Multi-temporal accumulation and risk assessment of available heavy metals in poultry litter fertilized soils from Rio de Janeiro upland region

  • Cláudio E. T. ParenteEmail author
  • Adan S. Lino
  • Elias R. Arruda Junior
  • Everaldo Zonta
  • Paulo R. Dorneles
  • João Paulo M. Torres
  • Rodrigo O. Meire
  • Olaf Malm


Poultry litter is widely used as fertilizer in soils and can be a relevant source of heavy metals for agricultural environments. In this study, poultry litter fertilization of long-term (< 1–30 years) was evaluated in tropical soils. Our main goal was to investigate the occurrence of temporal variation in the available fraction of heavy metals (Cu, Cr, Zn, Pb, Cd, and Mn) in soils, in addition to their environmental loads through new indexes for risk assessment. The highest mean concentrations in poultry litter were the following: 525 mg kg−1 for Mn, 146 mg kg−1 for Zn, and 94.4 mg kg−1 for Cu. For soils, concentrations were higher for the same heavy metals: Mn (906 mg kg−1), Zn (111 mg kg−1), and Cu (26.3 mg kg−1). Significant accumulation (p < 0.05) in fertilized soils was observed for Cu, Cr, and Zn. The high estimates of poultry litter input based on geological background (LIGB) for Cu, Cr, and Zn coincided with the accumulation observed in soils, confirming the effectiveness of the index. The risk of biogeochemical transfer based on fertilized soils (LIFS) decreased for Cu, Cr, and Zn between 10 and 30 years of soil fertilization. For Mn, a very high LIFS was estimated in all long-term fertilized soils. The proposed indices, based on heavy metal concentration, can be used in risk assessments to guide future studies that analyze other environmental matrices possibly impacted by manure and poultry litter fertilization.


Environmental risk Trace elements Agricultural soils Tropical soils 



Authors are grateful to National Council for Scientific and Technological Development (CNPq) of Brazilian Ministry of Science, Technology, Innovations, and Communications for doctoral scholarship to Cláudio E.T. Parente (153776/2015-3). The authors would like to thank to poultry farmers from SJVRP for their essential contribution to the work.

Funding information

This research was financed with resources from MCTI/CNPq-Universal—01/2016, process 426192/2016-8. OM and PRD have research grants from CNPq (PQ-1A proc. 306703/2014-9 and PQ-2 proc. 306847/2016-7, respectively). This study was also financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Supplementary material

10661_2018_7156_MOESM1_ESM.docx (121 kb)
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  1. Andrade, M. G., Melo, V. F., Souza, L. C. P., Gabardo, J., & Reissmann, C. B. (2009). Heavy metals in soils of a lead mining and metallurgy area. II—Forms and plant availability. R. Bras. Ci. Solo, 33, 1889–1897.CrossRefGoogle Scholar
  2. AOAC - Association of analytical communities (2011). Standard Format and Guidance for AOAC Standard Method Performance Requirement (SMPR) Documents (Version 12.1). 27p. Accessed 1 Oct 2018
  3. APHA - American Public Health Association. (1998). In L. S. Clesceri, A. E. Greenberg, & A. D. Eaton (Eds.), Standard methods for the examination of water and wastewater. American Water Works Association, Water Environment Federation (20th ed. ed.). Baltimore: United Book Press, Inc..Google Scholar
  4. 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
  5. ATSDR - Agency for Toxic Substances and Disease Registry (2004). Toxicological profile for copper. (accessed 21 October 2018).
  6. ATSDR - Agency for Toxic Substances and Disease Registry (2005). Toxicological profile for zinc. (accessed 21 October 2018).
  7. ATSDR - Agency for Toxic Substances and Disease Registry (2012a). Toxicological profile for chromium. (accessed 21 October 2018).
  8. ATSDR - Agency for Toxic Substances and Disease Registry (2012b). Toxicological profile for cadmium. (accessed 21 October 2018).
  9. ATSDR - Agency for Toxic Substances and Disease Registry (2012c). Toxicological profile for manganese. (accessed 21 October 2018).
  10. Azeez, J. O., Adekunle, I. O., Atiku, O. O., Akande, K. B., & Jamiu-Azeez, S. O. (2009). Effect of nine years of animal waste deposition on profile distribution of heavy metals in Abeokuta, south-western Nigeria and its implication for environmental quality. Waste Management, 29, 2582–2586.CrossRefGoogle Scholar
  11. Baker-Austin, C., Wright, M. S., Stepanauskas, R., & McArthur, J. V. (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4), 176–182.CrossRefGoogle Scholar
  12. Bolan, N. S., Adriano, D. C., & Mahimairaja, S. (2004). Distribution and bioavailabilty of trace elements in livestock and poultry manure by-products. Critical Reviews in Environmental Science and Technology, 34, 291–338.CrossRefGoogle Scholar
  13. Bolan, N. S., Szogi, A. A., Chuasavathi, T., Seshadri, B., Rothrock, M. J., Jr., & Panneerselvam, P. (2010). Uses and management of poultry litter. World's Poultry Science Journal, 66, 673–698 (accessed 21 October 2018).CrossRefGoogle Scholar
  14. Cang, L., Wang, Y., Zhou, D., & Dong, Y. (2004). Heavy metals pollution in poultry and livestock feeds and manure under intensive farming in Jiangsu Province, China. Journal of Environmental Sciences, 16(3), 371–374.Google Scholar
  15. Celestina, C., Midwood, J., Sherriff, S., Trengove, S., Hunt, J., Tang, C., Sale, P., & Franks, A. (2018). Crop yield responses to surface and subsoil applications of poultry litter and inorganic fertilizer in south-eastern Australia. Crop & Pasture Science, 69, 303–316.CrossRefGoogle Scholar
  16. Chen, H., Tenga, Y., Lu, S., Wang, Y., & Wang, J. (2015). Contamination features and health risk of soil heavy metals in China. The Science of the Total Environment, 512–513, 143–153.CrossRefGoogle Scholar
  17. Conama n° 420 de 28 de dezembro de 2009 - Conselho Nacional do Meio Ambiente. (accessed 21 October 2018).
  18. Conama no 375 de 29 de agosto de 2006 - Conselho Nacional do Meio Ambiente. (accessed 22 October 2018).
  19. Das, K., Malarvannan, G., Dirtu, A., Dulau, V., Dumont, M., Lepoint, G., Mongin, P., & Covaci, A. (2017). Linking pollutant exposure of humpback whales breeding in the Indian Ocean to their feeding habits and feeding areas off Antarctica. Environmental Pollution, 220, 1090–1099.CrossRefGoogle Scholar
  20. Dorneles, P. R., Lailson-Brito, J., Fernandez, M. A., Vidal, L. G., Barbosa, L. A., Azevedo, A. F., Fragoso, A. B., Torres, J. P., & Malm, O. (2008). Evaluation of cetacean exposure to organotin compounds in Brazilian waters through hepatic total tin concentrations. Environmental Pollution, 156(3), 1268–1276.CrossRefGoogle Scholar
  21. Dourado, F., Arraes, T. C., & Fernandes e Silva, M. (2012). The “Megadesastre” in the mountain region of Rio de Janeiro state—causes, mechanisms of mass movements and spatial allocation of investments for reconstruction post disaster. Anu. Inst. Geociênc. UFRJ, 35(2), 43–54.Google Scholar
  22. Dziubanek, G., Baranowska, R., Ćwieląg-Drabek, M., Spychała, A., Piekut, A., Rusin, M., & Hajok, I. (2017). Cadmium in edible plants from Silesia, Poland, and its implications for health risk in populations. Ecotoxicology and Environmental Safety, 142, 8–13.CrossRefGoogle Scholar
  23. Embrapa (2013). Manual de calagem e adubação do Estado do Rio de Janeiro. Editor técnico, Luiz Rodrigues Freire et al. Brasília, DF. Embrapa; Seropédica, RJ. Editora UFRRJ. 434p.Google Scholar
  24. Fiszman, M., Pfeiffer, W. C., & Lacerda, L. D. (1984). Comparison of methods used for extraction and geochemical distribution of heavy metals in bottom sediments from Sepetiba Bay, RJ. Environmental Technology Letters, 5, 567–575.CrossRefGoogle Scholar
  25. Gerber, P., Opio, C., Steinfeld, H. (2008). Poultry production and the environment—a review. In: O. Thieme, D. Pilling (Eds.) FAO Animal Production and Health Proceedings, No. 9. Rome. FAO - Food and Agriculture Organization of the United Nations. Poultry in the 21st Century: avian influenza and beyond. Proceedings of the International Poultry Conference, held 5–7 November 2007, Bangkok, Thailand. (accessed 17 October 2018).
  26. Gonçalves Jr., A.C., Nacke, H., Schwantes, D., Coelho, G.F. (2014). Heavy metal contamination in Brazilian agricultural soils due to application of fertilizers. Environmental Risk Assessment of Soil Contamination, Dr. Maria C. Hernandez Soriano (Ed.) (accessed 10 September 2018).
  27. Gupta, G., & Charles, S. (1999). Trace elements in soils fertilized with poultry litter. Poultry Science, 78, 1695–1698.CrossRefGoogle Scholar
  28. Han, F. X., Kingery, W. L., Selim, H. M., & Gerard, P. D. (2000). Accumulation of heavy metals in a long-term poultry waste-amended soil. Soil Science, 165(3), 260–268.CrossRefGoogle Scholar
  29. Ho, Y. B., Zakaria, M. P., Latif, P. A., & Saari, N. (2014). Occurrence of veterinary antibiotics and progesterone in broiler manure and agricultural soil in Malaysia. The Science of the Total Environment, 488–489, 261–267.CrossRefGoogle Scholar
  30. IBAMA - Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (2017). Relatórios de comercialização de agrotóxicos. Boletim 2016/Químicos e Bioquímicos/Vendas de ingredientes ativos por UF. (Accessed 28 May 2018).
  31. IEA - Instituto de Economia Agrícola. (2016). Safra 2016/17 Revigora as Vendas do Segmento de Fertilizantes. Análises e Indicadores do Agronegócio, 11(9), 1–6 (accessed 02 April 2018).Google Scholar
  32. IN no 25/2009 – Instrução Normativa n° 25, de 23 de julho de 2009—Normas sobre as especificações e as garantias, as tolerâncias, o registro, a embalagem e a rotulagem dos fertilizantes orgânicos simples, mistos, compostos, organominerais e biofertilizantes destinados à Agricultura (Accessed 28 May 2018).
  33. Jaja, N., Mbila, M., Codling, E. E., Reddy, S. S., & Reddy, C. K. (2013). Trace metal enrichment and distribution in a poultry litter-amended soil under different tillage practices. The Open Agriculture Journal, 7, 88–95.CrossRefGoogle Scholar
  34. Ji, X., Shen, Q., Liu, F., Ma, J., Xu, G., Wang, Y., & Wu, M. (2012). Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai, China. Journal of Hazardous Materials, 235–236, 178–185.CrossRefGoogle Scholar
  35. Jiang, X., Don, R., & Zhao, R. (2011). Meat products and soil pollution caused by livestock and poultry feed additive in Liaoning, China. Journal of Environmental Sciences, 23, S135–S137.CrossRefGoogle Scholar
  36. Karcı, A., & Balcıoğlu, I. A. (2009). Investigation of the tetracycline, sulfonamide, and fluoroquinolone antimicrobial compounds in animal manure and agricultural soils in Turkey. The Science of the Total Environment, 407, 4652–4664.CrossRefGoogle Scholar
  37. 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
  38. Khan, A., Khan, S., Khan, M. A., Qamar, Z., & Waqas, M. (2015). The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environmental Science and Pollution Research International, 22(18), 13772–13799.CrossRefGoogle Scholar
  39. Kowalska, J. B., Mazurek, R., Gasiorek, M., & Zaleski, T. (2018). Pollution indices as useful tools for the comprehensive evaluation of the degree of soil contamination—A review. Environmental Geochemistry and Health, 40, 2395–2420. Scholar
  40. Leclerc, A., & Laurent, A. (2017). Framework for estimating toxic releases from the application of manure on agricultural soil: National release inventories for heavy metals in 2000–2014. The Science of the Total Environment, 590–591, 452–460.CrossRefGoogle Scholar
  41. Li, Z., & Shuman, L. M. (1997). Mobility of Zn, Cd, and Pb in soils as affected by poultry litter extract—I. Leaching in soil columns. Environmental Pollution, 95(2), 219–226.CrossRefGoogle Scholar
  42. Lino, A. S., Galvão, P. M. A., Longo, R. T. L., Azevedo-Silva, C. E., Dorneles, P. R., Torres, J. P. M., & Malm, O. (2016). Metal bioaccumulation in consumed marine bivalves in Southeast Brazilian coast. Journal of Trace Elements in Medicine and Biology, 34, 50–55.CrossRefGoogle Scholar
  43. Mattias, J. L., Ceretta, C. A., Nesi, C. N., Girotto, E., Trentin, E. E., Lourenzi, C. R., & Vieira, R. C. B. (2010). Copper, zinc and manganese in soils of two watersheds in Santa Catarina with intensive use of pig slurry. R. Bras. Ci. Solo, 34, 1445–1454.CrossRefGoogle Scholar
  44. Millaleo, R., Reyes-Díaz, M., Ivanov, A. G., Mora, M. L., & Alberdi, M. (2010). Manganese as essential and toxic element for plants: Transport, accumulation and resistance mechanisms. Journal of Soil Science and Plant Nutrition, 10(4), 476–494.CrossRefGoogle Scholar
  45. Mitra, S. (2003). Sample preparation techniques in analytical chemistry. Chemical Analysis. Hoboken, John Wiley & Sons (accessed 29 January 2018).
  46. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters, 8, 199–216.CrossRefGoogle Scholar
  47. Nicholson, F. A., Chambers, B. J., Williams, J. R., & Unwin, R. J. (1999). Heavy metal contents of livestock feeds and animal manures in England and Wales. Bioresource Technology, 70, 23–31.CrossRefGoogle Scholar
  48. Parente, C. E. T., Azeredo, A., Vollú, R. E., Zonta, E., Azevedo-Silva, C. E., Brito, E. M., Seldin, L., Torres, J. P. M., Meire, R. O., & Malm, O. (2018). Fluoroquinolones in agricultural soils: Multi-temporal variation and risks in Rio de Janeiro upland region. Chemosphere, 219, 409–417.
  49. Ravindran, B., Mupambwa, H. A., Silwana, S., & Mnkeni, P. N. S. (2017). Assessment of nutrient quality, heavy metals and phytotoxic properties of chicken manure on selected commercial vegetable crops. Heliyon, 3, e00493. Scholar
  50. Rehman, Z. U., Khan, S., Shah, M. T., Brusseau, M. L., Khan, S. A., & Mainhagu, J. (2018). Transfer of heavy metals from soils to vegetables and associated human health risk in selected sites in Pakistan. Pedosphere, 28(4), 666–679.CrossRefGoogle Scholar
  51. Shi, Y., Xu, X., Li, Q., Zhang, M., Li, J., Lu, Y., Liang, R., Zheng, X., & Shao, X. (2018). Integrated regional ecological risk assessment of multiple metals in the soils: A case in the region around the Bohai Sea and the Yellow Sea. Environmental Pollution, 242, 288–297.CrossRefGoogle Scholar
  52. Suleiman, N., Ibitoye, E. B., Jimoh, A. A., & Sani, Z. A. (2015). Assessment of heavy metals in chicken feeds available in Sokoto, Nigeria. Sokoto J. Vet. Sci., 13(1), 17–21.Google Scholar
  53. USDA. (1999). Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys (2.ed ed.). Washington: United States Department of Agriculture. Natural Resources Conservation Service. Soil Survey Staff 169p.Google Scholar
  54. US-EPA Part 503 (1994). United States Environmental Protection Agency. A Plain English Guide to the EPA Part 503 Biosolids Rule. EPA/832/R-93/003. 180p.Google Scholar
  55. Violante, A., Cozzolino, V., Perelomov, L., Caporale, A. G., & Pigna, M. (2010). Mobility and biovailability of HM and metalloids in the soil. Journal of Soil Science and Plant Nutrition, 10(3), 268–292.CrossRefGoogle Scholar
  56. Vollú, E., Cotta, S. R., Jurelevicius, D., Leite, D. C., Parente, C. E., Malm, O., Martins, D. C., Resende, A. V., Marriel, I. E., & Seldin, L. (2018). Response of the bacterial communities associated with maize rhizosphere to poultry litter as an organomineral fertilizer. Frontiers in Environmental Science, 6.
  57. Wang, H., Dong, Y., Yang, Y., Toor, G. S., & Zhang, X. (2013). Changes in heavy metal contents in animal feeds and manures in an intensive animal production region of China. Journal of Environmental Sciences, 25(12), 2435–2442.CrossRefGoogle Scholar
  58. Wang, H., Dong, Y., & Wang, H. (2015). Hazardous metals in animal manure and their changes from 1990 to 2010 in China. Toxicological and Environmental Chemistry, 96(9), 1346–1355.CrossRefGoogle Scholar
  59. Williams, C.M. (2013). Poultry waste management in developing countries. In: FAO - Food and Agriculture Organization of the United Nations. Poultry Development Review. 127p. Accessed 21 October 2018.
  60. Wu, S., Peng, S., Zhang, X., Wu, D., Luo, W., Zhang, T., Zhou, S., Yang, G., Wan, H., & Wu, L. (2015). Levels and health risk assessments of heavy metals in urban soils in Dongguan, China. Journal of Geochemical Exploration, 148, 71–78.CrossRefGoogle Scholar
  61. Xiong, X., Yanxia, L., Wei, L., Chunye, L., Wei, H., & Ming, Y. (2010). Copper content in animal manures and potential risk of soil copper pollution with animal manure use in agriculture. Resources, Conservation and Recycling, 54, 985–990.CrossRefGoogle Scholar
  62. Zhang, F., Li, Y., Yang, M., & Li, W. (2012). Content of heavy metals in animal feeds and manures from farms of different scales in Northeast China. International Journal of Environmental Research and Public Health, 9, 2658–2668.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Cláudio E. T. Parente
    • 1
    Email author
  • Adan S. Lino
    • 1
  • Elias R. Arruda Junior
    • 2
  • Everaldo Zonta
    • 3
  • Paulo R. Dorneles
    • 1
  • João Paulo M. Torres
    • 1
  • Rodrigo O. Meire
    • 1
  • Olaf Malm
    • 1
  1. 1.Laboratório de Radioisótopos, Instituto de Biofísica Carlos Chagas FilhoUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Departamento de Análise Geoambiental, Instituto de GeociênciasUniversidade Federal FluminenseNiteróiBrazil
  3. 3.Departamento de SolosUniversidade Federal Rural do Rio de JaneiroRio de JaneiroBrazil

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