Abstract
Mosquito-borne diseases represent a deadly threat for millions of people worldwide. The Culex genus, with special reference to Culex quinquefasciatus, comprises the most common vectors of filariasis across urban and semi-urban areas of Asia. In recent years, important efforts have been conducted to propose green-synthesized nanoparticles as a valuable alternative to synthetic insecticides. However, the mosquitocidal potential of carbon nanoparticles has been scarcely investigated. In this study, the larvicidal and pupicidal activity of carbon nanoparticle (CNP) and silver nanoparticle (AgNP) was tested against Cx. quinquefasciatus. UV–Vis spectrophotometry, Fourier transform infrared (FTIR) spectroscopy, X-ray diffraction (XRD) analysis, scanning electron microscopy (SEM), transmission electron microscopy (TEM), energy-dispersive X-ray (EDX) spectroscopy, and Raman analysis confirmed the rapid and cheap synthesis of carbon and silver nanoparticles. In laboratory assays, LC50 (lethal concentration that kills 50 % of the exposed organisms) values ranged from 8.752 ppm (first-instar larvae) to 18.676 ppm (pupae) for silver nanoparticles and from 6.373 ppm (first-instar larvae) to 14.849 ppm (pupae) for carbon nanoparticles. The predation efficiency of the water bug Lethocerus indicus after a single treatment with low doses of silver and carbon nanoparticles was not reduced. Moderate evidence of genotoxic effects induced by exposure to carbon nanoparticles was found on non-target goldfish, Carassius auratus. Lastly, the plant extract used for silver nanosynthesis was tested for 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2′-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) radical scavenging activity. Overall, our results pointed out that AgNP and CNP can be a candidate for effective tools to reduce larval and pupal populations of filariasis vectors, with reduced genotoxicity and impact on behavioral traits of other aquatic organisms sharing the same ecological niche of Cx. quinquefasciatus.







Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Ali GH, El-Taweel GE, Ali MA (2004) The cytotoxicity and antimicrobial efficiency of Moringa oleifera seeds extracts. Int J Environ Stud 61:699–708
Amer A, Mehlhorn H (2006a) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490
Amer A, Mehlhorn H (2006b) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499
Amer A, Mehlhorn H (2006c) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
Amer A, Mehlhorn H (2006d) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477
Arnao MB, Cano A, Acosta M (2001) The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chem 73:239–244
Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res. doi:10.1007/s00436-015-4586-9
Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114:3201–3212
Benelli G (2016) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res. doi:10.1007/s00436-015-4800-9
Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015) Old ingredients for a new recipe? Neem cake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol Res 114:391–397
Bharali R, Tabassum J, Azad MR (2003) Chemomodulatory effect of Moringa oleifera Lam. on hepatic carcinogen metabolising enzymes, antioxidant parameters and skin papillomagenesis in mice. Asian Pac J Cancer Prev 4:131–139
Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–2000
Bowatte G, Perera P, Senevirathne G, Meegaskumbura S, Meegaskumbura M (2013) Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biol Control 67:469–474
Cárceres A, Saraiva A, Rizzio S, Zabala L, De Leon E, Navy F (1992) Pharmacological properties of Moringa oleifera: screening for antispasmodic, anti-inflammatory and diuretic activity. J Ethnopharmacol 36:233–237
Cavaş T, Könen S (2007) Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis 22(4):263–268
Chandran SP, Chaudhary M, Pasricha R, Ahmad A, Sastry M (2006) Synthesis of gold nanotriangles and silver nanoparticles using Aloe vera plant extract. Biotechnol Prog 22:577–583
Chuang PH, Lee CW, Chou JY, Murugan M, Shieh BJ, Chen HM (2007) Anti-fungal activity of crude extracts and essential oil of Moringa oleifera Lam. Bioresour Technol 98:232–236
Cidamis AB, Panga JT, Sarwatt SV, Chore BE, Shayo NB (2003) Nutrient and antinutrient contents in raw and cooked young leaves and immature pods of Moringa oleifera, Lam. Ecol Food Nutri 42:399–411
Countryman PI, Heddle JA (1976) The production of micronuclei from chromosome aberrations in irradiated cultures of human lymphocytes. Mutat Res 41:321–332
Das J, Paul Das M, Velusamy P (2013) Sesbania grandiflora leaf extract mediated green synthesis of antibacterial silver nanoparticles against selected human pathogens. Spectrochim Acta A Mol Biomol Spectrosc 104:265–270
De Miranda Cabral Gontijo AM, Barreto RE, Speit G, Valenzuela Reyes VA, Volpato GL, Favero Salvadori DM (2003) Anesthesia of fish with benzocaine does not interfere with comet assay results. Mutat Res 534(1-2):165–172
Deguchi Y, Toyoizumi T, Masuda S, Yasuhara A, Mohri S, Yamada M, Inoue Y, Kinae N (2007) Evaluation of mutagenic activities of leachates in landfill sites by micronucleus test and comet assay using goldfish. Mutat Res 627:178–185
Dillard CJ, German JB (2000) Phytochemicals: nutraceuticals and human health: a review. J Sci Food Agric 80:1744–1756
Dinesh D, Murugan K, Madhiyazhagan P, Panneerselvam C, Nicoletti M, Jiang W, Benelli G, Chandramohan B, Suresh U (2015) Mosquitocidal and antibacterial activity of green-synthesized silver nanoparticles from Aloe vera extracts: towards an effective tool against the malaria vector Anopheles stephensi? Parasitol Res 114:1519–1529
Dominko R, Gaberscek M, Drofenik J, Bele M, Jamnik J (2003) Influence of carbon black distribution on performance of oxide cathodes for Li ion batteries. Electrochim Acta 48:3709–3716
Dubey P, Muthukumaran D, Dash S, Mukhopadhyay R, Sarkar S (2005) Synthesis and characterization of water-soluble carbon nanotubes from mustard soot. J Phys 65(4):681–697
Fenech M (1993) The cytokinesis-block micronucleus technique: a detailed description of the method and its application to genotoxicity studies in human populations. Mutat Res 285:35–44
Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University Press, Cambridge
Goodsell DS (2004) Bionanotechnology: lessons from nature. Wiley, Hoboken
Govindarajan M, Benelli G (2016) Facile biosynthesis of silver nanoparticles using Barleria cristata: mosquitocidal potential and biotoxicity on three non-target aquatic organisms. Parasitol Res. doi:10.1007/s00436-015-4817-0
Govindarajan M, Rajeswary M, Veerakumar K, Muthukumaran U, Hoti SL, Mehlhorn H, Barnard DR, Benelli G (2016) Novel synthesis of silver nanoparticles using Bauhinia variegata: a recent eco-friendly approach for mosquito control. Parasitol Res. doi:10.1007/s00436-015-4794-3
Guevara AP, Vargas C, Sakurai H, Fujiwara Y, Hashimoto K, Maoka T, Kozuka M, Ito Y, Tokuda H, Nishino H (1999) An antitumor promoter from Moringa oleifera Lam. Mutat Res 440:181–188
Hafeez F, Akram W, Abdul E, Shaalan S (2011) Mosquito larvicidal activity of citrus limonoids against Aedes albopictus. Parasitol Res 109:221–229
Huang Q, Li D, Sun Y, Lu Y, Su X, Yang H, Wang Y, Wang W, Shao N, Hong J, Chen C (2007) Biosynthesis of silver and gold nanoparticles by novel sundried Cinnamomum camphora leaf. Nanotechnology 18:105104–105114
Kalimuthu K, Lin SM, Tseng LC, Murugan K, Hwang JS (2014) Bio-efficacy potential of seaweed Gracilaria firma with copepod, Megacyclops formosanus for the control larvae of dengue vector Aedes aegypti. Hydrobiologia 741:113–123
Kiruba Daniel SCG, Kumar R, Sathish V, Sivakumar M, Sunitha S, Anitha Sironmani T (2011) Green synthesis (Ocimum tenuiflorum) of silver nanoparticles and toxicity studies in zebra fish (Danio rerio) model. Int J Nano Sci Nanotech 2(2):103–117
Kumar DA, Palanichamy V, Roopan SM (2014) Green synthesis of silver nanoparticles using Alternanthera dentata leaf extract at room temperature and their antimicrobial activity. Spectrochimica Acta A Molecul Biomolecul Spect 127:168–171
Laforgue A, Simon P, Fauvarque JF, Mastragostino M, Soav F, Sarrau JF, Lailler P, Conte M, Rossi E, Saguatti S (2003) Activated carbon/conducting polymer hybrid super capacitors. J Electrochem Soc 150:A645–A651
Lam PKS, Gray JS (2003) The use of biomarkers in environmental monitoring programmes. Mar Pollut Bull 46:182–186
Lee GJ, Shin S, Kim YC, Oh SG (2004) Preparation of silver nanorods through the control of temperature and pH of reaction medium. Mater Chem Phys 84:197–204
Li HT, He XD, Liu Y, Huang H, Lian SY, Lee ST, Kang ZH (2011) One-step ultrasonic synthesis of water-soluble carbon nanoparticles with excellent photoluminescent properties. Carbon 49:605–609
Liu H, Qiu N, Ding H, Yao R (2008) Polyphenols contents and antioxidant capacity of 68 Chinese herbals suitable for medical or food uses. Foodserv Res Int 41:363–370
McCarthy JF, Shugart LR (1990) Biological markers of environmental contamination. In: McCarthy JF, Shugart LR (eds) Biomarkers of environmental contamination. Lewis, Boca Raton, pp 3–14
Mehlhorn H, Schmahl G, Schmidt J (2005) Extract of the seeds of the plant Vitex agnus castus proven to be highly efficacious as a repellent against ticks, fleas, mosquitoes and biting flies. Parasitol Res 95:363–365
Mehlhorn H, Al-Rasheid KAS, Al-Quraishy S, Abdel-Ghaffar F (2012) Research and increase of expertise in arachno-entomology are urgently needed. Parasitol Res 110:259–265
Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramfrez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotech 16:2346–2353
Murugan K, Hwang JS, Kovendan K, Prasanna Kumar K, Vasugi C, Naresh Kumar A (2011) Use of plant products and copepods for control of the dengue vector, Aedes aegypti. Hydrobiologia 666:331–338
Murugan K, Benelli G, Ayyappan S, Dinesh D, Panneerselvam C, Nicoletti M, Hwang JS, Mahesh Kumar P, Subramaniam J, Suresh U (2015a) Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus. Parasit Res 114:2243–2253
Murugan K, Benelli G, Panneerselvam C, Subramaniam J, Jeyalalitha T, Dinesh D, Nicoletti M, Hwang JS, Suresh U, Madhiyazhagan P (2015b) Cymbopogon citratus-synthesized gold nanoparticles boost the predation efficiency of copepod Mesocyclops aspericornis against malaria and dengue mosquitoes. Exp Parasitol 153:129–138
Murugan K, Priyanka V, Dinesh D, Madhiyazhagan P, Panneerselvam C, Subramaniam J, Suresh U, Chandramohan B, Roni M, Nicoletti M, Alarfaj AA, Higuchi A, Munusamy MA, Khater HF, Messing RH, Benelli G (2015c) Enhanced predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector Aedes aegypti in an aquatic environment treated with mosquitocidal nanoparticles: towards “boosted” biological control? Parasitol Res. doi:10.1007/s00436-015-4582-0
Murugan K, Eugine Venus JS, Panneerselvam C, Bedini S, Conti B, Nicoletti M, Kumar Sarkar S, Hwang JS, Subramaniam J, Madhiyazhagan P, Mahesh Kumar P, Dinesh D, Suresh U, Benelli G (2015d) Biosynthesis, mosquitocidal and antibacterial properties of Toddalia asiatica-synthesized silver nanoparticles: do they impact predation of guppy Poecilia reticulata against the filariasis mosquito Culex quinquefasciatus? Environ Sci Pollut Res. doi:10.1007/s11356-015-4920-x
Murugan K, Aarthi N, Kovendan K, Panneerselvam C, Chandramohan B, Mahesh Kumar P, Amerasan D, Paulpandi M, Chandirasekar R, Dinesh D, Suresh U, Subramaniam J, Higuchi A, Abdullah A, Alarfaj NM, Mehlhorn H, Benelli G (2015e) Mosquitocidal and antiplasmodial activity of Senna occidentalis (Cassiae) and Ocimum basilicum (Lamiaceae) from Maruthamalai hills against Anopheles stephensi and Plasmodium falciparum. Parasitol Res. doi:10.1007/s00436-015-4593-x
Murugan K, Samidoss CM, Panneerselvam C, Higuchi A, Roni M, Suresh U, Chandramohan B, Subramaniam J, Madhiyazhagan P, Dinesh D, Rajaganesh R, Alarfaj AA, Nicoletti M, Kumar S, Wei H, Canale A, Mehlhorn H, Benelli G (2015f) Seaweed-synthesized silver nanoparticles: an eco-friendly tool in the fight against Plasmodium falciparum and its vector Anopheles stephensi? Parasitol Res. doi:10.1007/s00436-015-4638-1
Murugan K, Aamina Labeeba M, Panneerselvam C, Dinesh D, Suresh U, Subramaniam J, Madhiyazhagan P, Hwang JS, Wang L, Nicoletti M, Benelli G (2015g) Aristolochia indica green-synthesized silver nanoparticles: a sustainable control tool against the malaria vector Anopheles stephensi? Res Vet Sci 102:127–135
Perez-Goodwyn PJ (2006) Taxonomic revision of the subfamily Lethocerinae Lauck & Menke (Heteroptera: Belostomatidae). Stuttgarter Beiträge zur Naturkunde A (Biologie) 695:1–71
Perry AS, Yamamoto I, Ishaaya I, Perry RY (1998) Insecticides in agriculture and environment. Springer, Berlin
Phanjom P, Ahmed G (2015) Biosynthesis of silver nanoparticles by Aspergillus oryzae (MTCC No. 1846) and its characterizations. Nanosci Nanotech 5(1):14–21
Pokhrel LR, Dubey B (2012) Potential impact of low-concentration silver nanoparticles on predator-prey interactions between predatory dragonfly nymphs and Daphnia magna as a prey. Environ Sci Tech 46:7755–7762
Prasad TNVKV, Elumalai EK (2011) Biofabrication of Ag nanoparticles using Moringa oleifera leaf extract and their antimicrobial activity. Asian Pac J Trop Biomed 1:439–442
Qu D, Zheng M, Zhang L, Zhao H, Xie Z, Jing X, Hadda RE, Fan H, Sun Z (2014) Formation mechanism and optimization of highly luminescent N-doped graphene quantum dots. Sci Rep 4(5294):1–9
Ravikumar S, Ramanathan G, Inbaneson SJ, Ramu A (2011a) Antiplasmodial activity of two marine polyherbal preparations from Chaetomorpha antennina and Aegiceras corniculatum against Plasmodium falciparum. Parasitol Res 108:107–113
Ravikumar S, Ali MS, Beula JM (2011b) Mosquito larvicidal efficacy of seaweed extracts against dengue vector of Aedes aegypti. Asia Pac J Trop Biomed 1:S143–S146
Roopan RSM, Madhumitha G, Rahuman AA, Kamaraj C, Bharathi A (2013) Low-cost and eco-friendly phyto-synthesis of silver nanoparticles using Cocos nucifera coir extract and its larvicidal activity. Ind Crop Prod 43:631–635
Salam HA, Rajiv P, Kamaraj M, Jagadeeswaran P, Gunalan S, Sivaraj R (2012) Plants: green route for nanoparticles synthesis. Int Res J Biol Sci 1:85–90
Saxena M, Sumit Kumar Sonkar S, Sarkar S (2013) Water soluble nanocarbons arrest the growth of mosquitoes. RSC Adv 3:22504
Service MW (1973) Mortalities of the larvae of the Anopheles gambiae Giles complex and detection of predators by the precipitin test. Bull Entomol Res 62:359–369
Service MW (1977) Mortalities of the immature stages of species B of the Anopheles gambiae complex in Kenya: comparison between rice fields and temporary pools, identification of predators. J Med Entomol 13(4-5):535–545
Shankar SS, Rai A, Ahmad A, Sastry M (2004) Rapid synthesis of Au, Ag, and bimetallic Au core Ag shell nanoparticles using neem (Azadirachta indica) leaf broth. J Colloid Interface Sci 275:496–502
Shugart LR (1999) Structural damage to DNA in response to toxicant exposure. In: Forbes VE (ed) Genetics and ecotoxicology. Taylor & Francis, London, pp 151–167
Siddhuraju P, Becker K (2003) Antioxidant properties of various solvent extracts of total phenolic constituents from three different agro-climatic origins of drumstick tree (Moringa oleifera Lam.). J Agric Food Chem 15:2144–2155
Singh NP (2000) Microgel for estimation of DNA strand breaks, DNA protein crosslinks and apoptosis. Mutat Res 455:111–127
Song JY, Kim BS (2009) Rapid biological synthesis of silver nanoparticles using plant leaf extract. Bioprocess Biosyst Eng 32:79–84
Srinivas NL, Paul MK, Sree vennela P, Venkata RD (2013) Green synthesis of silver nanoparticles using strawberry leaf extract (Arbutus unedo) and evaluation of its antimicrobial activity—a novel study. Int J Nanomat Biostructures pp. 47-50
Stuart BH (2002) Polymer analysis. Wiley, United Kingdom
Sudha Lakshmi Y (2011) Green synthesis of silver nanoparticles from Cleome viscosa: synthesis and antimicrobial activity. International conference on bioscience, biochemistry and bioinformatics IPCBEE, 5th edn. IACSIT, Singapore, pp 334–337
Suganya G, Karthi S, Shivakumar MS (2014) Larvicidal potential of silver nanoparticles synthesized from Leucas aspera leaf extracts against dengue vector Aedes aegypti. Parasitol Res 113(5):1673–1679
Sujitha V, Murugan K, Paulpandi M, Panneerselvam C, Suresh U, Roni M, Nicoletti M, Higuchi A, Madhiyazhagan P, Subramaniam J, Dinesh D, Vadivalagan C, Chandramohan B, Alarfaj AA, Munusamy MA, Barnard DR, Benelli G (2015) Green-synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti. Parasitol Res. doi:10.1007/s00436-015-4556-2
Theodorakis CW, D’Surney SJ, Shugart LR (1994) Detection of genotoxic insult as DNA strand breaks in fish blood cells by agarose gel electrophoresis. Environ Toxicol Chem 13:1023–1031
Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206–221
Udayasoorian C, Kumar RV, Jayabalakrishnan M (2011) Extracellular synthesis of silver nanoparticles using leaf extract of Cassia auriculata. Dig J Nanomater Biostruct 6(1):279–283
Veerakumar K, Govindrajan M, Rajeswary M, Muthukumaran U (2014) Low-cost and eco-friendly green synthesis of silver nanoparticles using Feronia elephantum (Rutaceae) against Culex quinquefasciatus, Anopheles stephensi, and Aedes aegypti (Diptera: Culicidae). Parasitol Res 113:1775–1785
Vinoth B, Manivasagaperumal R, Balamurugan S (2012) Phytochemical analysis and antibacterial activity of Moringa oleifera Lam. Int J Res Biol Sci 2:98–102
Von Maydell HJ (1986) Trees and shrubs of the Sahel, their characteristics and uses. Deutsche Gesellschaft fur Technische Zusammenarbeit, Federal Republic of Germany, pp 334–337
WHO (2014) Lymphatic filariasis. Fact sheet no. 102
Xu H, Kall M (2002) Surface-plasmon-enhanced optical forces in silver nanoaggregates. Phys Rev Lett 89:246802
Zheleva-Dimitrova D, Nedialkov P, Kitanov G (2010) Radical scavenging and antioxidant activities of methanolic extracts from Hypericum species growing in Bulgaria. Pharmacogn Mag 6:74–78
Acknowledgments
The authors would like to thank the financial support rendered by King Saud University, through the Vice Deanship of Research Chairs.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Conflict of interest
The authors declare that they have no competing interests. G. Benelli is an Editorial Board Member of Parasitology Research. This does not alter the authors’ adherence to all the Parasitology Research policies on sharing data and materials.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 122 kb)
Rights and permissions
About this article
Cite this article
Murugan, K., Nataraj, D., Madhiyazhagan, P. et al. Carbon and silver nanoparticles in the fight against the filariasis vector Culex quinquefasciatus: genotoxicity and impact on behavioral traits of non-target aquatic organisms. Parasitol Res 115, 1071–1083 (2016). https://doi.org/10.1007/s00436-015-4837-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-015-4837-9


