Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10937–10945 | Cite as

Biochar alleviates the toxicity of imidacloprid and silver nanoparticles (AgNPs) to Enchytraeus albidus (Oligochaeta)

  • Ngitheni Winnie-Kate Nyoka
  • Sthandiwe Nomthandazo Kanyile
  • Emile Bredenhand
  • Godfried Jacob Prinsloo
  • Patricks Voua Otomo
Research Article

Abstract

The present study investigated the use of biochar for the alleviation of the toxic effects of a nanosilver colloidal dispersion and a chloronicotinyl insecticide. The survival and reproduction of the potworm Enchytraeus albidus were assessed after exposure to imidacloprid and silver nanoparticles (AgNPs). E. albidus was exposed to 0, 25, 50, 100, 200, and 400 mg imidacloprid/kg and 0, 5, 25, 125, and 625 mg Ag/kg for 21 days in 10% biochar amended and non-biochar amended OECD artificial soil. In both exposure substrates, the effects of imidacloprid on survival were significant in the two highest treatments (p < 0.01). No biochar effect was observed as survival was statistically similar in both soils after exposure to imidacloprid. In the case of AgNPs, significant mortality was only observed in the highest AgNP treatments in both the amended and non-amended soils (p < 0.05). Nevertheless, statistically greater survival occurred in the biochar-amended treatment (p < 0.05). Reproduction results showed a more pronounced biochar effect with an EC50 = 22.27 mg imidacloprid/kg in the non-amended soil and a higher EC50 = 46.23 mg imidacloprid/kg in the biochar-amended soil. This indicated a 2-fold decrease in imidacloprid toxicity due to biochar amendment. A similar observation was made in the case of AgNPs where a reproduction EC50 = 166.70 mg Ag/kg soil in the non-amended soil increased to an EC50 > 625 mg Ag/kg soil (the highest AgNP treatment) in the amended soil. This indicated at least a 3.7-fold decrease in AgNPs toxicity due to biochar amendment. Although more studies may be needed to optimize the easing effects of biochar on the toxicity of these chemicals, the present results show that biochar could be useful for the alleviation of the toxic effects of imidacloprid and silver nanoparticles in the soil.

Keywords

Oligochaetes Nanotoxicity Metal nanomaterials Soil remediation Agrochemicals 

Supplementary material

11356_2018_1383_MOESM1_ESM.xlsx (52 kb)
ESM 1 (XLSX 52 kb)
11356_2018_1383_MOESM2_ESM.pdf (83 kb)
ESM 2 (PDF 83 kb)
11356_2018_1383_MOESM3_ESM.pdf (74 kb)
ESM 3 (PDF 74 kb)
11356_2018_1383_MOESM4_ESM.xlsx (77 kb)
ESM 4 (XLSX 76 kb)
11356_2018_1383_MOESM5_ESM.pdf (76 kb)
ESM 5 (PDF 76 kb)
11356_2018_1383_MOESM6_ESM.pdf (42 kb)
ESM 6 (PDF 41 kb)

References

  1. Ahmad M, Rajapaksha AU, Lim JE, Zhang M, Bolan N, Mohan D, Vithanage M, Lee SS, Ok YS (2014) Biochar as a sorbent for contaminant management in soil and water: a review. Chemosphere 99:19–33.  https://doi.org/10.1016/j.chemosphere.2013.10.071 CrossRefGoogle Scholar
  2. Amorim M, Römbke J, Scheffczyk A, Soares A (2005) Effect of different soil types on the enchytraeids Enchytraeus albidus and Enchytraeus luxuriosus using the herbicide phenmedipham. Chemosphere 61(8):1102–1114.  https://doi.org/10.1016/j.chemosphere.2005.03.048 CrossRefGoogle Scholar
  3. Anawar HM, Akter F, Solaiman ZM, Strezov V (2015) Biochar: an emerging panacea for remediation of soil contaminants from mining, industry and sewage wastes. Pedosphere 25(5):654–665.  https://doi.org/10.1016/S1002-0160(15)30046-1 CrossRefGoogle Scholar
  4. Bicho RC, Ribeiro T, Rodrigues NP, Scott-Fordsmand JJ, Amorim MJ (2016) Effects of Ag nanomaterials (NM300K) and Ag salt (AgNO 3) can be discriminated in a full life cycle long term test with Enchytraeus crypticus. J Hazard Mater 318:608–614.  https://doi.org/10.1016/j.jhazmat.2016.07.040 CrossRefGoogle Scholar
  5. Beesley L, Moreno-Jiménez E, Gomez-Eyles JL, Harris E, Robinson B, Sizmur T (2011) A review of biochars’ potential role in the remediation, revegetation and restoration of contaminated soils. Environ Pollut 159(12):3269–3282.  https://doi.org/10.1016/j.envpol.2011.07.023 CrossRefGoogle Scholar
  6. Boina DR, Onagbola EO, Salyani M, Stelinski LL (2009) Antifeedant and sublethal effects of imidacloprid on Asian citrus psyllid, Diaphorina citri. Pest Manag Sci 65(8):870–877.  https://doi.org/10.1002/ps.1767 CrossRefGoogle Scholar
  7. Cabrera A, Cox L, Spokas KURT, Hermosín MC, Cornejo J, Koskinen WC (2014) Influence of biochar amendments on the sorption–desorption of aminocyclopyrachlor, bentazone and pyraclostrobin pesticides to an agricultural soil. Sci Total Environ 470:438–443CrossRefGoogle Scholar
  8. Cao X, Harris W (2010) Properties of dairy-manure-derived biochar pertinent to its potential use in remediation. Bioresour Technol 101(14):5222–5228.  https://doi.org/10.1016/j.biortech.2010.02.052 CrossRefGoogle Scholar
  9. Capowiez Y, Bastardie F, Costagliola G (2006) Sublethal effects of imidacloprid on the burrowing behaviour of two earthworm species: modifications of the 3D burrow systems in artificial cores and consequences on gas diffusion in soil. Soil Biol Biochem 38:285–293CrossRefGoogle Scholar
  10. Capowiez Y, Rault M, Costagliola G, Mazzia C (2005) Lethal and sublethal effects of imidacloprid on two earthworm species (Aporrectodea nocturna and Allolobophora icterica). Biol Fertil Soils 41(3):135–143.  https://doi.org/10.1007/s00374-004-0829-0 CrossRefGoogle Scholar
  11. Capowiez Y, Rault M, Mazzia C, Belzunces L (2003) Earthworm behaviour as a biomarker—a case study using imidacloprid: the 7th International Symposium on Earthworm Ecology · Cardiff· Wales · 2002. Pedobiologia 47(5–6):542–547Google Scholar
  12. Denyes MJ, Langlois VS, Rutter A, Zeeb BA (2012) The use of biochar to reduce soil PCB bioavailability to Cucurbita pepo and Eisenia fetida. Sci Total Environ 437:76–82.  https://doi.org/10.1016/j.scitotenv.2012.07.081 CrossRefGoogle Scholar
  13. Drobne D, Blažič M, Van Gestel CA, Lešer V, Zidar P, Jemec A, Trebše P (2008) Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere 71:1326–1334CrossRefGoogle Scholar
  14. Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C, Eggers S (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11(2):97–105.  https://doi.org/10.1016/j.baae.2009.12.001 CrossRefGoogle Scholar
  15. Gomes SIL, Scott-Fordsmand JJ, Amorim MJB (2015) Cellular energy allocation to assess the impact of nanomaterials on soil invertebrates (Enchytraeids): the effect of Cu and Ag. Int J Environ Res Public Health 12(6):6858–6878.  https://doi.org/10.3390/ijerph120606858 CrossRefGoogle Scholar
  16. Gomes SIL, Soares AMVM, Scott-Fordsmand JJ, Amorim MJB (2013) Mechanism of response to silver nanoparticles on Enchytraeus albidus (Oligochaeta): survival, reproduction and gene expression profile. J Hazard Mater 254–255:336–344CrossRefGoogle Scholar
  17. Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50(4):977–987.  https://doi.org/10.1111/1365-2664.12111 CrossRefGoogle Scholar
  18. Gunther FA (1975) Residue Reviews. Springer, New YorkCrossRefGoogle Scholar
  19. Hayashi Y, Heckmann LH, Simonsen V, Scott-Fordsmand JJ (2013) Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida. Ecotoxicol Environ safe 98:219–226.  https://doi.org/10.1016/j.ecoenv.2013.08.017 CrossRefGoogle Scholar
  20. Hsiao IL, Hsieh YK, Wang CF, Chen IC, Huang YJ (2015) Trojan-horse mechanism in the cellular uptake of silver nanoparticles verified by direct intra-and extracellular silver speciation analysis. Environ Sci Technol 49(6):3813–3821.  https://doi.org/10.1021/es504705p CrossRefGoogle Scholar
  21. Jeong CY, Wang JJ, Dodla SK (2012) Effect of biochar amendment on tylosin adsorption–desorption and transport in two different soils. J Environ Qual 41(4):1185–1192.  https://doi.org/10.2134/jeq2011.0166 CrossRefGoogle Scholar
  22. Jin J, Kang M, Sun K, Pan Z, Wu F, Xing B (2016) Properties of biochar-amended soils and their sorption of imidacloprid, isoproturon, and atrazine. Sci Total Environ 550:504–513.  https://doi.org/10.1016/j.scitotenv.2016.01.117 CrossRefGoogle Scholar
  23. Kamrin MA (1997) Pesticide profiles: toxicity, environmental impact, and fate. CRC press, Florida.  https://doi.org/10.1201/9781420049220 CrossRefGoogle Scholar
  24. Kim B, Park CS, Murayama M, Hochella Jr MF (2010) Discovery and characterization of silver sulfide nanoparticles in final sewage sludge products. Environ Sci Technol 44(19): 7509–7514, DOI:  https://doi.org/10.1021/es101565j
  25. Klein CL, Comero S, Stahlmecke D, Romazanov J, Kuhlbusch TAJ, Van Doren E, de Temmerman PJ, Mast J, Wick P, Krug H, Locoro G, Hund-Rinke K, Kördel W, Friedrichs S, Maier G, Werner J, Linsinger T, Gawlik BM (2011) NM-series of representative manufactured nanomaterials: NM-300 silver. Characterisation, stability, homogeneity. Publication Office of the European Union (JRC scientific and technical reports 60709), LuxembourgGoogle Scholar
  26. Kookana RS (2010) The role of biochar in modifying the environmental fate, bioavailability, and efficacy of pesticides in soils: a review. Soil Res 48(7):627–637.  https://doi.org/10.1071/SR10007 CrossRefGoogle Scholar
  27. Kreutzweiser DP, Good KP, Chartrand DT, Scarr TA, Holmes SB, Thompson DG (2008) Effects on litter-dwelling earthworms and microbial decomposition of soil-applied imidacloprid for control of wood-boring insects. Pest Manag Sci 64(2):112–118.  https://doi.org/10.1002/ps.1478 CrossRefGoogle Scholar
  28. Kuperman RG, Amorim MJ, Römbke J, Lanno R, Checkai RT, Dodard SG, Sunahara GI, Scheffczyk A (2006) Adaptation of the enchytraeid toxicity test for use with natural soil types. Eur J Soil Biol 42:S234–S243.  https://doi.org/10.1016/j.ejsobi.2006.07.028 CrossRefGoogle Scholar
  29. Lashkari MR, Sahragard A, Ghadamyari M (2007) Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Sci 14(3):207–212CrossRefGoogle Scholar
  30. Lehmann J (2007) A handful of carbon. Nature 447(7141):143–144.  https://doi.org/10.1038/447143a CrossRefGoogle Scholar
  31. Lehmann J, Joseph S (2009) Biochar for environmental management science and technology. Earthscans, London, pp 1–12Google Scholar
  32. Lock K, De Schamphelaere KAC, Janssen CR (2002) The effect of lindane on terrestrial invertebrates. Arch Environ Contam Toxicol 42(2):217–221CrossRefGoogle Scholar
  33. Lock K, Janssen CR (2002) Ecotoxicity of chromium (III) to Eisenia fetida, Enchytraeus albidus, and Folsomia candida. Ecotoxicol Environ Saf 51(3):203–205.  https://doi.org/10.1006/eesa.2001.2122 CrossRefGoogle Scholar
  34. Luo Y, Zang Y, Zhong Y, Kong Z (1999) Toxicological study of two novel pesticides on earthworm Eisenia foetida. Chemosphere 39(13):2347–2356.  https://doi.org/10.1016/S0045-6535(99)00142-3 CrossRefGoogle Scholar
  35. Major J (2010) Guidelines on practical aspects of biochar application to field soil in various soil management systems. International Biochar Initiative 8Google Scholar
  36. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22(11):573–580.  https://doi.org/10.1016/S0165-6147(00)01820-4 CrossRefGoogle Scholar
  37. Mostert MA, Schoeman AS, van der Merwe M (2000) The toxicity of five insecticides to earthworms of the Pheretima group, using an artificial soil test. Pest Manag Sci 56(12):1093–1097.  https://doi.org/10.1002/1526-4998(200012)56:12<1093::AID-PS259>3.0.CO;2-6 CrossRefGoogle Scholar
  38. Novais SC, Gomes SI, Gravato C, Guilhermino L, De Coen W, Soares AM, Amorim MJ (2011) Reproduction and biochemical responses in Enchytraeus albidus (Oligochaeta) to zinc or cadmium exposures. Environ Pollut 159(7):1836–1843.  https://doi.org/10.1016/j.envpol.2011.03.031 CrossRefGoogle Scholar
  39. Novais SC, Soares AM, Amorim MJ (2010) Can avoidance in Enchytraeus albidus be used as a screening parameter for pesticides testing? Chemosphere 79(2):233–237.  https://doi.org/10.1016/j.chemosphere.2010.01.011 CrossRefGoogle Scholar
  40. OECD (Organization for Economic Cooperation and Development) (2004) Guidelines for the testing of chemicals no. 220. Enchytraeid reproduction test (Enchytraeus albidus). Paris, FranceGoogle Scholar
  41. OECD (Organization for Economic Cooperation and Development) (2015a) Guidelines for the testing of chemicals no. 220. Enchytraeid reproduction test (Enchytraeus albidus).Paris, FranceGoogle Scholar
  42. OECD (Organization for Economic Cooperation and Development) (2015b). Current developments in delegations on the safety of manufactured nanomaterials—Tour de table. Paris, France (2015)Google Scholar
  43. Park EJ, Yi J, Kim Y, Choi K, Park K (2010) Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol in Vitro 24(3):872–878.  https://doi.org/10.1016/j.tiv.2009.12.001 CrossRefGoogle Scholar
  44. Park J, Hung I, Gan Z, Rojas OJ, Lim KH, Park S (2013) Activated carbon from biochar: influence of its physicochemical properties on the sorption characteristics of phenanthrene. Bioresour Technol 149:383–389.  https://doi.org/10.1016/j.biortech.2013.09.085 CrossRefGoogle Scholar
  45. Park JH, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348(1):439–451.  https://doi.org/10.1007/s11104-011-0948-y CrossRefGoogle Scholar
  46. Peng X, Ye LL, Wang CH, Zhou H, Sun B (2011) Temperature-and duration-dependent rice straw-derived biochar: characteristics and its effects on soil properties of an ultisol in southern China. Soil Tillage Res 112(2):159–166.  https://doi.org/10.1016/j.still.2011.01.002 CrossRefGoogle Scholar
  47. Prabhu S, Poulose E (2012) Silver nanoparticles: mechanism of antimicrobial action, synthesis and medical applications and toxicity effects. Int Nano Lett 2(1):32.  https://doi.org/10.1186/2228-5326-2-32 CrossRefGoogle Scholar
  48. Qian K, Kumar A, Zhang H, Bellmer D, Huhnke R (2015) Recent advances in utilization of biochar. Renew Sustain Energy Rev 42:1055–1064.  https://doi.org/10.1016/j.rser.2014.10.074 CrossRefGoogle Scholar
  49. Quintela ED, McCoy CW (1998) Synergistic effect of imidacloprid and two entomopathogenic fungi on the behavior and survival of larvae of Diaprepes abbreviatus (Coleoptera: Curculionidae) in soil. J Econ Entomol 91(1):110–122.  https://doi.org/10.1093/jee/91.1.110 CrossRefGoogle Scholar
  50. Rajapaksha AU, Ahmad M, Vithanage M, Kim KR, Chang JY, Lee SS, Ok YS (2015) The role of biochar, natural iron oxides, and nanomaterials as soil amendments for immobilizing metals in shooting range soil. Environ Geochem Health 37(6):931–942.  https://doi.org/10.1007/s10653-015-9694-z CrossRefGoogle Scholar
  51. Ribeiro MJ, Maria VL, Scott-Fordsmand JJ, Amorim MJB (2015) Oxidative stress mechanisms caused by Ag nanoparticles (NM300K) are different from those of AgNO3: effects in the soil invertebrate Enchytraeus crypticus. Int J Environ Res Public Health 12(8):9589–9602.  https://doi.org/10.3390/ijerph120809589 CrossRefGoogle Scholar
  52. Roh JY, Sim SJ, Yi J, Park K, Chung KH, Ryu DY, Choi J (2009) Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ Sci Technol 43(10):3933–3940.  https://doi.org/10.1021/es803477u CrossRefGoogle Scholar
  53. Römbke J, Jänsch S, Junker T, Pohl B, Scheffczyk A, Schallnaß HJ (2006) Improvement of the applicability of ecotoxicological tests with earthworms, springtails, and plants for the assessment of metals in natural soils. Environ Toxicol Chem 25(3):776–787.  https://doi.org/10.1897/04-584R.1 CrossRefGoogle Scholar
  54. Römbke J (1989) Entwicklung eines Reproduktionstests an Bodenorganismen—Enchytraeen. Abschlußbericht des Battelle-Instituts eV, Frankfurt für das Umweltbundesamt (Berlin), FE-Vorhaben 106: 051Google Scholar
  55. Römbke J (2003) Ecotoxicological laboratory tests with enchytraeids: a review: the 7th International Symposium on Earthworm Ecology · Cardiff · Wales· 2002. Pedobiologia 47(5–6):607–616Google Scholar
  56. Schlich K, Klawonn T, Terytze K, Hund-Rinke K (2013) Effects of silver nanoparticles and silver nitrate in the earthworm reproduction test. Environ Toxicol Chem 32(1):181–188.  https://doi.org/10.1002/etc.2030 CrossRefGoogle Scholar
  57. Schüler S (2015) Assessing the chronic toxicity of silver nanoparticles and silver nitrate to the Enchytraeid Enchytraeus albidus in three standard substrates. Msc Thesis, University of Bremen, BremenGoogle Scholar
  58. Song XD, Xue XY, Chen DZ, He PJ, Dai XH (2014) Application of biochar from sewage sludge to plant cultivation: influence of pyrolysis temperature and biochar-to-soil ratio on yield and heavy metal accumulation. Chemosphere 109:213–220.  https://doi.org/10.1016/j.chemosphere.2014.01.070 CrossRefGoogle Scholar
  59. Tourinho C, Van Gestel C, Lofts S (2012) Metal-based nanoparticles in soil: fate, behaviour and effects on soil invertebrates. Environ Toxicol Chem 31(8):1679–1692CrossRefGoogle Scholar
  60. Tourinho PS, van Gestel CA, Jurkschat K, Soares AM, Loureiro S (2015) Effects of soil and dietary exposures to Ag nanoparticles and AgNO 3 in the terrestrial isopod Porcellionides pruinosus. Environ Pollut 205:170–177.  https://doi.org/10.1016/j.envpol.2015.05.044 CrossRefGoogle Scholar
  61. Van Der Werf HMG (1996) Assessing the impact of pesticides on the environment. Agric Ecosyst Environ 60(2-3):81–96.  https://doi.org/10.1016/S0167-8809(96)01096-1 CrossRefGoogle Scholar
  62. Xu G, Lv Y, Sun J, Shao H, Wei L (2012) Recent advances in biochar applications in agricultural soils: benefits and environmental implications. CLEAN–Soil, Air, Water 40(10):1093–1098.  https://doi.org/10.1002/clen.201100738 CrossRefGoogle Scholar
  63. Yang X, Liu J, McGrouther K, Huang H, Lu K, Guo X, Wang H (2016) Effect of biochar on the extractability of heavy metals (Cd, Cu, Pb, and Zn) and enzyme activity in soil. Environ Sci Pollut Res 23(2):974–984.  https://doi.org/10.1007/s11356-015-4233-0 CrossRefGoogle Scholar
  64. Yao Y, Gao B, Zhang M, Inyang M, Zimmerman AR (2012) Effect of biochar amendment on sorption and leaching of nitrate, ammonium, and phosphate in a sandy soil. Chemosphere 89(11):1467–1471CrossRefGoogle Scholar
  65. Yu JT, Dehkhoda AM, Ellis N (2010) Development of biochar-based catalyst for transesterification of canola oil. Energy Fuel 25(1):337–344CrossRefGoogle Scholar
  66. Yu XY, Ying GG, Kookana RS (2009) Reduced plant uptake of pesticides with biochar additions to soil. Chemosphere 76(5):665–671.  https://doi.org/10.1016/j.chemosphere.2009.04.001 CrossRefGoogle Scholar
  67. Zang Y, Zhong Y, Luo Y, Kong ZM (2000) Genotoxicity of two novel pesticides for the earthworm, Eisenia fetida. Environ Pollut 108(2):271–278.  https://doi.org/10.1016/S0269-7491(99)00191-8 CrossRefGoogle Scholar
  68. Zhang A, Cui L, Pan G, Li L, Hussain Q, Zhang X, Crowley D (2010) Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China. Agric Ecosyst Environ 139(4):469–475CrossRefGoogle Scholar
  69. Zheng W, Guo M, Chow T, Bennett DN, Rajagopalan N (2010) Sorption properties of greenwaste biochar for two triazine pesticides. J Hazard Mater 181(1-3):121–126.  https://doi.org/10.1016/j.jhazmat.2010.04.103 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Zoology and EntomologyUniversity of the Free StatePhuthaditjhabaRepublic of South Africa
  2. 2.Department of Crop ProtectionAgriculture Research Council—Small Grain InstituteBethlehemRepublic of South Africa

Personalised recommendations