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Environmental Science and Pollution Research

, Volume 25, Issue 11, pp 10371–10382 | Cite as

Acute toxicity of chemical pesticides and plant-derived essential oil on the behavior and development of earthworms, Eudrilus eugeniae (Kinberg) and Eisenia fetida (Savigny)

  • Prabhakaran Vasantha-Srinivasan
  • Sengottayan Senthil-Nathan
  • Athirstam Ponsankar
  • Annamalai Thanigaivel
  • Muthiah Chellappandian
  • Edward-Sam Edwin
  • Selvaraj Selin-Rani
  • Kandaswamy Kalaivani
  • Wayne B. Hunter
  • Veeramuthu Duraipandiyan
  • Naif Abdullah Al-Dhabi
Plant-borne compounds and nanoparticles: challenges for medicine, parasitology and entomology

Abstract

Comparative toxicity of two chemical pesticides (temephos and monocrotophos) versus a plant-derived betel leaf oil Piper betle (L.) to earthworm Eudrilus eugeniae (Kinberg) and redworm Eisenia fetida Savigny, historically: Eisenia foetida (Savigny 1826), was evaluated. Mortality rate was more prominent in temephos at 100 μg concentration to both the earthworms in filter paper test (FPT) as well as 10 mg concentration in artificial soil test (AST). In contrast, P. betle does not display much mortality rate to both the earthworms even at 1000 mg of treatment concentrations. The lethal concentration (LC50) value was observed at 3.89 and 5.26 mg/kg for temephos and monocrotophos against E. eugeniae and 3.81 and 5.25 mg/kg to E. fetida, respectively. Whereas, LC50 value of betel leaf oil was only observed at 3149 and 4081 mg/kg to E. eugeniae and E. fetida, respectively. Correspondingly, the avoidance or attraction assay also displayed that earthworms were more sensitive to the soil containing chemical pesticides. Whereas, the avoidance percentage was decreased in the P. betle oil. Similarly, sublethal concentration of chemical pesticides (5 and 6.5 mg) significantly reduced the earthworm weight and growth rate. However, P. betle oil did not change the developmental rate in the duration of the assay (2, 7 and 14 days) even at 4000 mg treatment concentration. The enzyme ratio of CAT and SOD was also affected significantly after exposure to the chemical pesticides (6.5 mg/kg). Hence, our study implied the risk assessment associated with the chemical pesticides and also recommends plant-derived harmless P. betle oil against beneficial species as an alternative pest control agent.

Keywords

Temephos Monocrotophos Earthworm Growth rate Enzyme 

Notes

Acknowledgements

The project was fully financially supported by the King Saud University through the Vice Deanship of Research Chairs.

Compliance with ethical standards

Disclaimer

The use or mention of a trademark or proprietary product does not constitute an endorsement, guarantee, or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other suitable products.

References

  1. Anamika R, Bajpai J, Bajpai AK (2008) Development of calcium alignate-gelatin based microspheres for controlled release of endosulfan as a model pesticide. Indian J Chem Technol 16:388–395Google Scholar
  2. Andrade, CE, Hunter WB (2016) RNA Interference–Natural Gene-Based Technology for Highly Specific Pest Control (HiSPeC). IY Abdurakhmonov (Croatia: InTech) 391–409Google Scholar
  3. Andres MF, Gonzalez-Coloma A, Sanz J, Burillo J, Sainz P (2013) Nematicidal activity of essential oils: a review. Phytochem Rev 11:371–390CrossRefGoogle Scholar
  4. Avery PB, Wekesa VW, Hunter WB, Hall DG, McKenzie CL, Osborne LS, Powell CA, Rogers ME (2011) Effects of the fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) on reduced feeding and mortality of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol Sci Tech 21:1065–1078CrossRefGoogle Scholar
  5. Bachman PM, Huizinga KM, Jensen PD, Mueller G, Tan J, Uffman JP, Levine SL (2016) Ecological risk assessment for DvSnf7 RNA: a plant-incorporated protectant with targeted activity against western corn rootworm. Regul Toxicol Pharmacol 81:77–88CrossRefGoogle Scholar
  6. Benelli G, Flamini G, Canale A, Molffeta I, Cioni PL, Conti B (2012) Repellence of Hyptis suaveolens whole essential oil and, major constituents against adults of the granary weevil Sitophilus granarius. Bull Insect 65:177–183Google Scholar
  7. Bradford MM (1976) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  8. Caburian AB, Osi MO (2010) Characterization and evaluation of antimicrobial activity of the essential oil from the leaves of Piper betle L. E-Int Sci Res J 2:2–13Google Scholar
  9. Chen C, Wang Y, Zhao X, Qian Y, Wang Q (2014) Combined toxicity of butachlor, atrazine and k-cyhalothrin on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Chemosphere 112:393–401CrossRefGoogle Scholar
  10. Coats JR (1994) Risks from natural versus synthetic insecticides. Annu Rev Entomol 39:489–515CrossRefGoogle Scholar
  11. Dammini-Premachandra WTS, Mampitiyarachchi H, Ebssa L (2014) Nematotoxic potential of betel (Piper betle L.) (Piperaceae) leaf. Crop Prot 65:1–5CrossRefGoogle Scholar
  12. Diao J, Xu P, Liu D, Lu Y, Zhou Z (2011) Enantiomer-specific toxicity and bioaccumulation of alpha-cypermethrin to earthworm Eisenia fetida. J Haz Mat 192:1072–1078CrossRefGoogle Scholar
  13. Edwards CA, Bohlen PJ (1992) The effects of toxic chemicals on earthworms. Rev Environ Contam Toxicol 125:23–99Google Scholar
  14. Edwin E, Vasantha-Srinivasan P, Senthil-Nathan S, Thanigaivel A, Ponsankar A, Selin-Rani S, Kalaivani K, Hunter WB, Duraipandiyan V, Al-Dhabi NA (2016) Effect of andrographolide on phosphatases activity and cytotoxicity against Spodoptera litura. Invert Sur J 13:153–163Google Scholar
  15. Fourie F, Reinecke SA, Reinecke AJ (2007) The determination of earthworm species sensitivity differences to cadmium genotoxicity using the comet assay. Ecotoxicol Environ Saf 67:361–368CrossRefGoogle Scholar
  16. Garcia M, Rombke J, de Brito MT, Scheffczyk A (2008) Effects of three pesticides on the avoidance behavior of earthworms in laboratory tests performed under temperate and tropical conditions. Environ Pollut 153:450–456CrossRefGoogle Scholar
  17. Grumiaux F, Demuynck S, Schikorski D, Lemiere S, Lepretre A (2010) Assessing the effects of FBC ash treatments of metal-contaminated soils using life history traits and metal bioaccumulation analysis of the earthworm Eisenia andrei. Chemosphere 79:156–161CrossRefGoogle Scholar
  18. Hunter WB, Glick E, Paldi N, Bextine BR (2012) Advances in RNA interference: dsRNA treatment in trees and grapevines for insect pest population suppression. Southwest Entomol 37(1):85–87CrossRefGoogle Scholar
  19. ISO, International Organization for Standardization (2006) Draft ISO-17512: soil quality-avoidance test for evaluating the quality of soils and the toxicity of chemicals. Test with earthworms (Eisenia fetida/andrei), Geneva, SwitzerlandGoogle Scholar
  20. James C (2015) Global status of commercialized biotech/GM crops: 2015. ISAAA Brief No. 51. ISAAA: Ithaca, NY. http://www.isaaa.org/resources/publications/briefs/51/default.asp
  21. Kareru P, Rotich ZK, Maina, EW (2013) Use of botanicals and safer insecticides designed in controlling insects: the African case. InTech. 297–309Google Scholar
  22. Kinney CA, Campbell BR, Thompson R, Furlong ET, Kolpin DW, Burkhardt MR, Zaugg SD, Werner SL, Hay AG (2012) Earthworm bioassays and seedling emergence for monitoring toxicity, aging and bioaccumulation of anthropogenic waste indicator compounds in bio solids-amended soil. Sci Total Environ 433:507–515CrossRefGoogle Scholar
  23. Liu J, Xiong K, Ye X, Zhang J, Yang Y, Ji L (2015) Toxicity and bioaccumulation of bromadiolone to earthworm Eisenia fetida. Chemosphere 135:250–256CrossRefGoogle Scholar
  24. Ma WC, Bodt J (1993) Differences in toxicity of the insecticide chlorpyrifos to six species of earthworm (Oligochaeta: Lumbricidae) in standardized soil test. Bull Environ Contam Toxicol 50:864–890CrossRefGoogle Scholar
  25. Mithofer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450CrossRefGoogle Scholar
  26. Miyazaki A, Amano T, Saito H, Nakano Y (2002) Acute toxicity of chlorophenols to earthworms using a simple paper contact method and comparison with toxicities to fresh water organisms. Chemosphere 47:65–69CrossRefGoogle Scholar
  27. Mohottalage S, Tabacchi R, Guerin PM (2007) Components from Sri Lankan Piper betle L. leaf oil and their analogues showing toxicity against the housefly, Musca domestica. Flavour Fragr J 22:130–138CrossRefGoogle Scholar
  28. Mugisha-Kamatenesi M, Deng AL, Ogendo JO, Omolo EO, Mihale MJ, Otim M, Buyungo JP, Bett PK (2008) Indigenous knowledge of field insect pests and their management around Lake Victoria basin in Uganda. Afr J Environ Sci Technol 2:342–348Google Scholar
  29. Nattudurai G, Vendan SE, Ramachandran PV, Lingathurai S (2014) Vermicomposing of coirpith with cow dung by Eudrilus eugeniae Kinberg and its efficacy on the growth of Cyamopsis tetragonaloba (L) Taub. J Saudi Soc Agri Sci 13:23–27Google Scholar
  30. Navarro MJ, Hautea RA, Huang J, Mayee C, Torres CS, Wang X, Choudhary B, Daya RA (2014) Adoption and uptake pathways of GM/Biotech crops by small-scale, resource-poor farmers in China, India, and the Philippines. ISAAA Briefs 48Google Scholar
  31. Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378CrossRefGoogle Scholar
  32. OECD (1984) Guideline for testing of chemicals no. 207. Earthworm, acute toxicity tests, OECD—guideline for testing chemicals. Paris, FranceGoogle Scholar
  33. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21(12):1000–1007Google Scholar
  34. Pelosi C, Joimel S, Makowski D (2013) Searching for a more sensitive earthworm species to be used in pesticide homologation tests—a meta-analysis. Chemosphere 90:895–900CrossRefGoogle Scholar
  35. Ponsankar A, Vasantha-Srinivasan P, Senthil-Nathan S, Thanigaivel A, Edwin E, Selin-Rani S, Kalaivani K, Hunter WB, Alessandro RT, Abel-Megeed A, Paik C, Duraipandiyan V, Al-Dhabi NA (2016) Target and non-target toxicity of botanical insecticide derived from Couroptia guianensis L. flower against generalist herbivore, Spodoptera litura Fab. and an earthworm, Eisenia foetida Savigny. Ecotoxicol Environ Saf 133:260–270CrossRefGoogle Scholar
  36. Poorjavad N, Goldansaz SH, Dadpour H, Khajehali J (2014) Effect of Ferula assafoetida essential oil on some biological and behavioral traits of Trichogramma embryophagum and T. evanescens. Biol Control 59:403–413Google Scholar
  37. Porretta D, Gargani M, Bellini R, Medici A, Punelli F, Urbanelli S (2008) Defense mechanisms against insecticides temephos and diflubenzuron in the mosquito Aedes caspius: the P-glycoprotein efflux pumps. Med Vet Entomol 22:48–54CrossRefGoogle Scholar
  38. Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protect 29:913–920CrossRefGoogle Scholar
  39. Revathi K, Chandrasekaran R, Kirubakaran SA, Senthil-Nathan S (2014) Biocontrol efficacy of protoplast fusants between Bacillus thuringiensis and Bacillus subtilis against Spodoptera litura Fabr. Arch Phytopathol Plant Prot 47:1365–1375CrossRefGoogle Scholar
  40. Scott JG, Michel K, Bartholomay L, Siegfried BD, Hunter WB, Smagghe G, Zhu KY, Douglas AE (2013) Towards the elements of successful insect RNAi. J Insect Physiol 59:1212–1221CrossRefGoogle Scholar
  41. Selin-Rani S, Senthil-Nathan S, Revathi K, Chandrasekaran R, Thanigaivel A, Vasantha-Srinivasan P, Ponsankar A, Edwin E, Pradeepa V (2016) Toxicity of Alangium salvifolium Wang chemical constituents against the tobacco cutworm Spodoptera litura Fab. Pest Biochem Phys 126:92–101CrossRefGoogle Scholar
  42. Senthil-Nathan S (2007) The use of Eucalyptus tereticornis Sm. (Myrtaceae) oil (leaf extract) as a natural larvicidal agent against the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Bioresour Technol 98:1856–1860Google Scholar
  43. Senthil-Nathan S (2013) Physiological and biochemical effect of Neem and other Meliaceae plants secondary metabolites against Lepidopteran insects. Front Physiol 4:1–17CrossRefGoogle Scholar
  44. Senthil-Nathan S (2015) A review of bio pesticides and their mode of action against insect pests. In: Environmental Sustainability- Role of Green Technologies, Springer-Verlag, pp.49–63Google Scholar
  45. Senthil-Nathan S, Kalaivani K (2006) Combined effects of azadirachtin and nucleopolyhedrovirus (SpltNPV) on Spodoptera litura Fabricius (Lepidoptera:Noctuidae) larvae. Biol Control 36:94–104Google Scholar
  46. Senthil-Nathan S, Choi MY, Seo HY, Paik CH, Kalaivani K, Kim JD (2008) Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown plant hopper Nilaparvata lugens (Stal). Ecotoxicol Environ Saf 70:244–250CrossRefGoogle Scholar
  47. Senthil-Nathan S, Choi MY, Paik CH, Seo HY, Kalaivani K (2009) Toxicity and physiological effects of neem pesticides applied to rice on the Nilaparvata lugens Stål, the brown planthopper. Ecotoxicol Environ Saf 72:1707–1713CrossRefGoogle Scholar
  48. Silva WJ, Doria GAA, Maia RT, Nunes RS, Carvalho GA, Blank AF, Alves PB, Marcal RM, Cavalcanti SCH (2008) Effects of essential oils on Aedes aegypti larvae: alternatives to environmentally safe insecticides. Bioresour Technol 99:3251–3255CrossRefGoogle Scholar
  49. Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biol Biochem 41:905–909CrossRefGoogle Scholar
  50. Tripathi G, Kachhwaha N, Dabi I (2010) Comparative studies on carbofuran-induced changes in some cytoplasmic and mitochondrial enzymes and proteins of epigeic, anecic and endogeic earthworms. Pest Biochem Physiol 96:30–35CrossRefGoogle Scholar
  51. Tufts DM, Spencer K, Hunter WB, Bextine BR (2011) Delivery system using sodium alginate virus loaded pellets to red imported fire ants (Solenopsis invicta, Hymenoptera: Formicidae). Florida Entomol 94(2):237–241CrossRefGoogle Scholar
  52. USDA (2009) Natural Resources Conservation Services, NRCS, Soil quality indicator sheetsGoogle Scholar
  53. USDA (2015) Natural Resources Conservation Services, Soil quality indicator sheetsGoogle Scholar
  54. Vasantha-Srinivasan P, Senthil-Nathan S, Thanigaivel A, Edwin E, Ponsankar A, Selin-Rani S, Pradeepa V, Sakthi-Bagavathy M, Kalaivani K, Hunter WB, Duraipandiyan V, Al-Dhabi NA (2016) Developmental response of Spodoptera litura Fab. to treatments of crude volatile oil from Piper betle L. and evaluation of toxicity to earthworm, Eudrilus eugeniae Kinb. Chemosphere 155:336–347CrossRefGoogle Scholar
  55. Viljoen SA, Reinecke AJ (1992) The temperature requirement of the epigeic earthworm species Eudrilus eugeniae (Oligochaeta)—a laboratory study. Soil Biol Biochem 24:1345–1350CrossRefGoogle Scholar
  56. Wang Y, Cang T, Zhao X, Yu R, Chen L, Wu C, Wang Q (2012) Comparative acute toxicity of twenty-four insecticides to earthworm, Eisenia fetida. Ecotoxicol Environ Saf. doi: 10.1016/j.ecoenv.2011.12.016
  57. Wang K, Mu X, Qi S, Chai T, Pang S, Yang Y, Wang C, Jiang J (2015) Toxicity of a neonicotinoid insecticide, guadipyr, in earthworm (Eisenia fetida). Ecotoxicol Environ Saf 114:17–22CrossRefGoogle Scholar
  58. World Health Organization (2009) Health implications from monocrotophos use: a review of the evidence in India. South-East Asia. Revision 2013. ISBN 978-92-9022-345-0Google Scholar
  59. Yoon M, Cha B, Kim J (2013) Recent trends in studies on botanical fungicides in agriculture. Plant Pathol J 29:1–9CrossRefGoogle Scholar
  60. Zaka SM, Abbas N, Shad SA, Shah RM (2014) Effect of emamectin benzoate on life history traits and relative fitness of Spodoptera litura (Lepidoptera: Noctuidae). Phytoparasitica 42:493–501CrossRefGoogle Scholar
  61. Zelikoff JT, Wang W, Islam N, Twerdok LE, Curry M, Beaman J, Flescher E (1996) Assays of reactive oxygen intermediates and antioxidant enzymes: potential biomarkers for predicting effects of environmental pollution. In: Ostrander GK (ed) Techniques in aquatic toxicology. Lewis Publishers, Boca Raton, pp 287–306Google Scholar
  62. Zhang F, Wang Y, Lou Z, Dong J (2007) Effect of heavy metal stress on anti-oxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Prabhakaran Vasantha-Srinivasan
    • 1
  • Sengottayan Senthil-Nathan
    • 1
  • Athirstam Ponsankar
    • 1
  • Annamalai Thanigaivel
    • 1
  • Muthiah Chellappandian
    • 1
  • Edward-Sam Edwin
    • 1
  • Selvaraj Selin-Rani
    • 1
  • Kandaswamy Kalaivani
    • 2
  • Wayne B. Hunter
    • 3
  • Veeramuthu Duraipandiyan
    • 4
  • Naif Abdullah Al-Dhabi
    • 4
  1. 1.Division of Biopesticides and Environmental Toxicology, Sri Paramakalyani Centre for Excellence in Environmental SciencesManonmaniam Sundaranar UniversityTirunelveliIndia
  2. 2.Post Graduate and Research Centre, Department of ZoologySri Parasakthi College for WomenTirunelveliIndia
  3. 3.United States Department of Agriculture, Agricultural Research Service, U.S. Horticultural Research LaboratoryFort PierceUSA
  4. 4.Department of Botany and Microbiology, Addiriyah Chair for Environmental Studies, College of ScienceKing Saud UniversityRiyadhSaudi Arabia

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