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Development of an eco-friendly mosquitocidal agent from Alangium salvifolium against the dengue vector Aedes aegypti and its biosafety on the aquatic predator

Abstract

Plant extracts with their enriched chemical constituents have established potential alternative mosquito control agents. In this research, we developed an eco-friendly mosquitocidal agent from Alangium salvifolium leaves against the dengue and Zika virus vector Aedes aegypti and we investigated its biosafety on the mosquito aquatic predator Toxorhynchites splendens. Results showed that the methanolic extract of A. salvifolium leaves was composed by eight main compounds, with major peak area for hexadecenoic acid (21.74%). LC50 and LC90 values calculated on Ae. aegypti fourth instar larvae were 104.80 and 269.15 ppm respectively. The methanolic extract tested at 100 ppm decreased the α-β carboxylesterase and SOD ratio significantly and upregulated the GST and CYP450 level. The A. salvifolium methanolic extract displayed significant repellent and adulticidal activity at 100 and 400 ppm respectively. The treatment with 100 ppm of the methanolic extract led to 210 min of protection from Ae. aegypti bites. Four hundred parts per million of the extract showed 98% adult mortality within 30 min from the treatment. Lastly, biosafety assays on the mosquito aquatic predator Tx. splendens showed that the toxicity of the A. salvifolium extract was significantly lower if compared to the cypermethrin-based treatments. The methanolic extract of A. salvifolium showed a maximum of 47.3% mortality rate at the concentration of 1000 ppm, while 0.7 ppm of cypermethrin achieved 91.3% mortality rate on Tx. splendens. Overall, our study enhances basic knowledge on how to improve natural larvicidal agents against dengue and Zika virus mosquito vector with harmless responses on non-target aquatic predators.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Article  Google Scholar 

  • Agra-Neto AC, Napoleão TH, Pontual EV, Santos NDL, Luz LA, Oliveira CMF, Melo-Santos MAV, Coelho LCBB, Navarro DMAF, Paiva PMG (2015) Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res 113:175–184

    Article  Google Scholar 

  • Benelli G (2015) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805

    Article  Google Scholar 

  • Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754

    Article  Google Scholar 

  • Boyer S, David JP, Rey D, Lemperiere G, Ravenel P (2005) Response of Aedes aegypti (Diptera: Culicidae) larvae to three xenobiotic exposures: larval tolerance and detoxifying enzyme activities. Environ Toxicol Chem 25:470–476

    Article  Google Scholar 

  • Caballero C, López-Olguín JL, Ruiz M, Ortego F, Castañera P (2008) Antifeedant activity and effects of terpenoids on detoxification enzymes of the beet armyworm, Spodoptera exigua (Hübner). Span J Agric Res 6:177–184

    Article  Google Scholar 

  • Cheng SS, Lin CY, Chung MJ, Liu YH, Huang CG, Chang ST (2013) Larvicidal activities of wood and leaf essential oils and ethanolic extracts from Cunninghamia konishii Hayata against the dengue mosquitoes. Ind Crop Prod 47:310–315

    CAS  Article  Google Scholar 

  • Choochote W, Chaithong U, Kamsuk K, Rattanachanpichai E, Jitpakdi A, Tippawangkosol P (2006) Adulticidal activity against Stegonyia aegypti (Diptera: Culicidae) of three Piper spp. Rev Do Insti De Med Trop De Sao Pau 48:33–37

    Article  Google Scholar 

  • Clark AG (1990) The glutathione S-transferases and resistance to insecticides. In: Hayes JD, Pickett CD, Mantle TJ (eds) Glutathione S-transferases and drug resistance. Taylor and Francis, London, pp 369–379

    Google Scholar 

  • David JP, Faucon F, Chandor-Proust A, Poupardin R, Riaz MA, Bonin A, Navratil V, Reynaud S (2014) Comparative analysis of response to selection with three insecticides in the dengue mosquito Aedes aegypti using mRNA sequencing. BMC Genomics 15:174

    Article  Google Scholar 

  • Dua VK, Alam MF, Pandey AC, Rai S, Chopra AK, Kaul VK (2008) Insecticidal activity of Valeriana jatamansi (Verbenaceae) against mosquitoes. J Am Mosq Control Assoc 24:315–318

    CAS  Article  Google Scholar 

  • Edwin E, Vasantha-Srinivasan P, Senthil-Nathan S, Thanigaivel A, Ponsankar A, Pradeepa V, Selin-Rani S, Kalaivani K, Hunter WB, Abdel-Megeed A, Duraipandiyan V, Al-Dhabi NA (2016) Anti-dengue efficacy of bioactive andrographolide from Andrographis paniculata (Lamiales: Acanthaceae) against the primary dengue vector Aedes aegypti (Diptera: Culicidae). Acta Trop 163:167–178

  • Erland LAE, Rheault MR, Mahmoud SS (2015) Insecticidal and oviposition deterrent effects of essential oils and their constituents against the invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). Crop Prot 78:20–26

    CAS  Article  Google Scholar 

  • Finney DJ (1971) Probit analysis. 3rd ed., Cambridge University Press, Cambridge

  • Ghosh A, Chowdhury N, Chandra G (2012) Plant extracts as potential mosquito larvicides. Indian J Med Res 135:581–598

    CAS  Google Scholar 

  • Gillij YG, Gleiser RM, Zygadlo JA (2008) Mosquito repellent activity of essential oils of aromatic plants growing in Argentina. Bioresour Technol 99:2507–2515

    CAS  Article  Google Scholar 

  • Govindarajan M, Sivakumar R (2012) Adulticidal and repellent properties of indigenous plant extracts against Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Parasitol Res 110:1607–1620

    Article  Google Scholar 

  • Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martínez E, Nathan MB (2010) Dengue: a continuing global threat. Nature Rev Microbiol 1:8:S7–16

  • Hung TM, Dang NH, Kim JS, Choi JS, Lee HK, Min BS (2009) Phenolic glycosides from Alangium salviifolium leaves with inhibitory activity on LPS-induced NO, PGE2, and TNF-α production. Bioorg Med Chem Lett 19:4389–4393

    CAS  Article  Google Scholar 

  • Kalaivani K, Senthil-Nathan S, Murugesan AG (2012) Biological activity of selected Lamiaceae and Zingiberaceae plant essential oils against the dengue vector Aedes aegypti L. (Diptera: Culicidae). Parasitol Res 110:1261–1268

    Article  Google Scholar 

  • Koodalingam A, Mullainadhan P, Arumugam M (2011) Effects of extract of soapnut Sapindus emarginatus on esterases and phosphatases of the vector mosquito, Aedes aegypti (Diptera: Culicidae). Acta Trop 118:27–36

    CAS  Article  Google Scholar 

  • Kraemer MUG, Sinka ME, Duda KA, Mylne A, Shearer FM, Brady OJ, Messina JP, Barker CM, Moore CG, Carvalho RG, Coelho GE, Bortel WV, Hendrickx G, Schaffner F, William-Wint GR, Elyazer IRF, Teng H, Hay SI (2015) The global compendium of Aedes aegypti and Ae. albopictus occurrence. Science Data 2:150035. doi:10.1038/sdata.2015.35

    Article  Google Scholar 

  • Larson RT, Lorch JM, Pridgeon JW, Becnel JJ, Clark GG (2010) The biological activity of α-mangostin, a larvicidal otanic mosquito sterol carrier protein-2 inhibitor. J Med Entomol 47(2):249–257

    CAS  Google Scholar 

  • Lee SE, Lee BH, Choi WS, Park BS, Kim JG, Campbell BC (2001) Fumigant toxicity of volatile natural products from Korean spices and medicinal plants towards the rice weevil, Sitophilus oryzae (L.) Pest Manag Sci 57:548–553

    CAS  Article  Google Scholar 

  • Lek-Uthai U, Rattanapreechachai P, Chowanadisai L (2011) Bioassay and effective concentration of Temephos against Aedes aegypti larvae and the adverse effect upon indigenous predators: Toxorhynchites splendens and Micronecta sp. Asia J Public Health 2(2):67–77

    Google Scholar 

  • Lija-Escaline J, Senthil-Nathan S, Thanigaivel A, Pradeepa V, Vasantha-Srinivasan P, Ponsankar A, Edwin E, Selin-Rani S, Abdel-Megeed A (2015) Physiological and biochemical effects of chemical constituents from Piper nigrum Linn (Piperaceae) against the dengue vector Aedes aegypti Liston (Diptera: Culicidae). Parasitol Res 114(11):4239–4249

    Article  Google Scholar 

  • Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, Prapanthadara L, Somboon P, Lycett G, Ranson H (2011) The role of the Aedes aegypti Epsilon glutathione transferases in conferring. Insect Biochem Mol Biol 41:203–209

    CAS  Article  Google Scholar 

  • Napoleão TH, Pontual EV, Lima TA, Santos NDL, Sá RA, Coelho LCBB, Navarro DMAF, Paiva PMG (2012) Effect of Myracrodruon urundeuva leaf lectin on survival and digestive enzymes of Aedes aegypti larvae. Parasitol Res 110:609–616

    Article  Google Scholar 

  • Pates H, Curtis C (2005) Mosquito behavior and vector control. Annu Rev Entomol 50:53–70

    CAS  Article  Google Scholar 

  • Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187

    CAS  Article  Google Scholar 

  • Pavela R, Benelli G (2016) Essential oils as eco-friendly biopesticides. Challenges and constraints Tr Plant Sci. doi:10.1016/j. tplants.2016.10.005

    Google Scholar 

  • 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 133:260–270

    CAS  Article  Google Scholar 

  • Pratt HD (1959) A new classification of the life histories of North American mosquitoes. Proceedings of the New Jersey Mosquito Exterminators Association 46:148–152

    Google Scholar 

  • Ravindran J, Samuel T, Alex E, William J (2012) Adulticidal activity of Ageratum houstonianum Mill. (Asteraceae) leaf extracts against three vector mosquito species (Diptera: Culicidae). Asian Pac J Trop Dis 177–179

  • Reegan AD, Gandhi MR, Paulraj MG, Ignacimuthu S (2015) Ovicidal and oviposition deterrent activities of medicinal plant extracts against Aedes aegypti L. and Culex quinquefasciatus Say mosquitoes (Diptera: Culicidae) Osong. Public Health Res Perspect 6(1):64–69

    Article  Google Scholar 

  • Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-stakes world. Annu Rev Entomol 57:405–424

    CAS  Article  Google Scholar 

  • Rehman JU, Ali A, Khan IA (2014) Plant based products: use and development as repellents against mosquitoes: a review. Fitoterapia 95:65–74

    CAS  Article  Google Scholar 

  • Rodriquez A, Cera DL, Herrero P, Moreno F (2001) The hexokinase 2 protein regulates the expression of the GLK1, HXK1 and HXK2 genes of Saccharomyces cerevisiae. Biochem J 355:625–631

  • Sasaki DY, Jacobowski AC, de Souza AP, Cardoso MH, Franco OL, Macedo MLR (2015) Effects of proteinase inhibitor from Adenanthera pavonina seeds on short- and long term larval development of Aedes aegypti. Biochimie 112:172–186

    CAS  Article  Google Scholar 

  • 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 Physiol 126:92–101

    CAS  Article  Google Scholar 

  • 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 98:1856–1860

    Article  Google Scholar 

  • Senthil-Nathan S (2013) Physiological and biochemical effect of neem and other Meliaceae plants secondary metabolites against Lepidopteran insects. Front Physiol 4(359):1–17

    Google Scholar 

  • Senthil-Nathan S (2015) A review of bio pesticides and their mode of action against insect pests. Environmental Sustainability- Role of Green Technologies, Springer, In, pp 49–63

    Google Scholar 

  • Senthil-Nathan S, Chung PG, Murugan K (2004) Effect of botanical insecticides and bacterial toxins on the gut enzyme of the rice leaffolder Cnaphalocrocis medinalis. Phytoparasitica 32(5):433–443

    Article  Google Scholar 

  • Senthil-Nathan S, Kalaivani K, Murugan K (2005) Effects of neem limonoids on the malaria vector Anopheles stephensi Liston (Diptera: Culicidae). Acta Trop 96:47–55

    Article  Google Scholar 

  • Senthil-Nathan S, Kalaivani K, Sehoon K (2006) Effects of Dysoxylum malabaricum Bedd. (Meliaceae) extract on the malarial vector Anopheles stephensi Liston (Diptera: Culicidae). Bioresour Technol 97:2077–2083

    Article  Google Scholar 

  • Senthil-Nathan S, Hisham A, Jayakumar G (2008) Larvicidal and growth inhibition of the malaria vector Anopheles stephensi by triterpenes from Dysoxylum malabaricum and Dysoxylum beddomei. Fitoterapia 79:106–111

    Article  Google Scholar 

  • Senthil-Nathan S, Choi M-Y, Paik C-H, Seo H-Y, Kalaivani K (2009) Toxicity and physiological effects of neem pesticides applied to rice on the Nilaparvata lugens Stål, the brown planthopper. Ecotoxicol Environ Saf 72:1707–1713

    CAS  Article  Google Scholar 

  • Sivagnaname N, Kalyanasundaram M (2004) Laboratory evaluation of methanolic extract of Atlantia monophylla (Family: Rutaceae) against immature stages of mosquitoes and non-target organisms. Mem Inst Oswaldo Cruz, Rio de Janeiro 99(1):115–118

    CAS  Article  Google Scholar 

  • Tan K, Chen W, Dong S, Liu X, Wang Y, Nieh JC (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One 9:e102725

    Article  Google Scholar 

  • Thanigaivel A, Chandrasekaran R, Revathi K, Nisha S, Sathish-Narayanan S, Kirubakaran SA, Senthil-Nathan S (2012) Larvicidal efficacy of Adhatoda vasica (L.) Nees against the bancroftian filariasis vector Culex quinquefasciatus Say and dengue vector Aedes aegypti L. in in vitro condition. Parasitol Res 110:1993–1999

    Article  Google Scholar 

  • Thanigaivel A, Vasantha-Srinivasan P, Senthil-Nathan S, Edwin E, Ponsankar A, Chellappandian M, Selin-Rani S, Lija-Escaline J, Kalaivani K (2017) Impact of Terminalia chebula Retz. against Aedes aegypti L. and non-target aquatic predatory insects. Ecotoxicol Environ Saf 137:210–217

    CAS  Article  Google Scholar 

  • Vasantha-Srinivasan P, Senthil-Nathan S, Thanigaivel A, Edwin E, Ponsankar A, Selin-Rani S, Pradeepa V, Sakthi-Bhagavathy 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 155:336–347

    CAS  Article  Google Scholar 

  • World Health Organisation (1981) Instruction for determining the susceptibility or resistance of mosquito larvae to insecticides. WHOVBC 81(807):1–6

    Google Scholar 

  • World Health Organization (2005) Guidelines for laboratory and field testing of mosquito larvicides. WHO, Geneva, Switzerland

  • World Health Organization (2009) Guidelines for efficacy testing of mosquito repellents for human skins. WHO: Gevena, pp. 4–18. WHO/CDS/NTD/WHOPES/2009.4

  • World Health Organization (2014) A global brief on vector-borne diseases. WHO, Geneva, Switzerland

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Acknowledgements

Author Annamalai Thanigaivel was supported by the Indian Council of Medical Research (ICMR), Government of India (45/32/2013/BMS/TRM).

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Correspondence to Sengottayan Senthil-Nathan.

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All applicable international and national guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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The authors declare no conflict of interest.

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Thanigaivel, A., Vasantha-Srinivasan, P., Edwin, ES. et al. Development of an eco-friendly mosquitocidal agent from Alangium salvifolium against the dengue vector Aedes aegypti and its biosafety on the aquatic predator. Environ Sci Pollut Res 25, 10340–10352 (2018). https://doi.org/10.1007/s11356-017-9102-6

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Keywords

  • Biocontrol agent
  • Larvicides
  • GST
  • CYP450
  • Oxidative stress
  • Detoxification
  • Yellow fever