Skip to main content
Log in

Toxicity, monitoring and biodegradation of the fungicide carbendazim

  • Review
  • Published:
Environmental Chemistry Letters Aims and scope Submit manuscript

Abstract

The increasing use of toxic pesticides is a major environmental concern. Carbendazim is a systemic fungicide having wide applications for controlling fungal diseases in agriculture, forestry and veterinary medicines. Carbendazim is a major pollutant detectable in food, soil and water. Carbendazim extensive and repeated use induces acute and delayed toxic effects on humans, invertebrates, aquatic life forms and soil microorganisms. Here, we review the pollution, non-target toxicity and microbial degradation of carbendazim for crop and veterinary purposes. We found that carbendazim causes embryotoxicity, apoptosis, teratogenicity, infertility, hepatocellular dysfunction, endocrine-disrupting effects, disruption of haematological functions, mitotic spindle abnormalities, mutagenic and aneugenic effect. We also found that carbendazim disrupted the microbial community structure in various ecosystems. The detection of carbendazim in soil and reservoir sites is performed by spectroscopic, chromatographic, voltammetric, nanoparticles, carbon electrodes and mass spectrometry. A review of the degradation of carbendazim shows that carbendazim undergoes partial to complete biodegradation in the soil and water by Azospirillum, Aeromonas, Alternaria, Bacillus, Brevibacillus, Nocardioides, Pseudomonas, Ralstonia, Rhodococcus, Sphingomonas, Streptomyces and Trichoderma.

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

Access this article

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

  • Adedara IA, Vaithinathan S, Jubendradass R, Mathur PP, Farombi EO (2013) Kolaviron prevents carbendazim-induced steroidogenic dysfunction and apoptosis in testes of rats. Environ Toxicol Pharmacol 35:444–453. doi:10.1016/j.etap.2013.01.010

    Article  CAS  Google Scholar 

  • Aire TA (2005) Short-term effects of carbendazim on the gross and microscopic features of the testes of Japanese quails (Coturnix coturnix japonica). Anat Embryol 210:43–49. doi:10.1007/s00429-005-0001-0

    Article  CAS  Google Scholar 

  • Alvarez JLM, Calzón JAG, Fonseca JML (1997) Catalytic polarographic prewave of cobalt (II) induced by carbendazim. Application to the voltammetric determination of benomyl. Electroanal 9:500–502. doi:10.1002/elan.1140090614

    Article  Google Scholar 

  • Anastassiades M, Schwack W (1998) Analysis of carbendazim, benomyl, thiophanate methyl and 2,4-dichlorophenoxyacetic acid in fruits and vegetables after supercritical fluid extraction. J Chromatogr A 825:45–54. doi:10.1016/S0021-9673(98)00691-8

    Article  CAS  Google Scholar 

  • Andrade TS, Henriques JF, Almeida AR, Machado AL, Koba O, Giang PT, Soares AM, Domingues I (2016) Carbendazim exposure induces developmental, biochemical and behavioural disturbance in zebrafish embryos. Aquat Toxicol 170:390–399. doi:10.1016/j.aquatox.2015.11.017

    Article  CAS  Google Scholar 

  • Arya R, Sharma AK (2015) Bioremediation of carbendazim, a benzimidazole fungicide using Brevibacillus borstelensis and Streptomyces albogriseolus together. Curr Pharm Biotechnol 17:185–189. doi:10.2174/1389201016666150930115737

    Article  CAS  Google Scholar 

  • Bakirci GT, Acay DB, Bakirci F, Otles S (2014) Pesticide residues in fruits and vegetables from the Aegean region, Turkey. Food Chem 160:379–392. doi:10.1016/j.foodchem.2014.02.051

    Article  CAS  Google Scholar 

  • Banyiova K, Necasova A, Kohoutek J, Justan I, Čupr P (2016) New experimental data on the human dermal absorption of simazine and carbendazim help to refine the assessment of human exposure. Chemosphere 145:148–156. doi:10.1016/j.chemosphere.2015.11.018

    Article  CAS  Google Scholar 

  • Barnett RM, Carone CD, Groom DE, Trippe TG, Wohl CG, Armstrong B, Gee PS, Wagman GS, James F, Mangano M, Monig K (1996) Review of particle physics. Phys Rev D 54:1. doi:10.1103/PhysRevD.54.1

    Article  Google Scholar 

  • Bentley KS, Kirkland D, Murphy M, Marshall R (2000) Evaluation of thresholds for benomyl-and carbendazim-induced aneuploidy in cultured human lymphocytes using fluorescence in situ hybridization. Mutat Res 464:41–51. doi:10.1016/S1383-5718(99)00165-5

    Article  CAS  Google Scholar 

  • Bernard MB, Cole P, Kobelt A, Horne PA, Altmann J, Wratten SD, Yen AL (2010) Reducing the impact of pesticides on biological control in Australian vineyards: pesticide mortality and fecundity effects on an indicator species, the predatory mite Euseius victoriensis (Acari: Phytoseiidae). J Eco Entomol 103:2061–2071. doi:10.1603/EC09357

    Article  CAS  Google Scholar 

  • Bhushan C, Bhardwaj A, Misra SS (2013) State of pesticide regulations in India. Report of Centre for Science and Environment, New Delhi

    Google Scholar 

  • Bicchi C, Belliardo F, Cantamessa L, Gasparini G, Icardi M, Sesia E (1989) Simultaneous determination of benzimidazole fungicides by HPLC on apples, pears and their pulps. Pest Sci 25:355–360. doi:10.1002/ps.2780250405

    Article  CAS  Google Scholar 

  • Canton JH (1976) The toxicity of benomyl, thiophanate-methyl, and BCM to four freshwater organisms. Environ Contam Toxicol 16:214–218. doi:10.1007/BF01685230

    Article  CAS  Google Scholar 

  • Carter SD, Hess RA, Laskey JW (1987) The fungicide methyl 2-benzimidazole carbamate causes infertility in male Sprague-Dawley rats. Biol Reprod 37:709–717. doi:10.1095/biolreprod37.3.709

    Article  CAS  Google Scholar 

  • Chatupote W, Panapitukkul N (2005) Regional assessment of nutrient and pesticide leaching in the vegetable production area of Rattaphum catchment, Thailand. Water Air Soil Pollut Focus 5:165–173. doi:10.1007/s11267-005-7411-0

    Article  CAS  Google Scholar 

  • Correa LM, Nakai M, Strandgaard CS, Hess RA, Miller MG (2002) Microtubules of the mouse testis exhibit differential sensitivity to the microtubule disruptors carbendazim and colchicine. Toxicol Sci 69:175–182. doi:10.1093/toxsci/69.1.175

    Article  CAS  Google Scholar 

  • Daam MA, Satapornvanit K, Van den BPJ, Nogueira AJ (2009) Sensitivity of macroinvertebrates to carbendazim under semi-field conditions in Thailand: implications for the use of temperate toxicity data in a tropical risk assessment of fungicides. Chemosphere 74:1187–1194. doi:10.1016/j.chemosphere.2008.11.040

    Article  CAS  Google Scholar 

  • Dang Z, Smit CE (2008) Environmental risk limits for carbendazim. Bilthoven, The Netherlands: National Institute for Public Health and the Environment (RIVM). Letter Report (601716014)

  • EU Pesticide Database (2015) European Commission, (http://ec.europa.eu/food/plant/pesticides/eu-pesticides-database/public/?event=homepageandlanguage=EN)

  • Daundkar PS, Rampal S (2014) Evaluation of ameliorative potential of selenium on carbendazim induced oxidative stress in male goats. Environ Toxicol Pharmacol 38:711–719. doi:10.1016/j.etap.2014.09.007

    Article  CAS  Google Scholar 

  • Davidse LC (1986) Benzimidazole fungicides: mechanism of action and biological impact. Ann Rev Phytopathol 24:43–65. doi:10.1146/annurev.py.24.090186.000355

    Article  CAS  Google Scholar 

  • De A, Bose R, Kumar A, Mozumdar S (2014) Worldwide pesticide use. In: Targeted Delivery of Pesticides Using Biodegradable Polymeric Nanoparticles; Springer: New Delhi, India, pp 5–6

  • Devi PA, Paramasivam M, Prakasam V (2015) Degradation pattern and risk assessment of carbendazim and mancozeb in mango fruits. Environ Monit Assess 187:1–6. doi:10.1007/s10661-014-4142-6

    Article  CAS  Google Scholar 

  • Dikic D, Landeka I, Knežević F, Mojsović-Ćuić A, Benković V, Horvat-Knežević A, Rogić D (2012) Carbendazim impends hepatic necrosis when combined with imazalil or cypermethrin. Basic Clin Pharmacol Toxicol 110:433–440. doi:10.1111/j.1742-7843.2011.00831.x

    Article  CAS  Google Scholar 

  • Fang H, Wang Y, Gao C, Yan H, Dong B, Yu Y (2012) Isolation and characterization of Pseudomonas sp. CBW capable of degrading carbendazim. Biodegradation 21:939–946. doi:10.1007/s10532-010-9353-0

    Article  CAS  Google Scholar 

  • FAO (1998) Pesticides residues in food-1997 evaluations. Part I Residues, FAO Plant production and protection paper, Rome, p 146

    Google Scholar 

  • Farag A, Ebrahim H, ElMazoudy R, Kadous E (2011) Developmental toxicity of fungicide carbendazim in female mice. Birth Defe Res B: Develop Reprod Toxicol 92:122–130. doi:10.1002/bdrb.20290

    Article  CAS  Google Scholar 

  • Fawole OB, Aluko M, Olowonihi TE (2010) Effects of a Carbendazim-Mancozeb fungicidal mixture on soil microbial populations and some enzyme activities in soil. Agrosearch 10:1–2. doi:10.4314/agrosh.v10i1-2.69831

    Google Scholar 

  • Ferreira AL, Loureiro S, Soares AM (2008) Toxicity prediction of binary combinations of cadmium, carbendazim and low dissolved oxygen on Daphnia magna. Aqua Toxicol 89:28–39. doi:10.1016/j.aquatox.2008.05.012

    Article  CAS  Google Scholar 

  • Furini LN, Sanchez-Cortes S, López-Tocón I, Otero JC, Aroca RF, Constantino CJ (2015) Detection and quantitative analysis of carbendazim herbicide on Ag nanoparticles via surface-enhanced Raman scattering. J Raman Spectr 46:1095–1101. doi:10.1002/jrs.4737

    Article  CAS  Google Scholar 

  • Goodson WH, Lowe L, Carpenter DO, Gilbertson M, Ali AM, de Cerain Salsamendi AL et al (2015) Assessing the carcinogenic potential of low-dose exposures to chemical mixtures in the environment: the challenge ahead. Carcinogenesis 36:254–296. doi:10.1093/carcin/bgv039

    Article  Google Scholar 

  • Gray LE, Ostby J, Linder R, Goldman J, Rehnberg G, Cooper R (1990) Carbendazim-induced alterations of reproductive development and function in the rat and hamster. Fund Appl Toxicol 15:281–297. doi:10.1016/0272-0590(90)90055-O

    Article  CAS  Google Scholar 

  • Gupta RC, Aggarwal M (2007) Toxicity of fungicides. Veterinary Toxicology, New York

    Book  Google Scholar 

  • Hammond LA, Davidson K, Lawrence R, Camden JB, Von Hoff DD, Weitman S, Izbicka E (2001) Exploring the mechanisms of action of FB642 at the cellular level. J Cancer Res Clin Oncol 127:301–313

    Article  CAS  Google Scholar 

  • Hao LQ (2002) Advances on the pesticide residue analysis of Chinese herbal medicine. J Huazhong Agric 2:20–24

    Google Scholar 

  • Holtman MA, Kobayashi DY (1997) Identification of Rhodococcus erythropolis isolates capable of degrading the fungicide carbendazim. Appl Microbiol Biotechnol 47:578–582. doi:10.1007/s002530050976

    Article  CAS  Google Scholar 

  • Hsu YH, Chang CW, Chen MC, Yuan CY (2011) Carbendazim-induced androgen receptor expression antagonized by flutamide in male rats. J Food Drug Anal 19:4

    Google Scholar 

  • Huan Z, Luo J, Xu Z, Xie D (2016) Acute toxicity and genotoxicity of carbendazim, main impurities and metabolite to earthworms (Eisenia foetida). Bull Environ Contam Toxicol 96:62–69. doi:10.1007/s00128-015-1653-y

    Article  CAS  Google Scholar 

  • Itak JA, Selisker MY, Jourdan SW, Fleeker JR, Herzog DP (1993) Determination of benomyl (as carbendazim) and carbendazim in water, soil, and fruit juice by a magnetic particle-based immunoassay. J Agric Food Chem 41:2329–2332. doi:10.1021/jf00036a021

    Article  CAS  Google Scholar 

  • Janardhan A, Rao AB, Sisodia P (1987) Sub-chronic toxicity of methyl benzimidazole carbamate in rats. Bull Environ Contam Toxicol 38:890–898. doi:10.1007/BF01616717

    Article  CAS  Google Scholar 

  • Jansen JP (1999) Side effects of pesticides on adults of Aphidius rhopalosiphi De Stefani-Perez (Hym.: Aphidiidae) in the laboratory: results of the 8th Joint Pesticide Testing Programme. Versailles, France 27–29 October 23:65–72

    Google Scholar 

  • Javorekova SN, Svrcbreve ekova I, Makova J (2010) Influence of benomyl and prometryn on the soil microbial activities and community structures in pasture grasslands of Slovakia. J Environ Sci Health B 45:702–709. doi:10.1080/03601234.2010.502463

    Article  CAS  Google Scholar 

  • Jiang J, Wu S, Wang Y, An X, Cai L, Zhao X, Wu C (2015) Carbendazim has the potential to induce oxidative stress, apoptosis, immunotoxicity and endocrine disruption during zebrafish larvae development. Toxicol In Vitro 29:1473–1481. doi:10.1016/j.tiv.2015.06.003

    Article  CAS  Google Scholar 

  • Jing-Liang X, Xiang-Yang G, Biao S, Zhi-Chun W, Kun W, Shun-Peng L (2006) Isolation and characterization of a carbendazim-degrading Rhodococcus sp. djl-6. Curr Microbiol 53:72–76. doi:10.1007/s00284-005-0474-3

    Article  CAS  Google Scholar 

  • John EM, Shaike JM (2015) Chlorpyrifos: pollution and remediation. Environ Chem Lett 13:269–291. doi:10.1007/s10311-015-0513-7

    Article  CAS  Google Scholar 

  • Jones SE, Williams DJ, Holliman PJ, Taylor N, Baumann J, Forster B, Van Gestel CAM, Rodrigues JML (2004) Ring-testing and field-validation of a terrestrial model ecosystem (TME)-an instrument for testing potentially harmful substances: fate of the model chemical carbendazim. Ecotoxicol 3:29–42. doi:10.1023/B:ECTX.0000012403.90709.c9

    Article  Google Scholar 

  • Kalwasińska A, Kęsy J, Donderski W, Lalke-Porczyk E (2008a) Biodegradation of carbendazim by planktonic and benthic bacteria of eutrophic lake Chełmżyńskie. Pol J Environ Stud 17:515–523

    Google Scholar 

  • Kalwasińska A, Kęsy J, Donderski W (2008b) Biodegradation of carbendazim by epiphytic and neustonic bacteria of eutrophic chełmżyńskie lake. Pol J Microbiol 57:221–230

    Google Scholar 

  • Karlsson I, Friberg H, Steinberg C, Persson P (2014) Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS One 9:e111786. doi:10.1371/journal.pone.0111786

    Article  CAS  Google Scholar 

  • Kaur T, Toor AP, Wanchoo RK (2015) Parametric study on degradation of fungicide carbendazim in dilute aqueous solutions using nano TiO2. Desalination Water Treat 54:122–131. doi:10.1080/19443994.2013.879081

    Article  CAS  Google Scholar 

  • Kaur T, Sraw A, Toor AP, Wanchoo RK (2016) Utilization of solar energy for the degradation of carbendazim and propiconazole by Fe doped TiO2. Sol Energy 125:65–66. doi:10.1016/j.solener.2015.12.001

    Article  CAS  Google Scholar 

  • Kosasa T, Kuriya Y, Matsui K, Yamanishi Y (1999) Effect of donepezil hydrochloride (E2020) on basal concentration of extracellular acetylcholine in the hippocampus of rats. Eur J Pharmacol 380:101–107. doi:10.1016/S0014-2999(99)00545-2

    Article  CAS  Google Scholar 

  • Kumar M (2001) Acute oral toxicity study with carbendazim technical 98% in Wistar rats. Toxicology Department, Rallis Research Centre, Bangalore, India. Report number: 3179/1. Report date: 16 August 2001

  • Lacey E, Watson TR (1985) Structure-activity relationships of benzimidazole carbamates as inhibitors of mammalian tubulin in vitro. Biochem Pharmacol 34:1073–1077. doi:10.1016/0006-2952(85)90611-2

    Article  CAS  Google Scholar 

  • Lin X, Za Hou, Zhao SF, Xie L, Li HJ, Li MZ (2011a) A high efficient carbendazim-degrading bacterial strain: its isolation and identification. Chin J Ecol 7:031

    Google Scholar 

  • Lin X, Hou Z, Feng Y, Zhao S, Ye J (2011b) Isolation and characteristics of efficient carbendazim degradation bacterium. In: International Conference on Agricultural and Biosystems Engineering, Advances in Biomedical Engineering. 1:384–388

  • Liu K, Pan X, Han Y, Tang F, Yu Y (2012) Estimating the toxicity of the weak base carbendazim to the earthworm (Eisenia fetida) using in situ pore water concentrations in different soils. Sci Total Environ 438:26–32. doi:10.1016/j.talanta.2015.11.068

    Article  CAS  Google Scholar 

  • Lopez A, Yusà V, Millet M, Coscollà C (2016) Retrospective screening of pesticide metabolites in ambient air using liquid chromatography coupled to high-resolution mass spectrometry. Talanta 150:27–36. doi:10.1016/j.talanta.2015.11.068

    Article  CAS  Google Scholar 

  • Lu SY, Liao JW, Kuo ML, Wang SC, Hwang JS, Ueng TH (2004) Endocrine-disrupting activity in carbendazim-induced reproductive and developmental toxicity in rats. J Toxicol Env Heal A 67:1501–1515. doi:10.1080/15287390490486833

    Article  CAS  Google Scholar 

  • Ludwikowska A, Bojarski B, Socha M, Lutnicka H, Trzeciak KB (2013) The effect of carbendazim on embryonic Prussian carp (Carassius gibelio) development and hatching. Arch Polish Fisheries 21:367–371. doi:10.2478/aopf-2013-0038

    CAS  Google Scholar 

  • Ma J, Zheng R, Xu L, Wang S (2002) Differential sensitivity of two green algae, Scenedesmus obliqnus and Chlorella pyrenoidosa to 12 pesticides. Ecotoxicol Environ Saf 52:57–61. doi:10.1006/eesa.2002.2146

    Article  CAS  Google Scholar 

  • Manisankar P, Selvanathan G, Vedhi C (2005a) Utilisation of polypyrrole modified electrode for the determination of pesticides. Int J Environ Anal Chem 85:409–422. doi:10.1080/03067310500050726

    Article  CAS  Google Scholar 

  • Manisankar P, Selvanathan G, Vedhi C (2005b) Utilization of sodium montmorillonite clay-modified electrode for the determination of isoproturon and carbendazim in soil and water samples. Appl Clay Sci 29:249–257. doi:10.1016/j.clay.2005.01.006

    Article  CAS  Google Scholar 

  • Mantovani A, Maranghi F, Ricciardi C, Macrì C, Stazi AV, Attias L, Zapponi GA (1998) Developmental toxicity of carbendazim: comparison of no-observed-adverse-effect level and benchmark dose approach. Food Chem Toxicol 36:37–45. doi:10.1016/S0278-6915(97)00116-6

    Article  CAS  Google Scholar 

  • Mazellier P, Leroy E, De Laat J, Legube B (2003) Degradation of carbendazim by UV/H2O2 investigated by kinetic modelling. Environ Chem Lett 1:68–72. doi:10.1007/s10311-002-0010-7

    Article  CAS  Google Scholar 

  • Minta MA, Wilk IW, Żmudzki J (2004) Embryotoxicity of carbendazim in rat and hamster micromass cultures. Bull Vet Inst Pulawy 48:481–484

    Google Scholar 

  • Morinaga H, Yanase T, Nomura M, Okabe T, Goto K, Harada N, Nawata H (2004) A benzimidazole fungicide, benomyl, and its metabolite, carbendazim, induce aromatase activity in a human ovarian granulose-like tumor cell line (KGN). Endocrinology 145:1860–1869. doi:10.1210/en.2003-1182

    Article  CAS  Google Scholar 

  • Mountfort KA, Reynolds SL, Thorpe SA, White SN (1994) Comparison of ELISA and HPLC techniques for the analysis of carbendazim and thiabendazole residues in fruit and vegetables. Food Agric Immunol 6:17–22. doi:10.1080/09540109409354808

    Article  CAS  Google Scholar 

  • Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5(3):e9754. doi:10.1371/journal.pone.0009754

    Article  CAS  Google Scholar 

  • Muthuviveganandavel V, Muthuraman P, Muthu S, Srikumar K (2008) Toxic effects of carbendazim at low dose levels in male rats. J Toxicol Sci 33:25–30. doi:10.2131/jts.33.25

    Article  CAS  Google Scholar 

  • Naidu PK, Niranjan T, Naidu NVS (2011) Spectrophotometric determination of carbendazim in its formulations and environmental samples. Int J Chem Tech Res 3:1728–1733

    Google Scholar 

  • Niewiadomska A (2004) Effect of carbendazim, imazetapir and thiram on nitrogenase activity, the number of microorganisms in soil and yield of red clover (Trifolium pratense L.). Polish J Environ Studies 13:403–410

    CAS  Google Scholar 

  • Olayemi OA (2015) Comparative toxicity of two different pesticides on the skin of Japanese quail (Cortunix japonica). World Vet J 5:13–18

    Google Scholar 

  • Pacheco SE, Anderson LM, Sandrof MA, Vantangoli MM, Hall SJ, Boekelheide K (2012) Sperm mRNA transcripts are indicators of sub-chronic low dose testicular injury in the Fischer rat. PLoS One 7:e44280. doi:10.1371/journal.pone.0044280

    Article  CAS  Google Scholar 

  • Palanikumar L, Kumaraguru AK, Ramakritinan CM, Anand M (2014) Toxicity, biochemical and clastogenic response of chlorpyrifos and carbendazim in milkfish Chanos chanos. Int J Environ Sci Technol 11:765–774. doi:10.1007/s13762-013-0264-6

    Article  CAS  Google Scholar 

  • Pandey G, Dorrian SJ, Russell RJ, Brearley C, Kotsonis S, Oakeshott JG (2010) Cloning and biochemical characterization of a novel carbendazim (Methyl-1H-Benzimidazol-2-ylcarbamate)-hydrolyzing esterase from the newly isolated Nocardioides sp. strain SG-4G and its potential for use in enzymatic bioremediation. Appl Environ Microbiol 76:2940–2945. doi:10.1128/AEM.02990-09

    Article  CAS  Google Scholar 

  • Parsons KC, Mineau P, Renfrew RB (2010) Effects of pesticide use in rice fields on birds. Waterbirds 33:193–218. doi:10.1675/063.033.s115

    Article  Google Scholar 

  • Patel GM, Rohit JV, Singhal RK, Kailasa SK (2015) Recognition of carbendazim fungicide in environmental samples by using 4-aminobenzenethiol functionalized silver nanoparticles as a colorimetric sensor. Sensor Actuat B-Chem 206:684–691. doi:10.1016/j.snb.2014.09.095

    Article  CAS  Google Scholar 

  • Petroni JM, Lucca BG, Fogliato DK, Ferreira VS (2016) Sensitive approach for voltammetric determination of carbendazim based on the use of an anionic surfactant. Electroanalysis [published online]. doi: 10.1002/elan.201501069

  • Pourreza N, Rastegarzadeh S, Larki A (2015) Determination of fungicide carbendazim in water and soil samples using dispersive liquid-liquid microextraction and microvolume UV-vis spectrophotometry. Talanta 134:24–29. doi:10.1016/j.talanta.2014.10.056

    Article  CAS  Google Scholar 

  • Prashantkumar W, Sethi RS, Pathak D, Rampal S, Saini SP (2012) Testicular damage after chronic exposure to carbendazim in male goats. Toxicol Environ Chem 94:1433–1442. doi:10.1080/02772248.2012.693493

    Article  CAS  Google Scholar 

  • Rajeswari R, Kanmani S (2009) TiO2-based heterogeneous photocatalytic treatment combined with ozonation for carbendazim degradation. Iran J Environ Health Sci Eng 6:61–66

    CAS  Google Scholar 

  • Rama EM, Bortolan S, Vieira ML, Gerardin DC, Moreira EG (2014) Reproductive and possible hormonal effects of carbendazim. Regul Toxicol Pharmacol 69:476–486. doi:10.1016/j.yrtph.2014.05.016

    Article  CAS  Google Scholar 

  • Rico A, Sabater C, Castillo MÁ (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Saf 127:222–229. doi:10.1016/j.ecoenv.2016.02.004

    Article  CAS  Google Scholar 

  • Sakr S, Shalaby SY (2014) Carbendazim-induced testicular damage and oxidative stress in albino rats: ameliorative effect of licorice aqueous extract. Toxicol Ind Health 230:259–267. doi:10.1177/0748233712456059

    Article  CAS  Google Scholar 

  • Salihu M, Ajayi BO, Adedara IA, Farombi EO (2015) 6-Gingerol-rich fraction from Zingiber officinale prevents hematotoxicity and oxidative damage in kidney and liver of rats exposed to carbendazim. J Diet Suppl 16:1–16. doi:10.3109/19390211.2015.1107802

    Google Scholar 

  • Salunkhe VP, Sawant IS, Banerjee K, Wadkar PN, Sawant SD, Hingmire SA (2014) Kinetics of degradation of carbendazim by B. subtilis strains: possibility of in situ detoxification. Environ Monitor Assess 186:8599–8610. doi:10.1007/s10661-014-4027-8

    Article  CAS  Google Scholar 

  • Schaack S (2008) Daphnia comes of age: an ecological model in the genomic era. Mol Ecol 17:1634–1635. doi:10.1111/j.1365-294X.2008.03698.x

    Article  CAS  Google Scholar 

  • Segner H (2009) Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. Comp Biochem Physiol Part C: Toxicol Pharmacol 149:187–195. doi:10.1016/j.cbpc.2008.10.099

    Google Scholar 

  • Selmanoglu G, Barlas N, Songür S, KocSkaya EA (2001) Carbendazim-induced haematological, biochemical and histopathological changes to the liver and kidney of male rats. Hum Exp Toxicol 20:625–630. doi:10.1191/096032701718890603

    Article  CAS  Google Scholar 

  • Sharma KK (2007) Pesticide residue analysis manual. Directorate of Information and Publications of Agriculture. Indian Council of Agricultural Research, New Delhi

    Google Scholar 

  • Silva AR, Cardoso DN, Cruz A, Lourenço J, Mendo S, Soares AM, Loureiro S (2015) Ecotoxicity and genotoxicity of a binary combination of triclosan and carbendazim to Daphnia magna. Ecotoxicol Environ Saf 115:279–290. doi:10.1016/j.ecoenv.2015.02.022

    Article  CAS  Google Scholar 

  • Solomon KR, Brock TC, De Zwart D, Dyer SD, Posthuma L, Richards S, van den Brink PJ (2008) (eds). Extrapolation practice for ecotoxicological effect characterization of chemicals. CRC Press

  • Stollewerk A (2010) The water flea Daphnia—a ‘new’model system for ecology and evolution. J Biol 9:21. doi:10.1186/jbiol212

    Article  Google Scholar 

  • Strickland AD, Batt CA (2009) Detection of carbendazim by surface-enhanced Raman scattering using cyclodextrin inclusion complexes on gold nanorods. Anal Chem 81:2895–2903. doi:10.1021/ac801626x

    Article  CAS  Google Scholar 

  • Sun LN, Zhang J, Gong FF, Wang X, Hu G, Li SP, Hong Q (2014) Nocardioides soli sp. nov., a carbendazim-degrading bacterium isolated from soil under the long-term application of carbendazim. Int J Syst Evol Microbiol 64:2047–2052. doi:10.1099/ijs.0.057935-0

    Article  CAS  Google Scholar 

  • Teadoum DN, Noumbo SK, Arnaud KT, Ranil TT, Zé ADM, Tonle IK (2016) Square wave voltammetric determination of residues of carbendazim using a Fullerene/Multiwalled carbon nanotubes/Nafion®/coated glassy carbon electrode. Int J Electrochem. doi:10.1155/2016/7839708

    Google Scholar 

  • Tian L, Chen F (2009) Characterization of a carbendazim-degrading Trichoderma sp. T2-2 and its application in bioremediation. Wei Sheng Wu Xue Bao 49:925–930

    CAS  Google Scholar 

  • Torstensson L, Wessen B (1984) Interactions between the fungicide benomyl and soil microorganisms. Soil Biol Biochem 16:445–452. doi:10.1016/0038-0717(84)90050-6

    Article  CAS  Google Scholar 

  • Tortella GR, Mella-Herrera RA, Sousa DZ, Rubilar O, Briceño G, Parra L, Diez MC (2013) Carbendazim dissipation in the biomixture of on-farm biopurification systems and its effect on microbial communities. Chemosphere 93:1084–1093

    Article  CAS  Google Scholar 

  • Van Wijngaarden RPA, Crum SJH, Decraene K, Hattink J, Van Kammen A (1998) Toxicicity of derosal (active ingredient carbendazim) to aquatic invertebrates. Chemosphere 37:673–683. doi:10.1016/S0045-6535(98)00083-6

    Article  Google Scholar 

  • Wang X, Song M, Gao C, Dong B, Zhang Q, Fang H, Yu Y (2009a) Carbendazim induces a temporary change in soil bacterial community structure. J Environ Sci (China) 21:1679–1683. doi:10.1016/S1001-0742(08)62473-0

    Article  CAS  Google Scholar 

  • Wang YS, Huang YJ, Chen WC, Yen JH (2009b) Effect of carbendazim and pencycuron on soil bacterial community. J Hazard Mat 172:84–91. doi:10.1016/j.jhazmat.2009.06.142

    Article  CAS  Google Scholar 

  • Wang Z, Xu J, Li Y, Wang K, Wang Y, Hong Q, Li WJ, Li SP (2010a) Rhodococcus jialingiae sp. nov., an actinobacterium isolated from sludge of a carbendazim wastewater treatment facility. Int J Syst Evol Microbiol 60:378–381. doi:10.1099/ijs.0.013219-0

    Article  CAS  Google Scholar 

  • Wang Z, Wang Y, Gong F, Zhang J, Hong Q, Li S (2010b) Biodegradation of carbendazim by a novel actinobacterium Rhodococcus jialingiae djl-6-2. Chemosphere 81:639–644. doi:10.1016/j.chemosphere.2010.08.040

    Article  CAS  Google Scholar 

  • Wang X, Song M, Wang Y, Gao C, Zhang Q, Chu X, Fang H, Yu Y (2012) Response of soil bacterial community to repeated applications of carbendazim. Ecotoxicol Environ Saf 75:33–39. doi:10.1016/j.ecoenv.2011.08.014

    Article  CAS  Google Scholar 

  • Wang C, Wang F, Zhang Q, Liang W (2016) Individual and combined effects of tebuconazole and carbendazim on soil microbial activity. Eur J Soil Biol 72:6–13. doi:10.1016/j.ejsobi.2015.12.005

    Article  CAS  Google Scholar 

  • Wu YS, Lee HK, Li SFY (1997) Determination of carbendazim residues in grains by solid-phase extraction and micellar electrokinetic chromatography with ultraviolet detection. J Chromatogr Sci 35(11):513–518. doi:10.1093/chromsci/35.11.513

    Article  CAS  Google Scholar 

  • Xiao W, Wang H, Li T, Zhu Z, Zhang J, He Z, Yang X (2013) Bioremediation of Cd and carbendazim co-contaminated soil by Cd-hyperaccumulator Sedum alfredii associated with carbendazim-degrading bacterial strains. Environ Sci Pollut Res 20:380–389. doi:10.1007/s11356-012-0902-4

    Article  CAS  Google Scholar 

  • Xu JL, Wang ZC, Wang K, Li SP (2006) The isolation identification and degradation characters of an efficient carbendazim-degrading bacterium. China Environ Sci 26(3):307–310

    CAS  Google Scholar 

  • Xu JL, He J, Wang ZC, Wang K, Li WJ, Tang SK, Li SP (2007) Rhodococcus qingshengii sp. nov., a carbendazim-degrading bacterium. Int J Syst Evol Microbiol 57:2754–2757. doi:10.1099/ijs.0.65095-0

    Article  CAS  Google Scholar 

  • Yan H, Wang D, Dong B, Tang F, Wang B, Fang H, Yu Y (2011) Dissipation of carbendazim and chloramphenicol alone and in combination and their effects on soil fungal: bacterial ratios and soil enzyme activities. Chemosphere 84:634–641. doi:10.1016/j.chemosphere.2011.03.038

    Article  CAS  Google Scholar 

  • Yarden O, Katan J, Aharonson N, Ben-Yephet Y (1985) Delayed and enhanced degradation of benomyl and carbendazim in disinfected and fungicide-treated soils. Phytopathol 75:763–777

    Article  CAS  Google Scholar 

  • Yarden O, Salomon R, Katan J, Aharonson N (1990) Involvement of fungi and bacteria in enhanced and nonenhanced biodegradation of carbendazim and other benzimidazole compounds in soil. Can J Microbiol 36:15–23. doi:10.1139/m90-004

    Article  CAS  Google Scholar 

  • Yenjerla M, Cox C, Wilson L, Jordan MA (2009) Carbendazim inhibits cancer cell proliferation by suppressing microtubule dynamics. J Pharmacol Exp Ther 328:390–398. doi:10.1124/jpet.108.143537

    Article  CAS  Google Scholar 

  • Yoon CS, Jin JH, Park JH, Yeo CY, Kim SJ, Hwang YG, Hong SJ, Cheong SW (2008) Toxic effects of carbendazim and n-butyl isocyanate, metabolites of the fungicide benomyl, on early development in the African clawed frog, Xenopus laevis. Environ Toxicol 23:131–144. doi:10.1002/tox.20338

    Article  CAS  Google Scholar 

  • Yunlong YU, Xiaoqiang CHU, Guohui PANG, Xiang Y, Hua FANG (2009) Effects of repeated applications of fungicide carbendazim on its persistence and microbial community in soil. J Environ Sci 21(2):179–185. doi:10.1016/S1001-0742(08)62248-2

    Article  CAS  Google Scholar 

  • Zamora DP, Galera MM, Frenich AG, Vidal JM (2000) Trace determination of carbendazim, fuberidazole and thiabendazole in water by application of multivariate calibration to cross-sections of three-dimensional excitation–emission matrix fluorescence. Analyst 125(6):1167–1174. doi:10.1039/A909886K

    Article  CAS  Google Scholar 

  • Zhang GS, Jia XM, Cheng TF, Ma XH, Zhao YH (2005) Isolation and characterization of a new carbendazim-degrading Ralstonia sp. strain. World J Microbiol Biotechnol 21:265–269. doi:10.1007/s11274-004-3628-8

    Article  CAS  Google Scholar 

  • Zhang L, Qiao X, Ma L (2009) Influence of environmental factors on degradation of carbendazim by Bacillus pumilus strain NY97-1. Int J Environ Pollut 38:309–317. doi:10.1504/IJEP.2009.027231

    Article  CAS  Google Scholar 

  • Zhang X, Huang Y, Harvey PR, Li H, Ren Y (2013) Isolation and characterization of carbendazim-degrading Rhodococcus erythropolis djl-11. PLoS One 8:1–6. doi:10.1371/journal.pone.0074810

    CAS  Google Scholar 

  • Zhu SH, Wu HL, Li BR, Xia AL, Han QJ, Zhang Y, Yu RQ (2008) Determination of pesticides in honey using excitation–emission matrix fluorescence coupled with second-order calibration and second-order standard addition methods. Anal Chim Acta 619:165–172. doi:10.1016/j.aca.2008.05.005

    Article  CAS  Google Scholar 

  • Zubrod JP, Baudy P, Schulz R, Bundschuh M (2014) Effects of current-use fungicides and their mixtures on the feeding and survival of the key shredder Gammarus fossarum. Aquatic Toxicol 150:133–143. doi:10.1016/j.aquatox.2014.03.002

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joginder Singh.

Ethics declarations

Conflicts of interest

Authors declare that no conflicts of interest exist.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Singh, S., Singh, N., Kumar, V. et al. Toxicity, monitoring and biodegradation of the fungicide carbendazim. Environ Chem Lett 14, 317–329 (2016). https://doi.org/10.1007/s10311-016-0566-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10311-016-0566-2

Keywords

Navigation