Skip to main content

Advertisement

SpringerLink
Log in

Bioaccumulation of cadmium, lead, and zinc in agriculture-based insect food chains

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Globally, the metal concentration in soil is increasing due to different anthropogenic and geogenic factors. These metals are taken up by plants and further transferred in the food chain through different routes. The present study was designed to assess the transfer and bioaccumulation of the heavy metals, cadmium (Cd), lead (Pb), and zinc (Zn), in food chains from soil to berseem plants (Triofolium alexandrinum), to insect herbivores (the grasshopper Ailopus thalassinus and the aphid Sitobion avenae) and to an insect carnivore (the ladybird beetle Coccinella septempunctata). The soil of studied berseem fields were slightly alkaline, silty loam in texture and moderate in organic matter. In soil, the concentration of Zn and Pb were under permissible level while Cd was above the permissible level. The accumulation of metals in T. alexandrinum were found in the order Zn > Cd > Pb. Grasshoppers showed higher accumulation of Pb than of Cd and Zn. In the soil-berseem-aphid-beetle food chain, metal enrichment was recorded. However, aphids did not show bioaccumulation for Cd. Metals accumulation in beetles showed that translocation of Zn, Cd, and Pb was taking place in the third trophic level. Our study highlights the mobility of metals in insect food chains and showed that insect feeding style greatly influenced the bioaccumulation. However, different metals showed variable bioaccumulation rates depending on their toxicity and retention.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ali, H., Naseer, M., & Sajad, M. A. (2012). Phytoremediation of heavy metals by Trifolium alexandrinum. International Journal of Environmental Sciences, 2(3), 1459. https://doi.org/10.6088/ijes.00202030031.

    Article  CAS  Google Scholar 

  • Arnon, D. I., & Stout, P. R. (1939). The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiology, 14(2), 371–375 http://www.jstor.org/stable/4257358.

    Article  CAS  Google Scholar 

  • Balasoiu, C. F., Zagury, G. J., & Deschenes, L. (2001). Partitioning and speciation of chromium, copper, and arsenic in CCA-contaminated soils: influence of soil composition. Science of Total Environment, 280(1–3), 239–255. https://doi.org/10.1016/S0048-9697(01)00833-6.

    Article  CAS  Google Scholar 

  • Behmer, S. T., Lloyd, C. M., Raubenheimer, D., Stewart-Clark, J., Knight, J., Leighton, R. S., et al. (2005). Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Functional Ecology, 19(1), 55–66. https://doi.org/10.1111/j.0269-8463.2005.00943.x.

    Article  Google Scholar 

  • Bhat, S. (2013). Phytoremidation properties and CLA content of berseem (Trifolium alexandrinum). Asian Journal Of Microbiology, Biotechnology And Environmental Sciences, 15(3), 573–577 https://www.researchgate.net/profile/Shanky_Bhat/publication/258228887_Phytoremediation_and_CLA_content_in_Berseem/links/00b495277ab1ba73ee000000.pdf.

    Google Scholar 

  • Bhatti, S. S., Sambyal, V., & Nagpal, A. K. (2016). Heavy metals bioaccumulation in berseem (Trifolium alexandrinum) cultivated in areas under intensive agriculture, Punjab. India. Springerplus, 5(1), 173. https://doi.org/10.1186/s40064-016-1777-5.

    Article  Google Scholar 

  • Bitterli, C., Banuelos, G. S., & Schulin, R. (2010). Use of transfer factors to characterize uptake of selenium by plants. Journal of Geochemical Exploration, 107(2), 206–216. https://doi.org/10.1016/j.gexplo.2010.09.009.

    Article  CAS  Google Scholar 

  • 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. 53–69). Toronto: John Wiley and Sons.

    Google Scholar 

  • Boyd, R. S. (2004). Ecology of metal hyperaccumulation. New Phytologist, 162(3), 563–567.

    Article  Google Scholar 

  • Boyd, R. S. (2007). The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant and Soil, 293(1–2), 153–176.

    Article  CAS  Google Scholar 

  • Cao, H. B., Chen, J. 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(11), 1792–1799. https://doi.org/10.1016/S1001-0742(09)60321-1.

    Article  CAS  Google Scholar 

  • Chaney, R. L., Reeves, P. G., Ryan, J. A., Simmons, R. W., Welch, R. M., & Angle, J. S. (2004). An improved understanding of soil Cd risk to humans and low cost methods to phytoextract Cd from contaminated soils to prevent soil Cd risks. Biometals, 17(5), 549–553. https://doi.org/10.1023/B:BIOM.0000045737.85738.cf.

    Article  CAS  Google Scholar 

  • Cokca, E., & Birand, A. (1993). Determination of cation exchange capacity of clayey soils by the methylene blue test. Geotecnical Testing Journal, 6(4), 518–524. https://doi.org/10.1520/GTJ10291J.

    Article  Google Scholar 

  • Crawford, L. A., Hodkinson, I. D., & Lepp, N. W. (1995). The effects of elevated host-plant cadmium and copper on the performance of the aphid Aphis-Fabae (Homoptera, Aphididae). Journal of Applied Ecology, 32(3), 528–535. https://doi.org/10.2307/2404650.

    Article  CAS  Google Scholar 

  • Dar, M. I., Khan, F. A., Green, I. D., & Naikoo, M. I. (2015). The transfer and fate of Pb from sewage sludge amended soil in a multi-trophic food chain: a comparison with the labile elements Cd and Zn. Environmental Science and Pollution Research, 22(20), 16133–16142. https://doi.org/10.1007/s11356-015-4836-5.

    Article  CAS  Google Scholar 

  • Farooqi, I. S., Jebb, S. A., Langmack, G., Lawrence, E., Cheetham, C. H., Prentice, A. M., Hughes, I. A., McCamish, M. A., & O'Rahilly, S. (1999). Effects of recombinant leptin therapy in a child with congenital leptin deficiency. The New England Journal of Medicine, 341(12), 879–884. https://doi.org/10.1056/NEJM199909163411204.

    Article  CAS  Google Scholar 

  • Ferrer, A., Dixon, A. F. G., & Hemptinne, J. L. (2008). Prey preference of ladybird larvae and its impact on larval mortality, some life-history traits of adults and female fitness. Bulletin of Insectology, 61(1), 5–10.

    Google Scholar 

  • Gall, J. E., Boyd, R. S., & Rajakaruna, N. (2015). Transfer of heavy metals through terrestrial food webs: a review. Environmental Monitoring and Assessment, 187(4), 201. https://doi.org/10.1007/S10661-015-4436-3.

    Article  Google Scholar 

  • Gall, J. E., & Rajakaruna, N. (2013). The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In M. Lang (Ed.), Brassicaceae: characterization, functional genomics and health benefits (pp. 121–148). New York: Nova Science Publisher.

  • Gao, H. H., Zhao, H. Y., Du, C., Deng, M. M., Du, E. X., Hu, Z. Q., et al. (2012). Life table evaluation of survival and reproduction of the aphid, Sitobion avenae, exposed to cadmium. Journal of Insect Science, 12(44), 1–9. https://doi.org/10.1673/031.012.4401.

    Article  Google Scholar 

  • Ghosh, M., & Singh, S. (2005). A review on phytoremediation of heavy metals and utilization of it’s by products. Asian Jounal On Energy And Environment, 6(4), 18.

    Google Scholar 

  • 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(1), 135–141. https://doi.org/10.1016/j.envpol.2009.07.032.

    Article  CAS  Google Scholar 

  • Green, I. D., Merrington, G., & Tibbett, M. (2003). Transfer of cadmium and zinc from sewage sludge amended soil through a plant-aphid system to newly emerged adult ladybirds (Coccinella septempunctata). Agriculture Ecosystems & Environment, 99(1–3), 171–178. https://doi.org/10.1016/S0167-8809(03)00147-6.

    Article  CAS  Google Scholar 

  • Green, I. D., Tibbett, M., & Diaz, A. (2005). Effects of aphid infestation on Cd and Zn concentration in wheat. Agriculture Ecosystems & Environment, 109(1–2), 175–178. https://doi.org/10.1016/j.agee.2005.02.014.

    Article  CAS  Google Scholar 

  • Greenberg, C. H., Crownover, S. H., & Gordon, D. R. (1997). Roadside soils: a corridor for invasion of xeric scrub by nonindigenous plants. Natural Areas Journal, 17(2), 99–109.

    Google Scholar 

  • Greger, M. (1999). Metal availability and bioconcentration in plants. In Heavy metal stress in plants (pp. 1–27). Berlin: Springer. https://doi.org/10.1007/978-3-662-07745-0_1.

  • Grzes, I. M. (2010). Zinc and cadmium regulation efficiency in three ant species originating from a metal pollution gradient. Bulletin of Environmental Contamination and Toxicology, 84(1), 61–65. https://doi.org/10.1007/s00128-009-9893-3.

    Article  CAS  Google Scholar 

  • Heikens, A., Peijnenburg, W. J., & Hendriks, A. J. (2001). Bioaccumulation of heavy metals in terrestrial invertebrates. Environmental Pollution, 113(3), 385–393. https://doi.org/10.1016/S0269-7491(00)00179-2.

    Article  CAS  Google Scholar 

  • Hobbelen, P. H., Koolhaas, J. E., & van Gestel, C. A. (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(2), 639–646. https://doi.org/10.1016/j.envpol.2006.01.019.

    Article  CAS  Google Scholar 

  • Hossain, M. A., Piyatida, P., da Silva, J. A. T., & 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, 1–37. https://doi.org/10.1155/2012/872875.

    Article  CAS  Google Scholar 

  • Huang, J., & Cunningham, S. (1996). Lead phytoextraction: species variation in lead uptake and translocation. New Phytologist, 134(1), 75–84. https://doi.org/10.1111/j.1469-8137.1996.tb01147.x.

    Article  CAS  Google Scholar 

  • Hunter, B. A., Johnson, M. S., & Thompson, D. J. (1987). Ecotoxicology of copper and cadmium in a contaminated grassland ecosystem. II. Invertebrates. Journal of Applied Ecology, 24, 587–599. https://doi.org/10.2307/2403895.

    Article  CAS  Google Scholar 

  • Khan, K., Lu, Y. L., Khan, H., Ishtiaq, M., Khan, S., Waqas, M., et al. (2013). Heavy metals in agricultural soils and crops and their health risks in Swat District, northern Pakistan. Food and Chemical Toxicology, 58, 449–458. https://doi.org/10.1016/j.fct.2013.05.014.

    Article  CAS  Google Scholar 

  • Labandeira, C. C. (1997). Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics, 28(1), 153–193. https://doi.org/10.1146/annurev.ecolsys.28.1.153.

    Article  Google Scholar 

  • Laghari, H. H., Channa, A. D., Solangi, A. A., & Soomro, S. A. (2000). Comparative digestibility of different cuts of berseem (Trifolium alexandrinum) in sheep. Pakistan Journal of Biological Sciences (Pakistan), 3, 1938–1939 http://agris.fao.org/agris-search/search.do?recordID=PK2000000622.

    Article  Google Scholar 

  • Lindqvist, L. (1992). Accumulation of cadmium, copper, and zinc in five species of phytophagous insects. Environmental Entomology, 21(1), 160–163. https://doi.org/10.1093/ee/21.1.160.

    Article  CAS  Google Scholar 

  • López, M. L., Peralta-Videa, J. R., Parsons, J. G., Benitez, T., & Gardea-Torresdey, J. L. (2007). Gibberellic acid, kinetin, and the mixture indole–3-acetic acid–kinetin assisted with EDTA-induced lead hyperaccumulation in alfalfa plants. Environmental Science & Technology, 41(23), 8165–8170. https://doi.org/10.1021/es0714080.

    Article  CAS  Google Scholar 

  • Lucho-Constantino, C. A., Alvarez-Suarez, M., Beltran-Hernandez, R. I., Prieto-Garcia, F., & Poggi-Varaldo, H. M. (2005). A multivariate analysis of the accumulation and fractionation of major and trace elements in agricultural soils in Hidalgo state, Mexico irrigated with raw wastewater. Environmental International, 31(3), 313–323. https://doi.org/10.1016/j.envint.2004.08.002.

    Article  CAS  Google Scholar 

  • Malik, R. N., Husain, S. Z., & Nazir, I. (2010). Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad. Pakistan. Pakistan Journal of Botany, 42(1), 291–301 http://www.pakbs.org/pjbot/PDFs/42(1)/PJB42(1)291.pdf.

    CAS  Google Scholar 

  • Mar, S. S., & Okazaki, M. (2012). Investigation of Cd contents in several phosphate rocks used for the production of fertilizer. Microchemical Journal, 104, 17–21. https://doi.org/10.1016/j.microc.2012.03.020.

    Article  CAS  Google Scholar 

  • Mathews, S., Ma, L. Q., Rathinasabapathi, B., & Stamps, R. H. (2009). Arsenic reduced scale-insect infestation on arsenic hyperaccumulator Pteris vittata L. Environmental and Experimental Botany, 65(2–3), 282–286. https://doi.org/10.1016/j.envexpbot.2008.09.010.

    Article  CAS  Google Scholar 

  • Meindl, G. A., & Ashman, T. L. (2015). Effects of floral metal accumulation on floral visitor communities: Introducing the elemental filter hypothesis. American Journal of Botany, 102(3), 379–389.

    Article  Google Scholar 

  • Migula, P., Przybyłowicz, W. J., Nakonieczny, M., Augustyniak, M., Tarnawska, M., & Mesjasz-Przybyłowicz, 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(3), 194–197. https://doi.org/10.1002/xrs.1310.

    Article  CAS  Google Scholar 

  • Mohammed, A. S., Kapri, A., & Goel, R. (2011). Heavy metal pollution: source, impact, and remedies. In M. Khan, A. Zaidi, R. Goel, & J. Musarrat (Eds.), Biomanagement of metal-contaminated soils (pp. 1–28). Dordrecht: Springer. https://doi.org/10.1007/978-94-007-1914-9_1.

    Chapter  Google Scholar 

  • Muhammad, S., Shah, M. T., & Khan, S. (2011). Heavy metal concentrations in soil and wild plants growing around Pb-Zn sulfide terrain in the Kohistan region, northern Pakistan. Microchemical Journal, 99(1), 67–75. https://doi.org/10.1016/j.microc.2011.03.012.

    Article  CAS  Google Scholar 

  • Naidu, R., Kookana, R. S., Sumner, M. E., Harter, R. D., & Tiller, K. G. (1997). Cadmium sorption and transport in variable charge soils: a review. Journal of Environmental Quality, 26(3), 602–617. https://doi.org/10.2134/jeq1997.00472425002600030004x.

    Article  CAS  Google Scholar 

  • Neilson, S., & Rajakaruna, N. (2015). Phytoremediation of agricultural soils: using plants to clean metal-contaminated arable land. In A. Ansari, S. Gill, R. Gill, G. Lanza, & L. Newman (Eds.), Phytoremediation (pp. 159–168). Cham: Springer.

    Google Scholar 

  • Olaniran, A. O., Balgobind, A., & Pillay, B. (2013). Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. International Journal of Molecular Sciences, 14(5), 10197–10228. https://doi.org/10.3390/ijms140510197.

    Article  CAS  Google Scholar 

  • Ostman, O., Ekbom, B., & Bengtsson, J. (2003). Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecological Economics, 45(1), 149–158. https://doi.org/10.1016/S0921-8009(03)00007-7.

    Article  Google Scholar 

  • 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 Jorurnal Of Biochemistry And Cell Biology, 41(8–9), 1665–1677. https://doi.org/10.1016/j.biocel.2009.03.005.

    Article  CAS  Google Scholar 

  • Perveen, S., Samad, A., Nazif, W., & Shah, S. (2012). Impact of sewage water on vegetables quality with respect to heavy metals in Peshawar Pakistan. Pakistan Journal of Botany, 44(6), 1923–1931 https://www.pakbs.org/pjbot/PDFs/44(6)/15.pdf.

    Google Scholar 

  • Pollard, A. J., Powell, K. D., Harper, F. A., & Smith, J. A. C. (2002). The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Sciences, 21(6), 539–566.

    Article  CAS  Google Scholar 

  • Price, P. W., Rathcke, B. J., & Gentry, D. A. (1974). Lead in terrestrial arthropods: evidence for biological concentration. Environmental Entomology, 3(3), 370–372 https://www.pakbs.org/pjbot/PDFs/44(6)/15.pdf.

    Article  CAS  Google Scholar 

  • Rajakaruna, N. (2009). Serpentinophiles from California and across the world gather in Maine to highlight recent research on soil-biota relations of serpentine outcrops. Fremontia, 37(1), 21–24.

    Google Scholar 

  • Rizwan, M., Siddique, M. T., Ahmed, H., Iqbal, M., & Ziad, T. (2016). Spatial variability of selected physico-chemical properties and macronutrients in the shale and sandstone derived soils. Soil & Environment, 35(1), 12–21.

    CAS  Google Scholar 

  • Roth-Holzapfel, M. (1990). Multi-element analysis of invertebrate animals in a forest ecosystem (Picea abies L). In H. Lieth & B. Markert (Eds.), Element concentration cadasters in ecosystems: methods of assessment and evaluation (pp. 281–295). Weinheim: VCH Publishers.

    Google Scholar 

  • Sabiha-Javied, M.,. 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(1), 94–99. https://doi.org/10.1016/j.microc.2008.08.009.

    Article  CAS  Google Scholar 

  • Sandrin, T. R., & Hoffman, D. R. (2007). Bioremediation of organic and metal co-contaminated environments: Effects of metal toxicity, speciation, and bioavailability on biodegradation. Environmental Bioremediation Technologies, 1, 1–34. https://doi.org/10.1007/978-3-540-34793-4_1.

    Article  Google Scholar 

  • Schmidt, G. H., & Ibrahim, N. M. M. (1994). Heavy-metal content (Hg2+, Cd2+, Pb2+) in various body parts—its impact on cholinesterase activity and binding glycoproteins in the grasshopper Aiolopus thalassinus adults. Ecotoxicology and Environmental Safety, 29(2), 148–164. https://doi.org/10.1016/0147-6513(94)90016-7.

    Article  CAS  Google Scholar 

  • Shuman, L. M. (1999). Organic waste amendments effect on zinc fractions of two soils. Journal of Environmental Quality, 28(5), 1442–1447. https://doi.org/10.2134/jeq1999.00472425002800050008x.

    Article  CAS  Google Scholar 

  • Soomro, F., Sultana, R., Wagan, M. S., Abbasi, A. R., & Solongi, B. K. (2015). Studies on the immature stages of Aiolopus thalassinus thalassinus (Fabricius)(Oedipodinae: Acrididae: Orthoptera). Sindh University Research Journal-SURJ (Science Series), 47(2), 267–274.

    Google Scholar 

  • Sterenborg, I., Vork, N. A., Verkade, S. K., van Gestel, C. A. M., & van Straalen, N. M. (2003). Dietary zinc reduces uptake but not metallothionein binding and elimination of cadmium in the springtail, Orchesella cincta. Environmental Toxicology and Chemistry, 22(5), 1167–1171. https://doi.org/10.1002/etc.5620220528.

    Article  CAS  Google Scholar 

  • Stevens, D. P., McLaughlin, M. J., & Heinrich, T. (2003). Determining toxicity of lead and zinc runoff in soils: salinity effects on metal partitioning and on phytotoxicity. Environmental Toxicology and Chemistry, 22(12), 3017–3024. https://doi.org/10.1897/02-290.

    Article  CAS  Google Scholar 

  • Szyczewski, P., Siepak, J., Niedzielski, P., & Sobczynski, T. (2009). Research on heavy metals in Poland. Polish Journal of Environmental Studies, 18(5), 755–768 http://www.6csnfn.pjoes.com/pdf/18.5/755-768.pdf.

    CAS  Google Scholar 

  • Unterbrunner, R., Puschenreiter, M., Sommer, P., Wieshammer, G., Tlustos, P., Zupan, M., et al. (2007). Heavy metal accumulation in trees growing on contaminated sites in Central Europe. Environmental Pollution, 148(1), 107–114. https://doi.org/10.1016/j.envpol.2006.10.035.

    Article  CAS  Google Scholar 

  • USEPA (2002). Supplemental guidance for developing soil screening levels for superfund sites. Office of Solid Waste and Emergency Response, Washington, D.C. http://www.epa.gov/superfund/health/conmedia/soil/index.htm

  • Violante, A., Cozzolino, V., Perelomov, L., Caporale, A. G., & Pigna, M. (2010). Mobility and bioavailability of heavy metals and metalloids in soil environments. Journal of Soil Science and Plant Nutrition, 10(3), 268–292. https://doi.org/10.4067/S0718-95162010000100005.

    Article  Google Scholar 

  • Walkley, A., & Black, I. A. (1934). An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science, 37(1), 29–38.

    Article  CAS  Google Scholar 

  • War, A. R., Paulraj, M. G., Ahmad, T., Buhroo, A. A., Hussain, B., Ignacimuthu, S., & Sharma, H. C. (2012). Mechanisms of plant defense against insect herbivores. Plant Signal and Behavior, 7(10), 1306–1320. https://doi.org/10.4161/psb.21663.

    Article  Google Scholar 

  • Warchałowska-Śliwa, E., Niklińska, M., Görlich, A., Michailova, P., & Pyza, E. (2005). Heavy metal accumulation, heat shock protein expression and cytogenetic changes in Tetrix tenuicornis (L.) (Tetrigidae, Orthoptera) from polluted areas. Environmental Pollution, 133(2), 373–381. https://doi.org/10.1016/j.envpol.2004.05.013.

    Article  CAS  Google Scholar 

  • Wijnhoven, S., Leuven, R., van der Velde, G., Jungheim, G., Koelemij, E., De Vries, F. T., et al. (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(4), 603–613.

    Article  CAS  Google Scholar 

  • WHO. (1996). Permissible limits of heavy metals in soil and plants. Geneva: World Health Organization). switzerland.

    Google Scholar 

  • Xun, E., Zhang, Y., Zhao, J., & Guo, J. (2017). Translocation of heavy metals from soils into floral organs and rewards of Cucurbita pepo: implications for plant reproductive fitness. Ecotoxicology and Environmental Safety, 145, 235–243.

    Article  CAS  Google Scholar 

  • You, S. J., Yin, Y. J., & Allen, H. E. (1999). Partitioning of organic matter in soils: effects of pH and water/soil ratio. Science of the Total Environment, 227(2–3), 155–160. https://doi.org/10.1016/S0048-9697(99)00024-8.

    Article  CAS  Google Scholar 

  • Zhang, Z. S., Lu, X. G., Wang, Q. C., & Zheng, D. M. (2009). Mercury, cadmium and lead biogeochemistry in the soil-plant-insect system in Huludao City. Bulletin of Environmental Contamination and Toxicology, 83(2), 255–259. https://doi.org/10.1007/s00128-009-9688-6.

    Article  CAS  Google Scholar 

  • Zhuang, P., Zou, H., & Shu, W. (2009). Biotransfer of heavy metals along a soil-plant-insect-chicken food chain: field study. Journal of Environmental Sciences, 21(6), 849–853.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of the Punjab, Lahore, Pakistan

    Abida Butt,  Qurat-ul-Ain, Kanwal Rehman & Muhammad Xaaceph Khan

  2. Department of Zoology, University of Oxford, Oxford, UK

    Thomas Hesselberg

Authors
  1. Abida Butt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qurat-ul-Ain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kanwal Rehman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Xaaceph Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas Hesselberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abida Butt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Butt, A., Qurat-ul-Ain, Rehman, K. et al. Bioaccumulation of cadmium, lead, and zinc in agriculture-based insect food chains. Environ Monit Assess 190, 698 (2018). https://doi.org/10.1007/s10661-018-7051-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-018-7051-2

Keywords

Search

Navigation