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Transfer of heavy metals through terrestrial food webs: a review

  • Jillian E. Gall
  • Robert S. Boyd
  • Nishanta Rajakaruna
Article

Abstract

Heavy metals are released into the environment by both anthropogenic and natural sources. Highly reactive and often toxic at low concentrations, they may enter soils and groundwater, bioaccumulate in food webs, and adversely affect biota. Heavy metals also may remain in the environment for years, posing long-term risks to life well after point sources of heavy metal pollution have been removed. In this review, we compile studies of the community-level effects of heavy metal pollution, including heavy metal transfer from soils to plants, microbes, invertebrates, and to both small and large mammals (including humans). Many factors contribute to heavy metal accumulation in animals including behavior, physiology, and diet. Biotic effects of heavy metals are often quite different for essential and non-essential heavy metals, and vary depending on the specific metal involved. They also differ for adapted organisms, including metallophyte plants and heavy metal-tolerant insects, which occur in naturally high-metal habitats (such as serpentine soils) and have adaptations that allow them to tolerate exposure to relatively high concentrations of some heavy metals. Some metallophyte plants are hyperaccumulators of certain heavy metals and new technologies using them to clean metal-contaminated soil (phytoextraction) may offer economically attractive solutions to some metal pollution challenges. These new technologies provide incentive to catalog and protect the unique biodiversity of habitats that have naturally high levels of heavy metals.

Keywords

Ecosystem health Metal toxicity Metal hyperaccumulation Bioaccumulation Environmental pollution Phytoremediation 

References

  1. Adriano, D. C., Wenzel, W. W., Vangronsveld, J., & Bolan, N. S. (2004). Role of assisted natural remediation in environmental cleanup. Geoderma, 122, 121–142.CrossRefGoogle Scholar
  2. Alonso, M. L., Benedito, J. L., Miranda, M., Castillo, C., Hernández, J., & Shore, R. F. (2002a). Interactions between toxic and essential trace metals in cattle from a region with low levels of pollution. Archives of Environmental Contamination and Toxicology, 42, 165–172.CrossRefGoogle Scholar
  3. Alonso, M. L., Benedito, J. L., Miranda, M., Castillo, C., Hernández, J., & Shore, R. F. (2002b). Cattle as biomonitors of soil arsenic, copper, and zinc concentrations in Galicia (NW Spain). Archives of Environmental Contamination and Toxicology, 43, 103–108.CrossRefGoogle Scholar
  4. Alonso, M. L., Benedito, J. L., Miranda, M., Castillo, C., Hernández, J., & Shore, R. F. (2003). Mercury concentrations in cattle from NW Spain. Science of the Total Environment, 302, 93–100.CrossRefGoogle Scholar
  5. Amaya, E., Gil, F., Olmedo, P., Fernandez-Rodriguez, M., Fernandez, M. F., & Olea, N. (2013). Placental concentrations of heavy metals in a mother-child cohort. Environmental Research, 120, 63–70.CrossRefGoogle Scholar
  6. Anderson, B., de Peyster, A., Gad, S. C., Hakkinen, P. J. B., Kamrin, M., Locey, B., Mehendale, H. M., Pope, C., Shugart, L., & Wexler, P. (2005). Encyclopedia of toxicology (2nd ed.). Amsterdam: Elsevier.Google Scholar
  7. Angle, J. S., & Linacre, N. A. (2005). Metal phytoextraction—a survey of potential risks. International Journal of Phytoremediation, 7, 241–254.CrossRefGoogle Scholar
  8. Appleton, J., Lee, K. M., Sawicka-Kapusta, K., Damek, M., & Cooke, M. (2000). The heavy metal content of the teeth of the bank vole (Clethrionomys glareolus) as an exposure marker of environmental pollution in Poland. Environmental Pollution, 110, 441–449.CrossRefGoogle Scholar
  9. Atafar, Z., Mesdaghinia, A., Nouri, J., Homaee, M., Yunesian, M., Ahmadimoghaddam, M., & Mahvi, A. H. (2010). Effect of fertilizer application on soil heavy metal concentration. Environmental Monitoring and Assessment, 160, 83–89.CrossRefGoogle Scholar
  10. Bååth, E. (1989). Effects of heavy metals in soil on microbial processes and populations (a review). Water, Air, and Soil Pollution, 47, 335–379.CrossRefGoogle Scholar
  11. Babin-Fenske, J. J., & Anand, M. (2010). Terrestrial insect communities and the restoration of an industrially perturbed landscape: assessing success and surrogacy. Restoration Ecology, 18, 73–84.CrossRefGoogle Scholar
  12. Babin-Fenske, J., & Anand, M. (2011). Patterns of insect communities along a stress gradient following decommissioning of a Cu-Ni smelter. Environmental Pollution, 159, 3036–3043.CrossRefGoogle Scholar
  13. Bahadorani, S., & Hilliker, A. J. (2009). Biological and behavioral effects of heavy metals in Drosophila melanogaster adults and larvae. Journal of Insect Behavior, 22, 399–411.CrossRefGoogle Scholar
  14. Baker, A. J. M. (1981). Accumulators and excluders—strategies in the response of plants to heavy metals. Journal of Plant Nutrition, 3, 643–654.CrossRefGoogle Scholar
  15. Baker, A. J. M., & Walker, P. L. (1989). Ecophysiology of metal uptake by tolerant plants. In A. J. Shaw (Ed.), Heavy metal tolerance in plants—evolutionary aspects (pp. 155–177). Boca Raton: CRC.Google Scholar
  16. Bayley, M., Baatrup, E., Heimbach, U., & Bjerregaard, P. (1995). Elevated copper levels during larval development cause altered locomotor behavior in the adult carabid beetle Pterostichus cupreus L. (Coleoptera: Carabidae). Ecotoxicology and Environmental Safety, 32, 166–170.CrossRefGoogle Scholar
  17. Beernaert, J., Scheirs, J., Leirs, H., Blust, R., & Verhagen, R. (2007). Non-destructive pollution exposure assessment by means of wood mice hair. Environmental Pollution, 145, 443–451.CrossRefGoogle Scholar
  18. Belimov, A. A., Hontzeas, N., Safronova, V. I., Demchinskaya, S. V., Piluzza, G., Bullitta, S., & Glick, B. R. (2005). Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biology & Biochemistry, 37, 241–250.CrossRefGoogle Scholar
  19. Behmer, S. T., Lloyd, C. M., Raubenheimer, D., Stewart-Clark, J., Knight, J., Leighton, R. S., Harper, F. A., & Smith, J. A. C. (2005). Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Functional Ecology, 19, 55–66.CrossRefGoogle Scholar
  20. Beyer, W. N., Connor, E. E., & Gerould, S. (1994). Estimates of soil ingestion by wildlife. Journal of Wildlife Management, 58, 375–382.CrossRefGoogle Scholar
  21. Bitterli, C., Bañuelos, G. S., & Schulin, R. (2010). Use of transfer factors to characterize uptake of selenium by plants. Journal of Geochemical Exploration, 107, 206–216.CrossRefGoogle Scholar
  22. Blaylock, M. J., & Huang, J. W. (2000). Phytoextraction of metals. In I. Raskin & B. D. Ensley (Eds.), Phytoremediation of toxic metals: using plants to clean up the environment (pp. 53–70). Toronto: Wiley.Google Scholar
  23. Blottner, S., Frölich, K., Roelants, H., Streich, J., & Tataruch, F. (1999). Influence of environmental cadmium on testicular proliferation in roe deer. Reproductive Toxicology, 13, 261–267.CrossRefGoogle Scholar
  24. Boshoff, M., De Jonge, M., Dardenne, F., Blust, R., & Bervoets, L. (2014). The impact of metal pollution on soil faunal and microbial activity in two grassland ecosystems. Environmental Research, 134, 169–180.CrossRefGoogle Scholar
  25. Bourioug, M., Gimbert, F., Alaoui-Sehmer, L., Benbrahim, M., Aleya, L., & Alaoui-Sossé, B. (2015). Sewage sludge application in a plantation: effects on trace metal transfer in soil–plant–snail continuum. Science of the Total Environment, 502, 309–314.CrossRefGoogle Scholar
  26. Boyd, R. S. (2002). Does elevated body Ni concentration protect insects against pathogens? A test using Melanotrichus boydi (Heteroptera: Miridae). American Midland Naturalist, 147, 225–236.CrossRefGoogle Scholar
  27. Boyd, R. S. (2004). Ecology of metal hyperaccumulation. New Phytologist, 162, 563–567.CrossRefGoogle Scholar
  28. Boyd, R. S. (2007). The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant and Soil, 293, 153–176.CrossRefGoogle Scholar
  29. Boyd, R. S. (2009). High-nickel insects and nickel hyperaccumulator plants: a review. Insect Science, 16, 19–31.CrossRefGoogle Scholar
  30. Boyd, R. S. (2010). Heavy metal pollutants and chemical ecology: exploring new frontiers. Journal of Chemical Ecology, 36, 46–58.CrossRefGoogle Scholar
  31. Boyd, R. S. (2012). Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Science, 195, 88–95.CrossRefGoogle Scholar
  32. Boyd, R. S. (2014). Ecology and evolution of metal-hyperaccumulator plants. In N. Rajakaruna, R. S. Boyd, & T. Harris (Eds.), Plant ecology and evolution in harsh environments (pp. 227–241). Hauppauge: Nova.Google Scholar
  33. Boyd, R. S., & Jaffré, T. (2001). Phytoenrichment of soil Ni concentration by Sebertia acuminata in New Caledonia and the concept of elemental allelopathy. South African Journal of Science, 97, 535–538.Google Scholar
  34. Boyd, R. S., Kruckeberg, A. R., & Rajakaruna, N. (2009). Biology of ultramafic rocks and soils: research goals for the future. Northeastern Naturalist, 16, 422–440.CrossRefGoogle Scholar
  35. Boyd, R. S., & Martens, S. N. (1998). The significance of metal hyperaccumulation for biotic interactions. Chemoecology, 8, 1–7.CrossRefGoogle Scholar
  36. Boyd, R. S., & Rajakaruna, N. (2013). Heavy metal tolerance. In D. Gibson (Ed.), Oxford bibliographies in ecology (pp. 1–24). New York: Oxford University Press.Google Scholar
  37. Boyd, R. S., & Wall, M. A. (2001). Responses of generalist predators fed high-Ni Melanotrichus boydi (Heteroptera: Miridae): elemental defense against the third trophic level. American Midland Naturalist, 146, 186–198.CrossRefGoogle Scholar
  38. Boyd, R. S., Wall, M. A., & Jaffré, T. (2006). Nickel levels in arthropods associated with Ni hyperaccumulator plants from an ultramafic site in New Caledonia. Insect Science, 13, 271–277.CrossRefGoogle Scholar
  39. Brandl, H. (2001). Heterotrophic leaching. In G. M. Gadd (Ed.), Fungi in bioremediation (pp. 383–423). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  40. Brandl, H., & Faramarzi, M. A. (2006). Microbe-metal-interactions for the biotechnological treatment of metal-containing solid waste. China Particuology, 4, 93–97.CrossRefGoogle Scholar
  41. Brekken, A., & Steinnes, E. (2004). Seasonal concentration of cadmium and zinc in native pasture plants: consequences for grazing animals. Science of the Total Environment, 326, 181–195.CrossRefGoogle Scholar
  42. Brussaard, L. (1997). Biodiversity and ecosystem function in soil. Ambio, 26, 563–570.Google Scholar
  43. Buchwalter, D. B., Cain, D. J., Clements, W. H., & Luoma, S. N. (2007). Using biodynamic models to reconcile differences between laboratory toxicity tests and field biomonitoring with aquatic insects. Environmental Science and Technology, 41, 4821–4828.CrossRefGoogle Scholar
  44. Cai, S., Yue, L., Hu, Z. N., Zhong, X. Z., Ye, Z. L., Xu, H. D., Liu, Y. R., Ji, R. D., Zhang, W. H., & Zhang, F. Y. (1990). Cadmium exposure and health effects among residents in an irrigation area with ore dressing waste water. Science of the Total Environment, 90, 67–73.CrossRefGoogle Scholar
  45. Cai, Q., Long, M. L., Zhu, M., Zhou, Q. Z., Zhang, L., & Liu, J. (2009). Food chain transfer of cadmium and lead to cattle in a lead-zinc smelter in Guizhou, China. Environmental Pollution, 157, 3078–3082.CrossRefGoogle Scholar
  46. Cao, H., Chen, J., Zhang, J., Zhang, H., Qiao, L., & Men, Y. (2010). Heavy metals in rice and garden vegetables and their potential health risks to inhabitants in the vicinity of an industrial zone in Jiangsu, China. Journal of Environmental Sciences, 22, 1792–1799.CrossRefGoogle Scholar
  47. Cao, X., Ma, L. Q., Rhue, D. R., & Appel, C. S. (2004). Mechanisms of lead, copper, and zinc retention by phosphate rock. Environmental Pollution, 131, 435–444.CrossRefGoogle Scholar
  48. Chaffai, R., & Koyama, H. (2011). Heavy metal tolerance in Arabidopsis thaliana. Advances in Botanical Research, 60, 1–49.CrossRefGoogle Scholar
  49. Chander, K., Brookes, P. C., & Harding, S. A. (1995). Microbial biomass dynamics following addition of metal-enriched sewage sludges to a sandy loam. Soil Biology and Biochemistry, 27, 1049–1421.CrossRefGoogle Scholar
  50. Chaney, R. L., Angle, J. S., Broadhurst, C. L., Peters, C. A., Tappero, R. V., & Sparks, D. L. (2007). Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. Journal of Environmental Quality, 36, 1429–1443.CrossRefGoogle Scholar
  51. Chary, N. S., Kamala, C. T., & Raj, D. S. S. (2008). Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicology and Environmental Safety, 69, 513–524.CrossRefGoogle Scholar
  52. Cheruiyot, D. J., Boyd, R. S., Coudron, T. A., & Cobine, P. (2013). Biotransfer, bioaccumulation and effects of herbivore dietary Co, Cu, Ni and Zn on growth and development of the insect predator Podisus maculiventris (Say) (Hemiptera: Pentatomidae). Journal of Chemical Ecology, 39, 764–772.CrossRefGoogle Scholar
  53. Cole, M. M. (1973). Geobotanical and biogeochemical investigations in the sclerophyllous woodland and shrub associations of the Eastern Goldfields area of Western Australia, with particular reference to the role of Hybanthus floribundus (Lindl.) F. Muell. as a nickel indicator and accumulator plant. Journal of Applied Ecology, 10, 269–320.CrossRefGoogle Scholar
  54. Comber, S. D. W., & Gunn, A. M. (1996). Heavy metals entering sewage-treatment works from domestic sources. Water and Environment Journal, 10, 137–142.CrossRefGoogle Scholar
  55. Cui, J., Zhu, Y. G., Zhai, R. H., Chen, D. Y., Huang, Y. Z., Qui, Y., & Liang, J. Z. (2004). Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environment International, 30, 785–791.CrossRefGoogle Scholar
  56. Dai, J., Becquer, T., Rouiller, J. H., Reversat, G., Bernhard-Reversat, F., Nahmani, J., & Lavelle, P. (2004). Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biology and Biochemistry, 36, 91–98.CrossRefGoogle Scholar
  57. Damek-Poprawa, M., & Sawicka-Kapusta, K. (2003). Damage to the liver, kidney, and testis with reference to burden of heavy metals in yellow-necked mice from areas around steelworks and zinc smelters in Poland. Toxicology, 186, 1–10.CrossRefGoogle Scholar
  58. Devkota, B., & Schmidt, G. H. (2000). Accumulation of heavy metals in food plants and grasshoppers from the Taigetos Mountains, Greece. Agriculture Ecosystems and Environment, 78, 85–91.CrossRefGoogle Scholar
  59. Drouhot, S., Raoul, F., Crini, N., Tougard, C., Prudent, A. S., Druart, C., Rieffel, D., Lambert, J. C., Tête, N., Giraudoux, P., & Scheifler, R. (2014). Responses of wild small mammals to arsenic pollution at a partially remediated mining site in Southern France. Science of the Total Environment, 470–471, 1012–1022.CrossRefGoogle Scholar
  60. Eckel, H., Roth, U., Döhler, H., & Schultheis, U. (2008). Assessment and reduction of heavy metal input into agro-ecosystems. In P. Schlegel, S. Durosoy, & A. W. Jongbloed (Eds.), Trace elements in animal production systems (pp. 33–43). The Netherlands: Wageningen Academic.Google Scholar
  61. Efremova, M., & Izosimova, A. (2012). Contamination of agricultural soils with heavy metals. In C. Jakobsson (Ed.), Sustainable agriculture (pp. 250–252). Uppsala: Baltic University Press.Google Scholar
  62. Ellis, R. J., Morgan, P., Weightman, A. J., & Fry, J. C. (2003). Cultivation-dependant and –independent approaches for determining bacterial diversity in heavy-metal contaminated soil. Applied and Environmental Microbiology, 69, 3223–3230.CrossRefGoogle Scholar
  63. Ensley, B. D. (2000). Rationale for use of phytoremediation. In I. Raskin & B. D. Ensley (Eds.), Phytoremediation of toxic metals: using plants to clean up the environment (pp. 3–13). New York: Wiley.Google Scholar
  64. Epstein, E., & Bloom, A. J. (2004). Mineral nutrition of plants: principles and perspectives (2nd ed.). Sunderland: Sinauer.Google Scholar
  65. Ernst, W. H. O. (2006). Evolution of metal tolerance in higher plants. Forest Snow and Landscape Research, 80, 251–274.Google Scholar
  66. Fitz, W. J., & Wenzel, W. W. (2002). Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. Journal of Biotechnology, 99, 259–278.CrossRefGoogle Scholar
  67. Freeman, J. L., Quinn, C. F., Marcus, M. A., Fakra, S., & Pilon-Smits, E. A. H. (2006). Selenium-tolerant diamondback moth disarms hyperaccumulator plant defense. Current Biology, 16, 2181–2192.CrossRefGoogle Scholar
  68. Friesl-Hanl, W., Platzer, K., Horak, O., & Gerzabek, M. H. (2009). Immobilising of Cd, Pb, and Zn contaminated arable soils close to a former Pb/Zn smelter: a field study in Austria over 5 years. Environmental Geochemistry and Health, 31, 581–594.CrossRefGoogle Scholar
  69. Fritsch, C., Coeurdassier, M., Giraudoux, P., Raoul, F., Douay, F., Rieffel, D., de Vaufleury, A., & Scheifler, R. (2011). Spatially explicit analysis of metal transfer to biota: influence of soil contamination and landscape. PLoS ONE, 6(5), e20682. doi: 10.1371/journal.pone.0020682.CrossRefGoogle Scholar
  70. Gadd, G. M. (1990). Heavy metal accumulation by bacteria and other microorganisms. Experientia, 46, 834–840.CrossRefGoogle Scholar
  71. Gadd, G. M. (2010). Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology, 156, 609–643.CrossRefGoogle Scholar
  72. Gall, J. E., & Rajakaruna, N. (2013). The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In L. Minglin (Ed.), Brassicaceae: characterization, functional genomics and health benefits (pp. 121–148). Hauppauge: Nova.Google Scholar
  73. Ghosh, M., & Singh, S. P. (2005). A review on phytoremediation of heavy metals and utilization of its byproducts. Applied Ecology and Environmental Research, 3, 1–18.CrossRefGoogle Scholar
  74. Giller, K. E., Witter, E., & McGrath, S. P. (1998). Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biology and Biochemistry, 30, 1389–1414.CrossRefGoogle Scholar
  75. Giller, K. E., Witter, E., & McGrath, S. P. (2009). Heavy metals and soil microbes. Soil Biology and Biochemistry, 41, 2031–2037.CrossRefGoogle Scholar
  76. Gimeno-García, E., Andreu, V., & Boluda, R. (1996). Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environmental Pollution, 92, 19–25.CrossRefGoogle Scholar
  77. Gollenberg, A. L., Hediger, M. L., Lee, P. A., Himes, J. H., & Louis, G. M. B. (2010). Association between lead and cadmium and reproductive hormones in peripubertal U.S. girls. Environmental Health Perspectives, 118, 1782–1787.Google Scholar
  78. Goodyear, K. L., & McNeill, S. (1999). Bioaccumulation of heavy metals by aquatic macro-invertebrates of different feeding guilds: a review. Science of the Total Environment, 229, 1–19.CrossRefGoogle Scholar
  79. Goyal, N., Jain, S. C., & Banerjee, U. C. (2003). Comparative studies on the microbial adsorption of heavy metals. Advances in Environmental Research, 7, 311–319.CrossRefGoogle Scholar
  80. Gray, J. S. (2002). Biomagnification in marine systems: the perspective of an ecologist. Marine Pollution Bulletin, 45, 46–52.CrossRefGoogle Scholar
  81. Green, I. D., Diaz, A., & Tibbett, M. (2010). Factors affecting the concentration in seven-spotted ladybirds (Coccinella septempunctata L.) of Cd and Zn transferred through the food chain. Environmental Pollution, 158, 135–141.CrossRefGoogle Scholar
  82. Grzes, I. M. (2010). Ants and heavy metal pollution—a review. European Journal of Soil Biology, 46, 350–355.CrossRefGoogle Scholar
  83. Gundacker, C., Frölich, S., Graf-Rohrmeister, K., Eibenberger, B., Jessenig, V., Gicic, D., Prinz, S., Witmann, K. J., Zielser, H., Vallant, B., Pollak, A., & Husslein, P. (2010). Prenatal lead and mercury exposure in Austria. Science of the Total Environment, 408, 5744–5749.CrossRefGoogle Scholar
  84. Gupta, S. K., Vollmer, M. K., & Krebs, R. (1996). The importance of mobile, mobilisable and pseudo total heavy metal fractions in soil for three-level risk assessment and risk management. Science of the Total Environment, 178, 11–20.CrossRefGoogle Scholar
  85. Haferburg, G., Kothe, E. (2007). Microbes and metals: interactions in the environment. Journal of Basic Microbiology, 453–467.Google Scholar
  86. Haferburg, G., & Kothe, E. (2010). Metallomics: lessons for metalliferous soil remediation. Applied Microbiology and Biotechnology, 87, 1271–1280.CrossRefGoogle Scholar
  87. Hamers, T., van den Berg, J. H. J., van Gestel, C. A. M., van Schooten, F. J., & Murk, A. J. (2006). Risk assessment of metals and organic pollutants for herbivorous and carnivorous small mammal food chains in a polluted floodplain (Biesbosch, The Netherlands). Environmental Pollution, 144, 581–595.CrossRefGoogle Scholar
  88. Harrison, S. P., & Rajakaruna, N. (2011). What have we learned from serpentine about evolution, ecology, and other sciences? In S. P. Harrison & N. Rajakaruna (Eds.), Serpentine: evolution and ecology of a model system (pp. 417–427). Berkeley: University of California Press.Google Scholar
  89. Heikens, A., Peijnenburg, W. J. G. M., & Hendriks, A. J. (2001). Bioaccumulation of heavy metals in terrestrial invertebrates. Environmental Pollution, 113, 385–393.CrossRefGoogle Scholar
  90. Hladun, K. R., Parker, D. R., & Trumble, J. T. (2011). Selenium accumulation in the floral tissues of two Brassicaceae species and its impact on floral traits and plant performance. Environmental and Experimental Botany, 74, 90–97.CrossRefGoogle Scholar
  91. Hobbelen, P. H. F., Koolhaas, J. E., & Van Gestel, C. A. M. (2006). Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environmental Pollution, 144, 639–646.CrossRefGoogle Scholar
  92. Hol, W. H., de Boer, W., Termorshuizen, A. J., Meyer, K. M., Schneider, J. H. M., van Dam, N. M., van Veen, J. A., & van der Putten, W. H. (2010). Reduction of rare soil microbes modifies plant-herbivore interactions. Ecology Letters, 13, 292–301.CrossRefGoogle Scholar
  93. Hossain, M.A., Piyatida, P., Teixeria da Silva, J.A., Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany 2012, doi.org/10.1155/2012/872875.Google Scholar
  94. Hough, R. L., Breward, N., Young, S. D., Crout, N. M., Tye, A. M., Moir, A. M., & Thornton, I. (2004). Assessing potential risk of heavy metal exposure from consumption of home-produced vegetables by urban populations. Environmental Health Perspectives, 112, 215–221.CrossRefGoogle Scholar
  95. Hunter, B. A., & Johnson, M. S. (1982). Food chain relationships of copper and cadmium in contaminated grassland ecosystems. Oikos, 38, 108–117.CrossRefGoogle Scholar
  96. Hunter, B. A., Johnson, M. S., & Thompson, D. J. (1987). Ecotoxicology of copper and cadmium in a contaminated grassland ecosystem. Journal of Applied Ecology, 24, 601–614.CrossRefGoogle Scholar
  97. Idris, R., Trifonova, R., Puschenreiter, M., Wenzel, W. W., & Sessitsch, A. (2004). Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Applied and Environmental Microbiology, 70, 2667–2677.CrossRefGoogle Scholar
  98. Jabeen, R., Ahmad, A., & Iqbal, M. (2009). Phytoremediation of heavy metals: physiological and molecular mechanisms. Botanical Review, 75, 339–364.CrossRefGoogle Scholar
  99. Janssens, T. K. S., Roelofs, D., & van Straalen, N. M. (2009). Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Science, 16, 3–18.CrossRefGoogle Scholar
  100. Järup, L. (2003). Hazards of heavy metal contamination. British Medical Bulletin, 68, 167–182.CrossRefGoogle Scholar
  101. Javied, S., Mehmood, T., Chaudhry, M. M., Tufail, M., & Irfan, N. (2009). Heavy metal pollution from phosphate rock used for the production of fertilizer in Pakistan. Microchemical Journal, 91, 94–99.CrossRefGoogle Scholar
  102. Jiao, W., Chen, W., Chang, A. C., & Page, A. L. (2012). Environmental risks of trace elements associated with long-term phosphate fertilizers applications: a review. Environmental Pollution, 168, 44–53.CrossRefGoogle Scholar
  103. Jin, T., Nordberg, M., Frech, W., Dumont, X., Bernard, A., Ye, T. T., Kong, Q., Wang, Z., Li, P., Lundstrom, N. G., Li, Y., & Nordberg, G. F. (2002). Cadmium biomonitoring and renal dysfunction among a population environmentally exposed to cadmium from smelting in China (ChinaCad). BioMetals, 15, 397–410.CrossRefGoogle Scholar
  104. Kabata-Pendias, A., & Pendias, H. (2001). Trace elements in soils and plants (3rd ed.). Boca Raton: CRC.Google Scholar
  105. Khan, A. T., Thompson, S. J., & Mielke, H. W. (1995). Lead and mercury levels in raccoons from Macon County, Alabama. Bulletin of Environmental Contamination and Toxicology, 54, 812–816.Google Scholar
  106. Khan, S., Cao, Q., Zheng, Y. M., Huang, Y. Z., & Zhu, Y. G. (2008). Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environmental Pollution, 152, 686–692.CrossRefGoogle Scholar
  107. Kelessidis, A., & Stasinakis, A. S. (2012). Comparative study of the methods used for treatment and final disposal of sewage sludge in European countries. Waste Management, 32, 1186–1195.CrossRefGoogle Scholar
  108. Kothe, E., & Büchel, G. (2014). Umbrella: using microbes for the regulation of heavy metal mobility at ecosystem and landscape scale. Environmental Science and Pollution Research, 21, 6761–6764.CrossRefGoogle Scholar
  109. Kramarova, M., Massanyi, P., Slamecka, J., Tataruch, F., Jancova, A., Gasparik, J., Fabis, M., Kovacik, J., Toman, R., Galova, J., & Jurcik, R. (2005). Distribution of cadmium and lead in liver and kidney, of some wild animals in Slovakia. Journal of Environmental Science and Health, Part A: Toxic/Hazardous Substances & Environmental Engineering, 40, 593–600.CrossRefGoogle Scholar
  110. Krämer, U. (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology, 61, 517–534.CrossRefGoogle Scholar
  111. Komarnicki, G. J. K. (2000). Tissue, sex and age specific accumulation of heavy metals (Zn, Cu, Pb, Cd) by populations of the mole (Talpa europaea L.) in a central urban area. Chemosphere, 41, 1593–1602.CrossRefGoogle Scholar
  112. Kools, S. A. E., Boivin, M. Y., Van Der Wurff, A. W. G., Berg, M. P., van Gestel, C. A. M., & Van Straalen, N. M. (2009). Assessment of structure and function in metal polluted grasslands using terrestrial model ecosystems. Ecotoxicology and Environmental Safety, 72, 51–59.CrossRefGoogle Scholar
  113. Kupper, H., & Leitenmaier, B. (2011). Cadmium-accumulating plants. In A. Sigel, H. Sigel, & R. K. O. Sigel (Eds.), Cadmium: from toxicity to essentiality (pp. 373–393). New York: Springer.Google Scholar
  114. Langdon, C. J., Piearce, T. G., Meharg, A. A., & Semple, K. T. (2003). Interactions between earthworms and arsenic in the soil environment: a review. Environmental Pollution, 124, 361–373.CrossRefGoogle Scholar
  115. Lee, I.-S., Kim, O. K., Chang, Y.-Y., Bae, B., Kim, H. H., & Baek, K. H. (2002). Heavy metal concentration and enzyme activities in soil from a contaminated Korean shooting range. Journal of Bioscience and Bioengineering, 94, 406–411.CrossRefGoogle Scholar
  116. Lopes, P. A., Viegas-Crespo, A. M., Nunes, A. C., Pinheiro, T., Marques, C., Santos, M. C., & Mathias, M. L. (2002). Influence of age, sex, and sexual activity on trace element levels and antioxidant enzyme activities in field mice (Apodemus sylvaticus and Mus pretus). Biological Trace Element Research, 85, 227–239.CrossRefGoogle Scholar
  117. Lord, C. G., Gaines, K. F., Boring, C. S., Brisbin, I. L., Gochfeld, M., & Burger, J. (2002). Raccoon (Procyon lotor) as a bioindicator of mercury contamination at the U.S. Department of Energy’s Savannah River site. Archives of Environmental Contamination and Toxicology, 43, 356–363.CrossRefGoogle Scholar
  118. Lugon-Moulin, N., Ryan, L., Donini, P., & Rossi, L. (2006). Cadmium content of phosphate fertilizers used for tobacco production. Agronomy for Sustainable Development, 26, 151–155.CrossRefGoogle Scholar
  119. Luo, L., Ma, Y., Zhang, S., Wei, D., & Zhu, Y. G. (2009). An inventory of trace element inputs to agricultural soils in China. Journal of Environmental Management, 90, 2524–2530.CrossRefGoogle Scholar
  120. Ma, W., Denneman, W., & Faber, J. (1991). Hazardous exposure of ground-living small mammals to cadmium, and lead in contaminated terrestrial ecosystems. Archives of Environmental Contamination and Toxicology, 20, 266–270.CrossRefGoogle Scholar
  121. Maestri, E., Marmiroli, M., Visioli, G., & Marmiroli, N. (2010). Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environmental and Experimental Botany, 68, 1–13.CrossRefGoogle Scholar
  122. Mahajan, V. E., Yadav, R. R., Dakshinkar, N. P., Dhoot, V. M., Bhojane, G. R., Naik, M. K., Shrivastava, P., Naoghare, P. K., & Krishnamurthi, K. (2012). Influence of mercury from fly ash on cattle reared nearby thermal power plant. Environmental Monitoring and Assessment, 184, 7365–7372.CrossRefGoogle Scholar
  123. Mann, R. M., Vijver, M. G., & Peijnenburg, W. J. G. M. (2011). Metals and metalloids in terrestrial systems: Bioaccumulation, biomagnification and subsequent adverse effects. In F. Sánchez-Bayo, P. J. van den Brink, & R. M. Mann (Eds.), Ecological impacts of toxic chemicals (pp. 43–62). Sharjah: Bentham.Google Scholar
  124. Marschner, P. (2012). Marschner’s mineral nutrition of higher plants (3rd ed.). London: Academic.Google Scholar
  125. Martens, S. N., & Boyd, R. S. (1994). The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia, 98, 379–384.CrossRefGoogle Scholar
  126. Martens, S. N., & Boyd, R. S. (2002). The defensive role of Ni hyperaccumulation by plants: a field experiment. American Journal of Botany, 89, 998–1003.CrossRefGoogle Scholar
  127. Mathews, S., Ma, L. Q., Rathinasabapathi, C., & Stamps, R. H. (2009). Arsenic reduced scale-insect infestation on arsenic hyperaccumulator Pteris vittata L. Environmental and Experimental Botany, 65, 282–286.CrossRefGoogle Scholar
  128. Matsubara, M., & Itoh, T. (2006). The present situation and future issues on beneficial use of sewage sludge. Saisei to riyo (Association for Utilization of Sewage Sludge), 29, 19–27.Google Scholar
  129. McClellan, K., & Halden, R. U. (2010). Pharmaceuticals and personal care products in archived US biosolids from the 2001 EPA national sewage sludge survey. Water Research, 44, 658–668.CrossRefGoogle Scholar
  130. Meier, S., Borie, F., Bolan, N., & Cornejo, P. (2012). Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Critical Reviews in Environmental Science and Technology, 42, 741–775.CrossRefGoogle Scholar
  131. Meindl, G. A., & Ashman, T.-L. (2013). The effects of aluminum and nickel in nectar on the foraging behavior of bumblebees. Environmental Pollution, 177, 78–81.CrossRefGoogle Scholar
  132. Meindl, G. A., Bain, D. J., & Ashman, T.-L. (2014). Nickel accumulation in leaves, floral organs and rewards varies by serpentine soil affinity. AoB Plants. doi: 10.1093/aobpla/plu036.Google Scholar
  133. Menzies, N. W., Donn, M. J., & Kopittke, P. M. (2007). Evaluation of extractants for estimation of the phytoavailable trace metals in soils. Environmental Pollution, 145, 121–130.CrossRefGoogle Scholar
  134. Mertens, J., Luyssaert, S., Verbeeren, S., Vervaeke, P., & Lust, N. (2001). Metal concentrations in small mammals and willow leaves on disposal facilities for dredged material. Environmental Pollution, 115, 17–22.CrossRefGoogle Scholar
  135. Mesjasz-Przybylowicz, J., & Przybylowicz, W. J. (2001). Phytophagous insects associated with the Ni-hyperaccumulating plant Berkheya coddii (Asteraceae) in Mpumalanga, South Africa. South African Journal of Science, 97, 596–598.Google Scholar
  136. Migula, P., Przybylowicz, W. J., Nakonieczny, M., Augustyniak, M., Tarnawska, M., & Mesjasz-Przybylowicz, J. (2011). Micro-PIXE studies of Ni-elimination strategies in representatives of two families of beetles feeding on Ni-hyperaccumulating plant Berkheya coddii. X-Ray Spectrometry, 40, 194–197.CrossRefGoogle Scholar
  137. Miranda, M., Benedito, J. L., Blanco-Penedo, I., Lopez-Lamas, C., Merino, A., & Lopez-Alonso, M. (2009). Metal accumulation in cattle raised in a serpentine-soil area: relationship between metal concentrations in soil, forage and animal tissues. Journal of Trace Elements in Medicine and Biology, 23, 231–238.CrossRefGoogle Scholar
  138. Miranda, M., López Alonso, M., Castillo, C., Hernández, J., & Benedito, J. L. (2005). Effects of moderate pollution on toxic and trace metal levels in calves from a polluted area of northern Spain. Environment International, 31, 543–548.CrossRefGoogle Scholar
  139. Mogren, C. L., & Trumble, J. T. (2010). The impacts of metals and metalloids on insect behavior. Entomologia Experimentalis et Applicata, 135, 1–17.CrossRefGoogle Scholar
  140. Moriarty, M. M., Koch, I., & Reimer, K. J. (2012). Arsenic speciation, distribution and bioaccessibility in shrews and their food. Archives of Environmental Contamination and Toxicology, 62, 529–538.CrossRefGoogle Scholar
  141. Mortvedt, J. J. (1996). Heavy metal contaminants in inorganic and organic fertilizers. Fertilizer Research, 43, 55–61.CrossRefGoogle Scholar
  142. Muchuweti, M., Birkett, J. W., Chinyanga, E., Zvauya, R., Scrimshaw, M. D., & Lester, J. N. (2006). Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agriculture, Ecosystems & Environment, 112, 41–48.CrossRefGoogle Scholar
  143. Nica, D. V., Bura, M., Gergen, I., Harmanescu, M., & Bordean, D. (2012). Bioaccumulative and conchological assessment of heavy metal transfer in a soil-plant-snail food chain. Chemistry Central Journal, 6, 1–15.CrossRefGoogle Scholar
  144. Nicholson, F. A., Smith, S. R., Alloway, B. J., Carlton-Smith, C., & Chambers, B. J. (2003). An inventory of heavy metals inputs to agricultural soils in England and Wales. Science of the Total Environment, 311, 205–219.CrossRefGoogle Scholar
  145. Neilson, S., & Rajakaruna, N. (2012). Roles of rhizospheric processes and plant physiology in phytoremediation of contaminated sites using oilseed Brassicas. In N. A. Anjum, I. Ahmad, M. E. Pereira, A. C. Duarte, S. Umar, & N. A. Khan (Eds.), The plant family brassicaceae: contribution towards phytoremediation. Environmental pollution book series (Vol. 21, pp. 313–330). Dordrecht: Springer.CrossRefGoogle Scholar
  146. Neilson, S., & Rajakaruna, N. (2014). Phytoremediation of agricultural soils: using plants to clean metal-contaminated arable lands. In A. A. Ansari, S. S. Gill, & G. R. Lanza (Eds.), Phytoremediation: management of environmental contaminants (pp. 159–168). Dordrecht: Springer.Google Scholar
  147. Nordberg, G. F., Jin, T., Kong, Q., Ye, T., Cai, S., & Wang, Z. (1997). Biological monitoring of cadmium exposure and renal effects in a population group residing in a polluted area in China. Science of the Total Environment, 199, 111–114.CrossRefGoogle Scholar
  148. Noret, N., Josens, G., Escarre, J., Lefevre, C., Panichelli, S., & Meerts, P. (2007). Development of Issoria lathonia (Lepidoptera: Nymphalidae) on zinc-accumulating and nonaccumulating Viola species (Violaceae). Environmental Toxicology and Chemistry, 26, 565–571.CrossRefGoogle Scholar
  149. Notten, M. J. M., Oosthoek, A. J. P., Rozema, J., & Aerts, R. (2006). Heavy metal pollution affects consumption of landsnail Cepaea nemoralis fed on naturally polluted Urtica dioica leaves. Ecotoxicology, 15, 295–304.CrossRefGoogle Scholar
  150. Notten, M. J. M., Walraven, N., Beets, C. J., Vroon, P., Rozema, J., & Aerts, R. (2008). Investigating the origin of Pb pollution in a terrestrial soil-plant-snail food chain by means of Pb isotope ratios. Applied Geochemistry, 23, 1581–1593.CrossRefGoogle Scholar
  151. Nziguheba, G., & Smolders, E. (2008). Inputs of trace elements in agricultural soils via phosphate fertilizers in European countries. Science of the Total Environment, 390, 53–57.CrossRefGoogle Scholar
  152. O’Dell, R. E., & Rajakaruna, N. (2011). Intraspecific variation, adaptation, and evolution. In S. H. Harrison & N. Rajakaruna (Eds.), Serpentine: the evolution and ecology of a model system (pp. 97–137). Berkeley: University of California Press.Google Scholar
  153. Oken, E., Wright, R. O., Kleinman, K. P., Bellinger, D., Amarasiriwardena, C. J., Hu, H., Rich-Edwards, J. W., & Gillman, M. W. (2005). Maternal fish consumption, hair mercury, and infant cognition in a U.S. cohort. Environmental Health Perspectives, 113, 1376–1380.CrossRefGoogle Scholar
  154. Otero, N., Vitoria, L., Soler, A., & Canals, A. (2005). Fertiliser characterisation: major, trace and rare earth elements. Applied Geochemistry, 20, 1473–1488.CrossRefGoogle Scholar
  155. Oves, M., Khan, M. S., Zaidi, A., & Ahmad, E. (2012). Soil contamination, nutritive value, and human health risk assessment of heavy metals: an overview. In A. Zaidi, P. A. Wani, & M. S. Khan (Eds.), Toxicity of heavy metals to legumes and bioremediation (pp. 1–27). New York: Springer.CrossRefGoogle Scholar
  156. Pan, J., Plant, J. A., Voulvoulis, N., Oates, C. J., & Ihlenfeld, C. (2010). Cadmium levels in Europe: implications for human health. Environmental Geochemistry and Health, 32, 1–12.CrossRefGoogle Scholar
  157. Pankakoski, E., Koivisto, I., Hyvarinen, H., & Terhivuo, J. (1994). Shrews as indicators of heavy metal pollution. Carnegie Museum of Natural History Special Publication, 18, 137–149.Google Scholar
  158. Patrashkov, S. A., Petukhov, V. L., Korotkevich, O. S., & Petukhov, I. V. (2003). Content of heavy metals in the hair. Journal de Physique IV France, 107, 1025–1027.CrossRefGoogle Scholar
  159. Pennanen, T., Perkiömäki, J., Kiikilä, O., Vanhala, P., Neuhoven, S., & Fritze, H. (1998). Prolonged, simulated acid rain and heavy metal deposition: separated and combined effects on forest soil microbial community structure. FEMS Microbiology Ecology, 27, 291–300.CrossRefGoogle Scholar
  160. Peralta-Videa, J. R., Lopez, M. L., Narayan, M., Saupe, G., & Gardea-Torresdey, J. (2009). The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. The International Journal of Biochemistry & Cell Biology, 41, 1665–1677.CrossRefGoogle Scholar
  161. Pérez-de-Mora, A., Burgos, P., Madejón, E., Cabrera, F., Jaeckel, P., & Schloter, M. (2006). Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biology & Biochemistry, 38, 327–341.CrossRefGoogle Scholar
  162. Peterson, L. R., Trivett, V., Baker, A. J. M., Aguiar, C., & Pollard, A. J. (2003). Spread of metals through an invertebrate food chain as influenced by a plant that hyperaccumulates nickel. Chemoecology, 13, 103–108.CrossRefGoogle Scholar
  163. Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.CrossRefGoogle Scholar
  164. Phillips, C. J. C., & Tudoreanu, L. (2011). A model of cadmium in the liver and kidney of sheep derived from soil and dietary characteristics. Journal of the Science of Food and Agriculture, 91, 370–376.CrossRefGoogle Scholar
  165. Pokorny, B., & Ribaric-Lasnik, C. (2002). Seasonal variability of mercury and heavy metals in roe deer. Environmental Pollution, 117, 35–46.CrossRefGoogle Scholar
  166. Pollard, A. J., Reeves, R. D., & Baker, A. J. M. (2014). Facultative hyperaccumulation of heavy metals and metalloids. Plant Science, 217, 8–17.CrossRefGoogle Scholar
  167. Pragst, F., & Balikova, M. (2006). State of the art in hair analysis for detection of drug and alcohol abuse. Clinica Chimica Acta, 370, 17–49.CrossRefGoogle Scholar
  168. Prosi, F., Storch, V., & Janssen, H. H. (1983). Small cells in the midgut glands of terrestrial Isopoda: sites of heavy metal accumulation. Zoomorphology, 102, 53–64.CrossRefGoogle Scholar
  169. Pruvot, C., Douay, F., Hervé, F., & Waterlot, C. (2006). Heavy metals in soil, crops and grass as a source of human exposure in the former mining areas. Journal of Soils and Sediments, 6, 215–220.CrossRefGoogle Scholar
  170. Przybylowicz, W. J., Mesjasz-Przybylowicz, J., Migula, P., Glowacka, E., Nakonieczny, M., & Augustyniak, M. (2003). Functional analysis of metals distribution in organs of the beetle Chrysolina pardalina exposed to excess of nickel by Micro-PIXE. Nuclear Instruments and Methods in Physics Research B, 210, 343–348.CrossRefGoogle Scholar
  171. Quinn, C. F., Prins, C. N., Freeman, J. L., Gross, A. M., Hantzis, L. J., Reynolds, R. J. B., Yang, S., Covey, P. A., Bañuelos, G. S., Pickering, I. J., Fakra, S. C., Marcus, M. A., Arathi, H. S., & Pilon-Smits, E. A. H. (2011). Selenium accumulation in flowers and its effects on pollination. New Phytologist, 192, 727–737.CrossRefGoogle Scholar
  172. Rajakaruna, N., & Boyd, R. S. (2008). Edaphic Factor. In S. E. Jorgensen & B. D. Fath (Eds.), General ecology: encyclopedia of ecology (2nd ed., pp. 1201–1207). Amsterdam: Elsevier Science.CrossRefGoogle Scholar
  173. Rajakaruna, N., Boyd, R. S., & Harris, T. B. (Eds.). (2014). Plant ecology and evolution in harsh environments. Hauppauge: Nova.Google Scholar
  174. Rajakaruna, N., Tompkins, K. M., & Pavicevic, P. G. (2006). Phytoremediation: an affordable green technology for the clean-up of metal contaminated sites in Sri Lanka. Ceylon Journal of Science, 35, 25–39.Google Scholar
  175. Rashed, M., & Soltan, M. (2005). Animal hair as biological indicator for heavy metal pollution in urban and rural areas. Environmental Monitoring and Assessment, 110, 41–53.CrossRefGoogle Scholar
  176. Rathinasabapathi, B., Rangasamy, M., Froeba, J., Cherry, R. H., McAuslane, H. J., Capinera, J. L., Srivastava, M., & Ma, L. Q. (2007). Arsenic hyperaccumulation in the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory. New Phytologist, 175, 363–369.CrossRefGoogle Scholar
  177. Rattan, R. K., Datta, S. P., Chhonkar, P. K., Suribabu, K., & Singh, A. K. (2005). Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater—a case study. Agriculture, Ecosystems & Environment, 109, 310–322.CrossRefGoogle Scholar
  178. Reeves, R. D., Brooks, R. R., & Macfarlane, R. M. (1981). Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae). American Journal of Botany, 68, 708–712.CrossRefGoogle Scholar
  179. Reglero, M. M., Monsalve-González, L., Taggart, M. A., & Mateo, R. (2008). Transfer of metals to plants and red deer in an old lead mining area in Spain. Science of the Total Environment, 406, 287–297.CrossRefGoogle Scholar
  180. Reglero, M. M., Taggart, M. A., 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. Environmental Pollution, 157, 1388–1395.CrossRefGoogle Scholar
  181. Roberts, R. D., & Johnson, M. S. (1978). Dispersal of heavy metals from abandoned mine workings and their transference through terrestrial food chains. Environmental Pollution, 16, 293–310.CrossRefGoogle Scholar
  182. Roggeman, S., van den Brink, N., Van Praet, N., Blust, R., & Bervoets, L. (2013). Metal exposure and accumulation patterns in free-range cows (Bos taurus) in a contaminated natural area: Influence of spatial and social behavior. Environmental Pollution, 172, 186–199.CrossRefGoogle Scholar
  183. Rogival, D., Scheirs, J., & Blust, R. (2007). Transfer and accumulation of metals in a soil-diet-wood mouse food chain along a metal pollution gradient. Environmental Pollution, 145, 516–528.CrossRefGoogle Scholar
  184. Rosen, G. D., & Roberts, P. A. (1996). Comprehensive survey of the response of growing pigs to supplementary copper in feed. London: Field Investigations and Nutrition Service Ltd.Google Scholar
  185. Ryan, J. A., Pahren, H. R., & Lucas, J. B. (1982). Controlling cadmium in the human food chain: a review and rationale based on health effects. Environmental Research, 28, 251–302.CrossRefGoogle Scholar
  186. Sahoo, P. K., & Kim, K. (2013). A review of the arsenic concentration in paddy rice from the perspective of geoscience. Geosciences Journal, 17, 107–122.CrossRefGoogle Scholar
  187. Sample, B. E., Schlekat, C., Spurgeon, D. J., Menzie, C., Rauscher, J., & Adams, B. (2014). Recommendations to improve wildlife exposure estimation for development of soil screening and cleanup values. Integrated Environmental Assessment and Management, 10, 372–387.CrossRefGoogle Scholar
  188. Sánchez, M. L. (Ed.). (2008). Causes and effects of heavy metal pollution. New York: Nova.Google Scholar
  189. Sánchez-Chardi, A., & Nadal, J. (2007). Bioaccumulation of metals and effects of landfill pollution in small mammals. Part I. The greater white-toothed shrew, Crocidura russula. Chemosphere, 68, 703–711.CrossRefGoogle Scholar
  190. Sánchez-Chardi, A., Penarroja-Matutano, C., Ribeiro, C. A. O., & Nadal, J. (2007a). Bioaccumulation of metals and effects of a landfill in small mammals. Part II. The wood mouse, Apodemus sylvaticus. Chemosphere, 70, 101–109.CrossRefGoogle Scholar
  191. Sánchez-Chardi, A., López-Fuster, M. J., & Nadal, J. (2007b). Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): Sex- and age-dependent variation. Environmental Pollution, 145, 7–14.CrossRefGoogle Scholar
  192. Santhiya, D., & Ting, Y. P. (2005). Bioleaching of spent refinery processing catalyst using Aspergillus niger with high-yield oxalic acid. Journal of Biotechnology, 116, 171–184.CrossRefGoogle Scholar
  193. Scheirs, J., De Coen, A., Covaci, A., Beernaert, J., Kayawe, V. M., Caturla, M., De Wolf, H., Baert, P., Van Oostveldt, P., Verhagen, R., Blust, R., & De Coen, W. (2006a). Genotoxicity in wood mice (Apodemus sylvaticus) along a pollution gradient: exposure-, age-, and gender-related effects. Environmental Toxicology and Chemistry, 25, 2154–2162.CrossRefGoogle Scholar
  194. Scheirs, J., Vandevyvere, I., Wollaert, K., Blust, R., & Bruyn, L. D. (2006b). Plant-mediated effects of heavy metal pollution on host choice of a grass miner. Environmental Pollution, 143, 138–145.CrossRefGoogle Scholar
  195. Schmidt, T., & Schlegel, H. G. (1989). Nickel and cobalt resistance of various bacteria isolated from soil and highly polluted domestic and industrial wastes. FEMS Microbiology Ecology, 62, 315–328.CrossRefGoogle Scholar
  196. Scott, C. A., Faruqui, N. I., & Raschid-Sally, L. (2004). Wastewater use in irrigated agriculture: management challenges in developing countries. In C. A. Scott, N. I. Faruqui, & L. Raschid-Sally (Eds.), Wastewater use in irrigated agriculture (pp. 1–10). Oxfordshire: CABI.Google Scholar
  197. Silver, S., & Phung, L. T. (2009). Heavy metals, bacterial resistance. In M. Schaechter (Ed.), Encyclopedia of microbiology (pp. 220–227). Oxford: Elsevier.CrossRefGoogle Scholar
  198. Smith, G. J., & Rongstad, O. J. (1982). Small mammal heavy metal concentrations from mined and controlled sites. Environmental Pollution, 28, 121–134.CrossRefGoogle Scholar
  199. Smith, K. S., Balistrieri, L. S., & Todd, A. S. (2014). Using biotic ligand models to predict metal toxicity in mineralized systems. Applied Geochemistry. doi: 10.1016/j.apgeochem.2014.07.005.Google Scholar
  200. Spears, J. W., Harvey, R. W., & Samsell, L. J. (1986). Effects of dietary nickel and protein on growth, nitrogen metabolism and tissue concentrations of nickel, iron, zinc, manganese and copper in calves. Journal of Nutrition, 116, 1873–82.Google Scholar
  201. Stankovic, S., Kalaba, P., & Stankovic, A. R. (2014). Biota as toxic metal indicators. Environmental Chemistry Letters, 12, 63–84.CrossRefGoogle Scholar
  202. Strauss, S. Y., & Boyd, R. S. (2011). Herbivory and other cross-kingdom interactions on harsh soils. In S. H. Harrison & N. Rajakaruna (Eds.), Serpentine: the evolution and ecology of a model system (pp. 181–199). Berkeley: University of California Press.Google Scholar
  203. Street, R. A. (2012). Heavy metals in medicinal plant products: an African perspective. South African Journal of Botany, 82, 67–74.CrossRefGoogle Scholar
  204. Sun, H., Dang, S., Xia, Q., Tang, W., & Zhang, G. (2011). The effect of dietary nickel on the immune responses of Spodoptera litura Fabricius larvae. Journal of Insect Physiology, 57, 954–961.CrossRefGoogle Scholar
  205. Swarup, D., & Dwivedi, S. K. (2002). Environmental pollution and effects of lead and fluoride on animal health. New Delhi: Indian Council of Agricultural Research.Google Scholar
  206. Tang, Y.-T., Deng, T.-H.-B., Wu, Q.-H., Wang, S.-Z., Qiu, R.-L., Wei, Z.-B., Guo, X.-F., Wu, Q.-T., Lei, M., Chen, T.-B., Echevarria, G., Sterckeman, T., Simonnot, M. O., & Morel, J. L. (2012). Designing cropping systems for metal-contaminated sites: a review. Pedosphere, 22, 470–488.CrossRefGoogle Scholar
  207. Tête, N., Durfort, M., Rieffel, D., Scheifler, R., & Sánchez-Chardi, A. (2014). Histopathology related to cadmium and lead bioaccumulation in chronically exposed wood mice, Apodemus sylvaticus, around a former smelter. Science of the Total Environment, 481, 167–177.CrossRefGoogle Scholar
  208. Tsao, D.T. (Ed.). (2003). Phytoremediation, advances in biochemical engineering/ biotechnology (Vol 78). Berlin/Heidelberg: Springer.Google Scholar
  209. Unterbrunner, R., Puschenreiter, M., Sommer, P., Wieshammer, G., Tlustoš, P., Zupan, M., & Wenzel, W. W. (2007). Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environmental Pollution, 148, 107–114.CrossRefGoogle Scholar
  210. Utmazian, M. N. D. S., Wieshammer, G., Vega, R., & Wenzel, W. W. (2007). Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environmental Pollution, 148, 155–165.CrossRefGoogle Scholar
  211. van den Brink, N., Lammertsma, D., Dimmers, W., Boerwinkel, M. C., & van der Hout, A. (2010). Effects of soil properties on food web accumulation of heavy metals to the wood mouse (Apodemus sylvaticus). Environmental Pollution, 158, 245–251.CrossRefGoogle Scholar
  212. van der Ent, A., Baker, A. J. M., Reeves, R. D., Pollard, A. J., & Schat, H. (2013). Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant and Soil, 362, 319–334.CrossRefGoogle Scholar
  213. van der Fels-Klerx, I., Römkens, P., Franz, E., & van Raamsdonk, L. (2011). Modeling cadmium in the feed chain and cattle organs. Biotechnology, Agronomy, Society and Environment, 15, 53–59.Google Scholar
  214. Van Kauwenbergh, S.J. (2002). Cadmium content of phosphate rocks and fertilizers, International Fertilizer Industry Association (IFA) Technical Conference, Chennai, India, September 2002.Google Scholar
  215. Vargha, B., Ötvös, E., & Tuba, Z. (2002). Investigations on ecological effects of heavy metal pollution in Hungary by moss-dwelling water bears (Tardigrada), as bioindicators. Annals of Agricultural and Environmental Medicine, 9, 141–146.Google Scholar
  216. Veltman, K., Huijbregts, M. A. J., Hamers, T., Wijnhoven, S., & Hendriks, A. J. (2007). Cadmium accumulation in herbivorous and carnivorous small mammals: meta-analysis of field data and validation of the bioaccumulation model optimal modeling for ecotoxicological applications. Environmental Toxicology and Chemistry, 26, 1488–1496.CrossRefGoogle Scholar
  217. Vermeulen, F., Van den Brink, N., 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.CrossRefGoogle Scholar
  218. Vithanage, M., Rajapaksha, A. U., Oze, C., Rajakaruna, N., & Dissanayake, C. B. (2014). Metal release from serpentine soils in Sri Lanka. Environmental and Monitoring Assessment, 186, 3415–3429.CrossRefGoogle Scholar
  219. Wall, M. A., & Boyd, R. S. (2002). Nickel accumulation in serpentine arthropods from the Red Hills, California. Pan-Pacific Entomologist, 78, 168–176.Google Scholar
  220. Wall, M. A., & Boyd, R. S. (2006). Melanotrichus boydi (Hemiptera: Miridae) is a specialist on the nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae). Southwestern Naturalist, 51, 481–489.CrossRefGoogle Scholar
  221. Watanabe, T., Zhang, Z. W., Qu, J. B., Gao, W. P., Jian, Z. K., Shimbo, S., Nakatsuka, H., Matsuda-Inoguchi, N., Higashikawa, K., & Ikeda, M. (2000). Background lead and cadmium exposure of adult women in Xian City and two farming villages in Shaanxi Province, China. Science of the Total Environment, 247, 1–13.CrossRefGoogle Scholar
  222. Wenzel, W. W. (2009). Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant and Soil, 321, 385–408.CrossRefGoogle Scholar
  223. Wenzel, W. W., & Jockwer, F. (1999). Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Environmental Pollution, 104, 145–155.CrossRefGoogle Scholar
  224. Whiting, S. N., Reeves, R. D., Richards, D., Johnson, M. S., Cooke, J. A., Malaisee, F., Paton, A., Smith, J. A. C., Angle, J. S., Chaney, R. L., Ginocchio, R., Jaffré, T., Johns, R., McIntyre, T., Purvis, O. W., Salt, D. E., Schat, H., Zhao, F. J., & Baker, A. J. M. (2004). Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restoration Ecology, 12, 106–116.CrossRefGoogle Scholar
  225. Wijnhoven, S., Leuven, R. S. E. W., van der Velde, G., Jungheim, G., Koelemij, E. I., de Vries, F. T., Eijsackers, H. J. P., & Smits, A. J. M. (2007). Heavy-metal concentrations in small mammals from a diffusely polluted floodplain: importance of species- and location-specific characteristics. Archives of Environmental Contamination and Toxicology, 52, 603–613.CrossRefGoogle Scholar
  226. Wilbur, S. B., Hansen, H., Pohl, H., Colman, J., & McClure, P. (2004). Using the ATSDR guidance manual for the assessment of joint toxic action of chemical mixtures. Environmental Toxicology and Pharmacology, 18, 223–230.CrossRefGoogle Scholar
  227. Wilkinson, J. M., Hill, J., & Phillips, C. J. (2003). The accumulation of potentially-toxic metals by grazing ruminants. The Proceedings of the Nutrition Society, 62, 267–77.CrossRefGoogle Scholar
  228. Williamson, S. D., & Balkwill, K. (2006). Factors determining levels of threat to serpentine endemics. South African Journal of Botany, 72, 619–626.CrossRefGoogle Scholar
  229. Witter, E., Gong, P., Bääth, E., & Marstorp, H. (2000). A study of the structure and metal tolerance of the soil microbial community six years after cessation of sewer sludge applications. Environmental Toxicology and Chemistry, 19, 1983–1991.CrossRefGoogle Scholar
  230. Wittman, R., & Hu, H. (2002). Cadmium exposure and nephropathy in a 28-year old female metals worker. Environmental Health Perspectives, 10, 1261–1266.CrossRefGoogle Scholar
  231. Wright, R. O., Amarasiriwardena, C., Woolf, A. D., Jim, R., & Bellinger, D. C. (2006). Neurophysical correlates of hair arsenic, manganese, and cadmium levels in school-age children residing near a hazardous waste site. Neurotoxicology, 27, 210–216.CrossRefGoogle Scholar
  232. Wuana, R.A., Okieimen, F.E. (2011). Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology, 1–20.Google Scholar
  233. Xiong, J., He, Z., Liu, D., Mahmood, Q., & Yang, X. (2008). The role of bacteria in the heavy metals removal and growth of Sedum alfredii in an aqueous medium. Chemosphere, 70, 489–904.CrossRefGoogle Scholar
  234. Yang, X. E., Jin, X. F., Feng, Y., & Islam, E. (2005). Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. Journal of Integrative Plant Biology, 47, 1025–1035.CrossRefGoogle Scholar
  235. Zhuang, P., McBride, M. B., Xia, H., Li, N., & Li, Z. (2009). Health risk from heavy metals via consumption of food crops in the vicinity of Dabaoshan mine, South China. Science of the Total Environment, 407, 1551–1561.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.College of the AtlanticBar HarborUSA
  2. 2.Department of Biological SciencesAuburn UniversityAuburnUSA
  3. 3.Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa

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