizard Psammodromus algirus After a Tailing-Dam Collapse in Aznalcóllar (Southwest Spain)

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

Abstract

Quantification of heavy metal concentrations in biota is a common technique that helps environmental managers measure the level of pollutants circulating in ecosystems. Despite interest in heavy metals as indicators of localized pollution, few studies have assessed these pollutants in reptiles. In 1998, the tailing pond of a pyrite mine near Aznalcóllar (southwestern Spain), containing mud with high heavy metal concentrations, collapsed, releasing 6 million m3 of toxic sludge into the Guadiamar Basin. Here we analyze heavy metal concentrations in the most common reptile in the area, the large psammodromus, Psammodromus algirus, a rather small lizard. We quantified levels of several elements (Hg, Sb, Cd, Cr, Tl, Sn, Ba, Cu, Pb, Sr, Mn, Rb, As, and Zn) in lizard tail clips collected in and around the affected area during the springs of 2005 and 2006. Samples were collected from two contaminated localities, one directly affected by the spill, and another adjacent to the tailing pond, but not covered by toxic mud. We also collected samples from a nonpolluted control site in the same basin. We found higher concentrations of As, Tl, Sn, Pb, Cd, and Cu in lizards from the affected area than in lizards from the control site, indicating the continued presence of heavy metal pollutants in the terrestrial food chain 8 years after the mine accident. We did not uncover sexual or annual differences in heavy metal concentrations, although concentrations increased with lizard size. We discuss how heavy metals moved across the food chain to lizards, despite intensive restoration efforts after the accident, and suggest that reptiles to be included in biomonitoring programs of heavy metals pollution in terrestrial habitats.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar J, Dorronsoro C, Fernández E, Fernández J, García I, Martín F, Sierra M, Simón M (2007) Remediation of As-contaminated soils in the Guadiamar River basin (SW Spain). Water Air Soil Pollut 180:109–118

    Article  CAS  Google Scholar 

  • Alastuey A, García-Sánchez A, López F, Querol X (1999) Evolution of pyrite mud weathering and mobility of heavy metals in the Guadiamar valley after the Aznalcóllar spill, south-west Spain. Sci Total Environ 242:41–55

    Article  CAS  Google Scholar 

  • Alcorlo P, Otero M, Crehuet M, Baltanás A, Montes C (2006) The use of the red-swamp crayfish (Procambarus clarkii, Girard) as indicator of the bioavailability of heavy metals in environmental monitoring in the River Guadiamar (SW, Spain). Sci Total Environ 366:380–390

    Article  CAS  Google Scholar 

  • Avery RA, White AS, Martín NH, Hopkin SP (1983) Concetrations of heavy metals in common lizards (Lacerta vivipara) and their food and environment. Amphibia-Reptilia 4:205–213

    Google Scholar 

  • Benito V, Devesa V, Munñoz O, Suñer MA, Montoro R, Baos R, Hiraldo F, Ferrer M, Fernández M, González MJ (1999) Trace elements in blood collected from birds feeding in the area around Doñana National Park affected by the toxic spill from the Aznalcóllar mine. Sci Total Environ 242:309–323

    Article  CAS  Google Scholar 

  • Beyersmann D (1991) The significance of interactions in metal essentiality and toxicity. In: Merian E (ed) Metals and their compounds in the environment. Occurrence, analysis and biological relevance. VCH Verlagsgesellscheft, Weinheim, Germany

    Google Scholar 

  • Burger J, Campbell KR, Campbell TS (2004) Gender and spatial patterns in metal concentrations in brown anoles (Anolis sagrei) in southern Florida, USA. Environ Toxicol Chem 23:712–718

    Article  CAS  Google Scholar 

  • Burger J, Campbell KR, Campbell TS, Shukla T, Jeitner C, Gochfeld M (2005) Use of skin and blood as non-lethal indicators of heavy metal contamination in northern water snakes (Nerodia sipedon). Arch Environ Contam Toxicol 49:232–238

    Article  CAS  Google Scholar 

  • Burger J, Murria S, Gaines KF, Novak JM, Punshon T, Dixon C, Gochfeld M (2006) Element levels in snakes in South Carolina: differences between a control site and an exposed site on Savannah River site. Environ Monit Assess 112:35–52

    Article  CAS  Google Scholar 

  • Cabrera F, Clemente L, Díaz Barrientos E, López R, Murillo JM (1999) Heavy metal pollution of soils affected by the Guadiamar toxic flood. Sci Total Environ 242:117–129

    Article  CAS  Google Scholar 

  • Campbell KR, Campbell TS (2002) A logical starting for developing priorities for lizard and snake ecotoxicology: a review of available data. Environ Toxicol Chem 21:894–898

    Article  CAS  Google Scholar 

  • Carretero MA, Kaliontzopoulou A (2005) Size and shape variation between populations of the lizard Psammodromus algirus. In: 5th World Congress of Herpetology 19–24 June. Abstract book. Stellonbosch, South Africa

  • Carretero MA, Llorente GA (1993) Feeding of two sympatric lacertids in a sandy coastal area (Ebro Delta, Spain). In: Valakos ED, Bohme W, Pérez-Mellado V, Maragou P (eds) Lacertids of the Mediterranean region. A biological approach. Hellenic Zoological Society, Athens, pp 155

    Google Scholar 

  • Carretero MA, Llorente GA (1997) Habitat preferences of two sympatric lacertid in the Ebro Delta (NE Spain). In: Bohme W, Bischoff W, Ziegler T (eds) Herpetologia Bonnensis. Societas Europaea Herpetologica, Bonn, p 51

    Google Scholar 

  • Carretero MA, Montori A, Llorente GA, Santos X (2002) Psammodromus algirus (Linné, 1758) Lagartija colilarga. In: Pleguezuelos JM, Márquez R, Lizana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Segunda impresión. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española, Madrid, p 260

    Google Scholar 

  • Chang LW (1996) Toxicology of metals. Lewis, Boca Raton, FL

    Google Scholar 

  • Díaz JA, Carrascal LM (1990) Prey size and food selection of Psammodromus algirus (Lacertidae) in central Spain. J Herpetol 2:342–347

    Article  Google Scholar 

  • Dorronsoro C, Martin F, Ortiz I, García I, Simón M, Fernández (2002) Migration of trace elements from pyrite tailings in carbonate soils. J Environ Qual 31:829–835

  • Fletcher DE, Hopkins WA, Saldaña T, Baionno JA, Arribas C, Standora MM, Fernández-Delgado C (2006) Geckos as indicators of mining pollution. Environ Toxicol Chem 25:2432–2445

    Article  CAS  Google Scholar 

  • Gallart F, Benito G, Martín-Vide JP (1999) Fluvial geomorphology and hydrology in the dispersal and fate of pyrite mud particles released by the Aznalcóllar mine tailings spill. Sci Total Environ 242:13–26

    Article  CAS  Google Scholar 

  • Grimalt JO, Ferrer M, Macpherson E (1999) The mine tailing accident in Aznalcóllar. Sci Total Environ 242:3–11

    Article  CAS  Google Scholar 

  • Hesel DR (1990) Less than obvious: statistical treatment of data below the detection limit. Environ Sci Technol 39:419–423

    Article  Google Scholar 

  • Hopkins WA (2000) Reptile toxicology: challenges and opportunities on the last frontier in vertebrate ecotoxicology. Environ Toxicol Chem 19:2391–2393

    Article  CAS  Google Scholar 

  • Hopkins WA, Roe JH, Snodgrass JW, Jackson BP, Kling DE, Rowe CL, Congdon JD (2001) Nondestructive indices of trace element exposure in squamate reptiles. Environ Pollut 115:1–7

    Article  CAS  Google Scholar 

  • Hopkins WA, Roe JH, Snodgrass JW, Staub BP, Jackson BP, Congdon JD (2002) Effects of chronic dietary exposure to trace elements on banded water snake (Nerodia fasciata). Environ Toxicol Chem 21:906–913

    Article  CAS  Google Scholar 

  • Hopkins WA, Stauba BP, Baionnoa JA, Jacksona BP, Talentb LG (2005) Transfer of selenium from prey to predators in a simulated terrestrial food chain. Environ Pollut 134:447–456

    Google Scholar 

  • Hsu MJ, Selvaraj K, Agoramoorthy G (2006) Taiwan’s industrial heavy metal pollution threatens terrestrial biota. Environ Pollut 143:327–334

    Article  CAS  Google Scholar 

  • Jelaska LS, Blanus M, Durbes P, Jelaska SD (2007) Heavy metal concentrations in ground beetles, leaf litter, and soil of a forest ecosystem. Ecotoxicol Environ Saf 66:74–81

    Article  CAS  Google Scholar 

  • Jon Peter AL, Viraraghavan T (2005) Thallium: a review of public health and environmental concerns. Environ Int 31:493–501

    Article  CAS  Google Scholar 

  • Krauss U, Wiegand J (2006) Long-term effects of the Aznalcóllar mine spill−heavy metal content and mobility in soils and sediments of the Guadiamar river valley (SW Spain). Sci Total Environ 367:855–871

    Article  CAS  Google Scholar 

  • Lambert MRK (1997) Environmental effects of heavy spillage from a destroyed pesticide store near Hargeisa (Somaliland) assessed during the dry season, using reptiles and amphibians as bioindicators. Arch Environ Contam Toxicol 32:80–93

    Article  CAS  Google Scholar 

  • Lance VA, Cort T, Masuoka J, Lawson R, Saltman P (1995) Unusual high zinc concentrations in snake plasma, with observations on plasma zinc concentrations in lizards, turtles and alligators. J Zool 235:577–585

    Article  Google Scholar 

  • Linder G, Grillitsch B (2000) Ecotoxicology of metals. In: Sparling DW, Linder G, Bishop CA (eds) Ecotoxicology of amphibians and reptiles. SETAC, Pensacola, FL, p 325

    Google Scholar 

  • Loumbordis NS (1997) Heavy metals contamination in a lizard, Agama stellio stellio, compared in urban, high altitude and agricultural, low altitude areas of north Greece. Environ Contam Toxicol 58:945–952

    Article  Google Scholar 

  • Madejón P, Marañón T, Murillo JA, Robinson B (2004) White poplar (Populus alba) as a biomonitor of trace elements in contaminated riparian forests. Environ Pollut 132:145–155

    Article  CAS  Google Scholar 

  • Madejón P, Marañón T, Murillo JA (2006) Biomonitoring of trace elements in the leaves and fruits of wild olive and Holm oak trees. Sci Total Environ 355:187–203

    Article  CAS  Google Scholar 

  • Mann RM, Serra EA, Soares AMVM (2006) Assimilation of cadmium in a European lacertid lizard: is trophic transfer important? Environ Toxicol Chem 25:3199–3203

    Article  CAS  Google Scholar 

  • Mann RM, Sánchez-Hernández JC, Serra EA, Soares AMVM (2007). Bioaccumulation of Cd by a European lacertid lizard after chronic exposure to Cd-contaminated food. Chemosphere 68:1525–1534

    Article  CAS  Google Scholar 

  • Marco A, López-Vicente M, Pérz-Mellado V (2004) Arsenic uptake by reptile flexible-shelled eggs from contamined nest substrates and toxic effect of embryos. Bull Environ Contam Toxicol 72:983–990

    Article  CAS  Google Scholar 

  • Marco A, López-Vicente ML, Pérez-Mellado V (2005) Soils acidification negatively affects embryonic development of flexible-shelled lizard eggs. Herpetol J 15:107–111

    Google Scholar 

  • Márquez-Ferrando R, Pleguezuelos JM, Santos X, Ontiveros D, Fernández- Cardenete JR (2008) Recovering the reptile community after the mine-tailing accident of Aznalcóllar (SW Spain). Res Ecol 2008 (in press)

  • Meharg AA, Osborn D, Pain DJ, Sánchez A, Naveso MA (1999) Contamination of Doñana food-chains after the Aznalcóllar mine disaster. Environ Pollut 105:387–390

    Article  CAS  Google Scholar 

  • Olías M, Cerón JC, Moral F, Ruiz F (2006) Water quality of the Guadiamar River after the Aznalcóllar spill (SW Spain). Chemosphere 62:213–225

    Article  CAS  Google Scholar 

  • Ordóñez R, Giráldez JV, Vanderlinden K, Carbonell R, González P (2006) Temporal and spatial monitoring of the pH and heavy metals in a soil polluted by mine spill post cleaning effects. Water Air Soil Pollut 178:229–243

    Article  CAS  Google Scholar 

  • Pain DJ, Sánchez A, Meharg AA (1998) The Doñana disaster: contamination of a world heritage estuarine marsh ecosystem with acidified pyrite mine waste. Sci Total Environ 222:45–54

    Article  CAS  Google Scholar 

  • Pérez-Quintero JC, Rubio-García JC (1997) Alimentación de la lagartija colilarga, Psammodromus algirus (L) (Sauria, Lacertidae), en el litoral de Huelva (SO España). Doñana-Acta Vertebrata 34:3–26

    Google Scholar 

  • PICOVER (2003) Ciencia y Restauración del Río Guadiamar. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla

  • Querol X, Alastuey A, López-Soler A, Plana F (2000) Levels and chemistry of atmospheric particulates induced by spill of heavy metal mining wastes in the Doñana area, southwest Spain. Atmos Environ 34:239–253

    Article  CAS  Google Scholar 

  • Querol X, Alastuey A, Moreno N, Alvarez-Ayuso E, García-Sánchez A, Cama J, Ayora C, Simón M (2006) Immobilization of heavy metals in polluted soils by the addition of zeolitic material synthesized from coal fly ash. Chemosphere 62:171–180

    Article  CAS  Google Scholar 

  • Salvador A. Reptiles (1998) In: Ramos MA (coord.) Fauna Ibérica, vol 10. Museo Nacional de Ciencias Naturales, CSIC, Madrid

  • Sanpera C, Morera M, Ruíz X, Jover L (2000) Variability of mercury and selenium levels in clutches of Audouin’s gulls (Larus audouinii) breeding at the Chafarinas Islands, southwest Mediterranean. Environ Contam Toxicol 39:119–123

    CAS  Google Scholar 

  • Sánchez-Chardi A (2007) Tissue, age, and sex distribution of thallium in shrews from Doñana, a protected area in SW Spain. Sci Total Environ 383:237–240

    Article  CAS  Google Scholar 

  • Santos X, Pastor D, Llorente GA, Albaigés J (1999) Organochlorine levels in viperine snake Natrix maura carcasses from the Ebro Delta (NE Spain): sexual and size-related differences. Chemosphere 39:2641–2650

    Article  CAS  Google Scholar 

  • Schmidt J (1980) Blei- und Cadmium-Rückstände bei inner- und ausserstädtischen Lacerta populationen. Verhand Gesell Ökol 9:297–300

    CAS  Google Scholar 

  • Schmidt J (1988) Indikatorbedeutung von Lacerta agilis für die Bewertung urbaner Raume. Mertensiella 1:195–204

    Google Scholar 

  • Simón M, Ortiz I, García I, Fernández E, Fernández J, Dorronsoro C (1999) Pollution of soils by the toxic spill of a pyrite mine (Aznalcóllar, Spain). Sci Total Environ 242:105–115

    Article  Google Scholar 

  • Solá C, Burgos M, Plazuelo A, Toja J, Plansa M, Prat N (2004) Heavy metal bioaccumulation and macroinvertebrate community changes in a Mediterranean stream affected by acid mine drainage and an accidental spill (Guadiamar River, SW Spain). Sci Total Environ 333:109–126

    Article  CAS  Google Scholar 

  • Taggart MA, Figuerola J, Green AJ, Mateo R, Deacon C, Osborn D, Meharg AA (2006) After the Aznalcóllar mine spill: arsenic, zinc, selenium, lead and copper levels in the livers and bones of five waterfowl species. Environ Res 100:349–361

    Article  CAS  Google Scholar 

  • Toja J, Alcalá E, Burgos MD, Martín G, Plazuelo A, de Schutter T (2003) Efecto del vertido tóxico en las comunidades de plancton y perifiton del río Guadiamar. In: Arenas JM, Martínez-Faraco FR, Mora A (eds) PICOVER 1998–2002. Ciencia y restauración del río Guadiamar. Junta de Andalucía: Consejería de Medio Ambiente, Sevilla, p 94

    Google Scholar 

  • Van Straalen NM, Butovsky RO, Pokarzhevskii AD, Zaitsev AS, Verhoef CS (2001) Metal concentrations in soil and in invertebrates in the vicinity of a metallurgical factory near Tula (Russia). Pedobiologia 45:451–466

    Article  Google Scholar 

Download references

Acknowledgments

We thank A. Herrero and M. Lorenzo for field assistance. We also thank M. Pizarro and J. Poquet for technical support. M. C. Cruces, C. Sanpera, and X. Ruiz made valuable comments on an early version of the manuscript. Kirk Setser improved the style of the manuscript. This study was supported by the SECOVER program (Regional Environmental Agency, Sevilla, Spain) from 2004 to 2006. Xavier Santos was supported by a Beatriu de Pinós postdoctoral grant from the Generalitat de Catalunya (BP-B1 10211).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rocío Márquez-Ferrando.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Márquez-Ferrando, R., Santos, X., Pleguezuelos, J.M. et al. Bioaccumulation of Heavy Metals in the Lizard Psammodromus algirus After a Tailing-Dam Collapse in Aznalcóllar (Southwest Spain). Arch Environ Contam Toxicol 56, 276–285 (2009). https://doi.org/10.1007/s00244-008-9189-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-008-9189-3

Keywords

Navigation