Abstract
Lead (Pb) contamination of agroecosystems is a serious issue as Pb is a persistent pollutant that is retained in soil for long, causing toxicities to organisms. This study examines biotransfer of Pb from soils treated with different concentrations of Pb through a broad bean (Vicia faba L.)–aphid (Aphis fabae Scop.)–ladybird (Coccinella transversalis Fabricius) food chain and its consequent inference for natural biological control, the ladybird. The soil was amended with Pb at the rates of 0, 25, 50, 75 and 100 mg kg−1 (w/w). The amount of Pb in plant, aphid and ladybird increased in a dose-dependent manner to Pb contents in the soil. The results showed that Pb biomagnified from soil to root with transfer coefficient always > 1. Biominimization of Pb occurred at the second trophic level in aphids and at the third trophic level in ladybirds as their respective transfer coefficients from shoot to aphid and aphid to ladybird were always < 1. The increased elimination of Pb via aphid excreta (honeydew) and pupal exuviae in a dose-dependent manner suggests that these are possible detoxification mechanisms at two different trophic levels which control Pb bioaccumulation along the food chain. The statistically significant (p ≤ 0.05) decreases in biomass and predation rate of predatory ladybirds at 100 mg kg−1 Pb indicate that high dose of Pb in soil may have sub-lethal effects on ladybirds. Further studies at cellular and sub-cellular levels are needed to further document the potential mechanisms of achieving Pb homeostasis in ladybirds under Pb stress.
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References
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190
Alexander PD, Alloway BJ, Dourado AM (2006) Genotype variations in the accumulation of Cd, Cu, Pb and Zn exhibited by six commonly grown vegetables. Environ Pollut 144:736–745
Allen SE, Grimshaw HM, Rowland AP (1986) Chemical analysis. In: Moore PD, Chapman SB (eds) Methods in plant ecology. Blackwell Scientific Publication, Oxford, pp 285–344
Anjum SA, Ashraf U, Khan I, Tanveer M, Ali M, Hussain I, Wang LC (2016) Chromium and aluminum phytotoxicity in maize: morpho-physiological responses and metal uptake. Clean–Soil Air Water 44:1075–1084
Arias JA, Peralta-Videa JR, Ellzey JT, Ren M, Viveros MN, Gardea-Torresdey JL (2010) Effects of Glomus deserticola inoculation on Prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environ Exp Bot 68:139–148
Awashthi SK (2000) Prevention of food adulteration act no. 37 of 1954. Central and state rules as amended for 1999, 3rd edn. Ashoka Law House, New Delhi
Babin-Fenske J, Anand M (2011) Patterns of insect communities along a stress gradient following decommissioning of a Cu-Ni smelter. Environ Pollut 159:3036–3043
Bai XY, Dong YJ, Wang QH, Xu LL, Kong J, Liu S (2015) Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biol Plant 59:163–170
Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567
Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33
Chaffai R, Koyama H (2011) Heavy metal tolerance in Arabidopsis thaliana. Adv Bot Res 60:1–49
Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z, Cui J (2016) Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul 81:253–264
Crawford LA, Hodkinson ID, Lepp NW (1995) The effects of elevated host-plant Cd and Cu on the performance of the aphid Aphis fabae (Homoptera: Aphididae). J Appl Ecol 32(3):528–535
Dar MI, Khan FA, Green ID, Naikoo MI (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. Environ Sci Pollut Res 22:16133–16142. https://doi.org/10.1007/s11356-015-4836-5
Dar MI, Khan FA, Rehman F (2016) Responses of antioxidative defense system and composition of photosynthetic pigments in Brassica juncea L. upon imidacloprid treatments. ABS J 1(1):3–15
Dar MI, Green ID, Naikoo MI, Khan FA, Ansari AA, Lone MI (2017) Assessment of biotransfer and bioaccumulation of cadmium, lead and zinc from fly ash amended soil in mustard–aphid-beetle food chain. Sci Total Environ 584-585:1221–1229
Darshana JS, Abishek S (2015) Feeding potential of Coccinella transversalis (Fabricius) on aphids. Ind J Entomol 77(2):197–198. https://doi.org/10.5958/0974-8172.2015.00039.5
Devkota B, Schmidt GH (2000) Accumulation of trace metals in food plants and grasshoppers from the Taigetos mountains, Greece. Agric Ecosyst Environ 78:85–91
Dwivedi S, Tripathi RD, Srivastava S, Mishra S, Shukla MK, Tiwari KK, Singh R, Rai UN (2007) Growth performance and biochemical responses of three rice (Oryza sativa L.) cultivars grown in fly-ash amendment soil. Chemosphere 67:140–151
Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187:201. https://doi.org/10.1007/s10661-015-4436-3
Gintenreiter S, Ortel J, Nopp HJ (1993) Bioaccumulation of cadmium, lead, copper and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae: lepidoptera)- a life cycle study. Arch Environ Contam Toxicol 25:55–61
Green ID, 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). Agric Ecosyst Environ 99:171–178
Gupta AK, Sinha S (2009) Growth and metal accumulation response of Vigna radiata L. var PDM54 (mung bean) grown on fly-ash-amended soil: effect on dietary intake. Environ Geochem Health 31:463–473
Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY et al (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479 484
Hakeem KR, Alharby HF, Rehman R (2018) Antioxidative defense mechanism against lead induced phytotoxicity in Fagopyrum kashmirianum. https://doi.org/10.1016/j.Chemosphere.2018.10.131
Hou X, Han H, Cai L, Liu A, Ma X, Zhou C, Wang G, Meng F (2018) Pb stress effects on leaf chlorophyll fluorescence, antioxidative enzyme activities, and organic acid contents of Pogonatherum crinitum seedlings. Flora 240:82–88
Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816
Jackson ML (1958) Soil chemical analysis. Prentice Hall Inc, USA
Jiang W, Liu D (2010) Pb-induced cellular defense system in the root meristematic cells of Allium sativum L. BMC Plant Biol 10:40–40
John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54(6):262–270
Kabata-Pendias A, Pendias H (2011) Trace elements in soils and plants, 4th edn. CRC Press, Boca Raton
Kaur G, Singh HP, Batish DR, Kohli RK (2013) Lead (Pb)-induced biochemical and ultrastructural changes in wheat (Triticum aestivum) roots. Protoplasma 250:53–62
Kazimirova M, Ortel J (2000) Metal accumulation by Ceratitis capitat (Diptera) and transfer to the parasitic wasp Coptera occidentalis (Hymenoptera). Environ Toxicol Chem 19:1822–1829
Khan M, Daud MK, Basharat A, Khan MJ, Azizullah A, Muhammad N, Muhammad N, ur Rehman Z, Zhu SJ (2016) Alleviation of lead-induced physiological, metabolic, and ultramorphological changes in leaves of upland cotton through glutathione. Environ Sci Pollut Res 23:8431–8440
Kopittke PM, Asher CJ, Kopittke RA, Menzies NW (2007) Toxic effects of Pb2+ on growth of cowpea (Vigna unguiculata). Environ Pollut 150(2):280–287
Kumar A, Prasad MNV, Sytar O (2012) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89:1056–1065
Kumar A, Prasad MNV (2015) Lead-induced toxicity and interference in chlorophyll fluorescence in Talinum triangulare grown hydroponically. Photosynthetica 53:66–71
Kumar A, Prasad MNV (2018) Plant-lead interactions: transport, toxicity, tolerance, and detoxification mechanisms. Ecotoxicol Environ Saf 166:401–418
Li Y, Zhou C, Huang M, Luo J, Hou X, Wu P, Ma X (2016) Lead tolerance mechanism in Conyza canadensis: subcellular distribution, ultrastructure, antioxidative defense system, and phytochelatins. J Plant Res 129:251–262
Liao Y, Chien SC, Wang M, Shen Y, Hung P, Das B (2006) Effect of transpiration on Pb uptake by lettuce and on water soluble low molecular weight organic acids in rhizosphere. Chemosphere 65(2):343–351
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428
Liu T, Liu S, Guan H, Ma L, Chen Z, Gu H, Qu LJ (2009) Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb). Environ Exp Bot 67:377–386
Malecka A, Piechalak A, Tomaszewska B (2009) Reactive oxygen species production and antioxidative defense system in pea root tissues treated with lead ions: the whole roots level. Acta Physiol Plant 31:1053–1063
Merrington G, Miller D, McLaughlin MJ, Keller MA (2001) Trophic barriers to fertilizer Cd bioaccumulation through the food chain: a case study using a plant–insect predator pathway. Arch Environ Contam Toxicol 41:151–156
Monferrán MV, Wunderlin DA (2013) Biochemistry of metals/metalloids toward remediation process. In: Gupta DK, Franciscom J, Palma CJM (eds) Trace metal stress in plants. Springer, Berlin, pp 43–72
Nicholson FA, Chambers BJ (2008) Sources and impacts of past, current and future contamination of soil appendix 1: heavy metals SP0547. (Defra science directorate) Department for Environment Food and Rural Affairs, London, UK
Parys E, Wasilewska W, Siedlecka M, Zienkiewicz M, Drożak A, Romanowska E (2014) Metabolic responses to lead of metallicolous and nonmetallicolous populations of Armeria maritima. Arch Environ Contam Toxicol 67:565–577
Pourrut B, Jean S, Silvestre J, Pinelli E (2011) Lead-induced DNA damage in Vicia faba root cells: potential involvement of oxidative stress. Mutat Res /Gene Toxicol Environ Mutagen 726:123–128
Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Gupta DK, Corpas FJ, Palma JM (eds) Trace metal stress in plants. Springer, Berlin, pp 121–148
Probst A, Liu H, Fanjul M, Liao B, Hollande E (2009) Response of Vicia faba L. to metal toxicity on mine tailing substrate: geochemical and morphological changes in leaf and root. Environ Exp Bot 66:297–308
Qiao X, Zheng Z, Zhang L, Wang J, Shi G, Xu X (2015) Lead tolerance mechanism in sterilized seedlings of Potamogeton crispus L.: subcellular distribution, polyamines and proline. Chemosphere 120:179–187
Rehman F, Khan FA, Anis SB (2014) Assessment of aphid infestation levels in some cultivars of mustard with varying defensive traits. Arch Phytopathol Plant Protect 47:1866–1874
Rodriguez E, da Conceição Santos M, Azevedo R, Correia C, Moutinho-Pereira J, Ferreira de Oliveira JMP, Dias MC (2015) Photosynthesis light independent reactions are sensitive biomarkers to monitor lead phytotoxicity in a Pb-tolerant Pisum sativum cultivar. Environ Sci Pollut Res 22:574–585
Rucińska-Sobkowiak R, Nowaczyk G, Krzesłowska M, Rabęda I, Jurga S (2013) Water status and water diffusion transport in lupine roots exposed to lead. Environ Exp Bot 87:100–109
Shaheen SM, Tsadilas CD (2010) Influence of fly ash and sewage sludge application on cadmium and lead sorption by an acidic alfisol. Pedosphere 20:436–445
Shahid M, Dumat C, Pourrut B, Sabir M, Pinelli E (2014) Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J Geochem Explor 144:290–297. https://doi.org/10.1016/j.gexplo.2014.01.003
Shahid M, Dumat C, Silvestre J, Pinelli E (2012) Effect of fulvic acids on lead induced oxidative stress to metal sensitive Vicia faba L. plant. Biol Fertil Soils 48:689–697
Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74(1):78–84
Shu X, Yin L, Zhang Q, Wang W (2012) Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res 19:893–902
Singh RP, Agarwal M (2010) Variations in trace metal accumulation, growth and yield of rice plants grown at different sewage sludge amendment rates. Ecotoxicol Environ Saf 73:632–641
Tsadilas CD, Shaheen SM, Samaras V, Gizas D, Hu Z (2009) Influence of fly ash application on copper and zinc sorption by acidic soil amended with sewage sludge. Commun Soil Sci Plant Anal 40:273–284
Wang CR, Tian Y, Wang XR, Yu HX, Lu XW, Wang C, Wang H (2010) Hormesis effects and implicative application in assessment of lead contaminated soils in roots of Vicia faba seedlings. Chemosphere. 80:965–971. https://doi.org/10.1016/j.chemosphere.2010.05.049
Wang G, SU MY, Chen YH, Lin FF, Luo D, Gao SF (2006) Transfer characteristics of cadmium and lead from soil to the edible parts of six vegetable species in south eastern China. Environ Pollut 144:127–135
Winder L, Merrington G, Green I (1999) The tri-trophic transfer of Zn from the agricultural use of sewage sludge. Sci Total Environ 229:73–81
Yuan H, Zhang Y, Huang S, Yang Y, Gu C (2015) Effects of exogenous glutathione and cysteine on growth, lead accumulation, and tolerance of Iris lactea var. chinensis. Environ Sci Pollut Res 22:2808–2816
Zhang C, Wang X, Ashraf U, Qiu B, Ali S (2017) Transfer of lead (Pb) in the soil- plant- mealybug-ladybird beetle food chain, a comparison between two host plants. Ecotoxicol Environ Saf 143:289–295
Zhou C, Huang M, Li Y, Luo J, Cai LP (2016) Changes in subcellular distribution and antioxidant compounds involved in Pb accumulation and detoxification in Neyraudia reynaudiana. Environ Sci Pollut Res 23:21794–21804
Zhou L, Zhao Y, Wang S, Han S, Liu J (2015) Lead in the soil-mulberry (Morus alba L.) silkworm (Bombyx mori) food chain: translocation and detoxification. Chemosphere 128:171–177
Acknowledgements
Authors are grateful to the chairman, Department of Botany, Aligarh Muslim University, Aligarh, for providing necessary facilities during the research. Dr. Iain Green, Department of Life and Environmental Science, Bournemouth University, UK, is acknowledged for providing the Certified Reference Material. Research fellowship to the first author by University Grants Commission, New Delhi, India, is gratefully acknowledged. NR was funded by a South and Central Asia Regional Travel Grant, The United States-India Educational Foundation.
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Naikoo, M.I., Dar, M.I., Khan, F.A. et al. Trophic transfer and bioaccumulation of lead along soil–plant–aphid–ladybird food chain. Environ Sci Pollut Res 26, 23460–23470 (2019). https://doi.org/10.1007/s11356-019-05624-x
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DOI: https://doi.org/10.1007/s11356-019-05624-x