, Volume 797, Issue 1, pp 335–350 | Cite as

Chitosan-fabricated Ag nanoparticles and larvivorous fishes: a novel route to control the coastal malaria vector Anopheles sundaicus?

  • Kadarkarai Murugan
  • Jaganathan Anitha
  • Udaiyan Suresh
  • Rajapandian Rajaganesh
  • Chellasamy Panneerselvam
  • Al Thabiani Aziz
  • Li-Chun Tseng
  • Kandasamy Kalimuthu
  • Mohamad Saleh Alsalhi
  • Sandhanasamy Devanesan
  • Marcello Nicoletti
  • Santosh Kumar Sarkar
  • Giovanni BenelliEmail author
  • Jiang-Shiou HwangEmail author
Primary Research Paper


Mosquitoes represent a key threat for millions of humans worldwide, since they act as vectors for malaria, dengue fever, yellow fever, Zika virus, filariasis, and encephalitis. In this study, we tested chitosan-synthesized silver nanoparticles (Ch–AgNP) using male crab shells as a source of chitosan, which acted as a reducing and capping agent. Ch–AgNP were characterized by UV–Vis spectroscopy, FTIR, SEM, EDX, and XRD. Chitosan and Ch–AgNP were tested against larvae and pupae of the malaria vector Anopheles sundaicus under laboratory and field conditions. Antibacterial properties of Ch–AgNP were tested on Bacillus subtilis, Escherichia coli, Klebsiella pneumoniae, and Proteus vulgaris using the agar disk diffusion assay. The standard predation efficiency of the mosquito natural enemy Carassius auratus in laboratory conditions was 60.80 (on larva II) and 19.68 individuals (on larva III) per day, while post-treatment with sub-lethal doses of Ch–AgNP, the predation efficiency was boosted to 72.00 (on larva II) and 25.80 individuals (on larva III). Overall, Ch–AgNP fabricated using chitosan extracted from the male crab shells of the hydrothermal vent species Xenograpsus testudinatus may offer a novel and safer control strategy against A. sundaicus mosquito vectors, as well as against Gram-negative and Gram-positive pathogenic bacteria.


Anopheline Biocontrol agent Indoor residual spraying Mosquito borne diseases Nanosynthesis 



We acknowledge the editor Veronica Ferreira and the two anonymous reviewers whose comments contributed to improve the manuscript. A. Jaganathan is grateful to the University Grant Commission (New Delhi, India), Project No. PDFSS-2014-15-SC-TAM-10125. The authors would like to thank the financial support rendered by King Saud University, through the Vice Deanship of Research Chairs. We are grateful for financial support from the Ministry of Science and Technology (MOST) of Taiwan through the Grant No. MOST 104-2611-M-019-004, MOST 105-2621-M-019-001 and MOST 105-2918-I-019-001 to J.-S. Hwang as well as the Grant No. MOST 104-2811-M-019-005 and MOST 105-2811-M-019-008 to L.-C. Tseng.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest.


  1. Ali, S. W., S. Rajendran & M. Joshi, 2011. Synthesis and characterization of chitosan and silver loaded chitosan nanoparticles for bioactive polyester. Carbohydrate Polymers 83: 438–446.CrossRefGoogle Scholar
  2. Amerasan, D., T. Nataraj, K. Murugan, P. Madhiyazhagan, C. Panneerselvam, P. Madhiyazhagan, M. Nicoletti & G. Benelli, 2016. Myco-synthesis of silver nanoparticles using Metarhizium anisopliae against the rural malaria vector Anopheles culicifacies Giles (Diptera: Culicidae). Journal of Pest Science 89: 249–256.CrossRefGoogle Scholar
  3. Arokiyaraj, S., V. D. Kumar, V. Elakya, T. Kamala, S. K. Park, M. Ragam, et al., 2015. Biosynthesized silver nanoparticles using floral extract of Chrysanthemum indicum L.—potential for malaria vector control. Environmental Science and Pollution Research 22: 9759–9765.CrossRefPubMedGoogle Scholar
  4. Azizi, S., M. B. Ahmad, F. Namvar & R. Mohamad, 2014. Green biosynthesis and characterization of zinc oxide nanoparticles using brown marine macroalga Sargassum muticum aqueous extract. Materials Letters 116: 275–277.CrossRefGoogle Scholar
  5. Badawy, M. E. I., 2010. Structure and antimicrobial activity relationship of quaternary N-alkyl chitosan derivatives against some plant pathogens. Journal of Applied Polymer Science 117: 960–969.CrossRefGoogle Scholar
  6. Badawy, M. E. I. & A. F. EI-Aswad, 2012. Insecticidal activity of chitosons of different molecular weights and chitoson–metal complexes against cotton leaf sworm Spodoptera littoralis and oleander aphid Aphis neri. Plant Protection Science 48: 131–141.Google Scholar
  7. Banerjee, P., M. Satapathy, A. Mukhopahayay & P. Das, 2014. Leaf extract mediated green synthesis of silver nanoparticles from widely available Indian plants: synthesis, characterization, antimicrobial property and toxicity analysis. Bioresources and Bioprocessing 1: 1–10.CrossRefGoogle Scholar
  8. Bartnicki-Garcia, S. & E. Lippman, 1982. Fungal wall composition. In Laskin, A. J. & H. A. Lechevalier (eds), CRC Hand Book of Microbiology, 2nd ed. CRC Press, Boca Raton: 229–252.Google Scholar
  9. Bauer, A. W., W. M. Kirby, J. C. Cherris & M. Truck, 1966. Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology 45: 493–496.PubMedGoogle Scholar
  10. Benelli, G., 2015a. Research in mosquito control: current challenges for a brighter future. Parasitology Research 114: 2801–2805.CrossRefPubMedGoogle Scholar
  11. Benelli, G., 2015b. Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitology Research 114: 3201–3212.CrossRefPubMedGoogle Scholar
  12. Benelli, G., 2016a. Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitology Research 115: 23–34.CrossRefPubMedGoogle Scholar
  13. Benelli, G., 2016b. Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer – a brief review. Enzyme and Microbial Technology 95: 58–68.CrossRefPubMedGoogle Scholar
  14. Benelli, G., 2017. Commentary: data analysis in bionanoscience—issues to watch for. Journal of Cluster Science 28: 11–14.CrossRefGoogle Scholar
  15. Benelli, G. & H. Mehlhorn, 2016. Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitology Research 115: 1747–1754.CrossRefPubMedGoogle Scholar
  16. Benelli, G., A. Lo Iacono, A. Canale & H. Mehlhorn, 2016. Mosquito vectors and the spread of cancer: an overlooked connection? Parasitology Research 115: 2131–2137.CrossRefPubMedGoogle Scholar
  17. Bowatte, G., P. Perera, G. Senevirathne, S. Meegaskumbura & M. Meegaskumbura, 2013. Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biological Control 67: 469–474.CrossRefGoogle Scholar
  18. Castro, S. P. M. & E. G. L. Paulin, 2012. Is chitosan a new panacea? Areas of application. In Karunaratne, D. N. (ed.), The Complex World of Polysaccharides. InTech, Rijeka.Google Scholar
  19. Chandramohan, B., K. Murugan, C. Panneerselvam, P. Madhiyazhagan, R. Chandirasekar, D. Dinesh, P. M. Kumar, K. Kovendan, U. Suresh, J. Subramaniam, R. Rajaganesh, A. T. Aziz, B. Syuhei, M. S. Alsalhi, S. Devanesan, M. Nicoletti, H. Wei & G. Benelli, 2016. Characterization and mosquitocidal potential of neem cake-synthesized silver nanoparticles: genotoxicity and impact on predation efficiency of mosquito natural enemies. Parasitology Research 115: 1015–1025.CrossRefPubMedGoogle Scholar
  20. Chen, P., L. Song, Y. Liu & Y. Fang, 2007. Synthesis of silver nonoparticles by r-ray irradiation in acetic water solution containing chitosan. Radiation Physics Chemistry 76: 1165–1168.CrossRefGoogle Scholar
  21. Chen, Q., H. Jiang, H. Ye, J. Li & J. Huang, 2014. Preparation, antibacterial, and antioxidant activities of silver/chitosan composites. Journal of Carbohydrate Chemistry 33: 298–312.CrossRefGoogle Scholar
  22. Chobu, M., G. Nkwengulila, A. M. Mahande, B. J. Mwang’onde & E. J. Kweka, 2015. Direct and indirect effect of predators on Anopheles gambiae sensu stricto. Acta Tropica 142: 131–137.CrossRefPubMedGoogle Scholar
  23. Cox, F. E. G., 2010. History of the discovery of the malaria parasites and their vectors. Parasites & Vectors 3: 1–9.CrossRefGoogle Scholar
  24. Dananjaya, S. H. S., G. I. Godahewa, R. G. P. T. Jayasooriya, O. H. Chulhong, L. Jehee & D. Z. Mahanama, 2014. Chitosan silver nano composites (CAgNCs) as potential antibacterial agent to control Vibrio tapetis. Journal of Veterinary Science Technology 5: 209. doi: 10.4172/2157-7579.1000209.Google Scholar
  25. Dinesh, D., K. Murugan, P. Madhiyazhagan, C. Panneerselvam, M. Nicoletti, W. Jiang, G. Benelli, B. Chandramohan & U. Suresh, 2015. Mosquitocidal and antibacterial activity of green-synthesized silver nanoparticles from Aloe vera extracts: towards an effective tool against the malaria vector Anopheles stephensi? Parasitology Research 114: 1519–1529.CrossRefPubMedGoogle Scholar
  26. El-Mohamedy, R. S., F. Abdel-Kareem, H. Jaboun-Khiareddine & M. Daami-Remadi, 2014. Chitosan and Trichoderma harzianum as fungicide alternatives for controlling Fusarium crown and root rot of tomato. Tunisian Journal of Plant Protection 9: 31–43.Google Scholar
  27. Fayaz, M., K. Balaji, M. Girilal, R. Yadav, P. T. Kalaichelvan & R. Venketesan, 2010. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against Gram-positive and Gram-negative bacteria. Nanomedicine: Nanotechnology, Biology and Medicine 6: 103–109.CrossRefGoogle Scholar
  28. Feng, Q. L., J. Wu, G. Q. Chen, F. Z. Cui & T. N. Kim, 2000. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. Journal of Biomedical Materials Research Part A 52: 662–668.CrossRefGoogle Scholar
  29. Finney, D. J., 1971. Probit analysis. Cambridge University Press, London: 68–72.Google Scholar
  30. Gaffigan, T. V., R. C. Wilkerson, J. E. Pecor, J. A. Stoffer & T. Anderson, 2015. Systematic catalog of Culicidae.
  31. Gohel, V., A. Singh, M. Vimal, P. Ashwini & H. S. Chhatpar, 2006. Bioprospecting and antifungal potential of chitinolytic microorganisms. African Journal of Biotechnology 5: 54–72.Google Scholar
  32. Gooday, G. W., 1990. The ecology of chitin degradation. Advances in Microbial Ecology 11: 387–419.CrossRefGoogle Scholar
  33. Govindan, S., E. A. K. Nivethaa, R. Saravanan, V. Narayanan & A. Stephen, 2012. Synthesis and characterization of chitosan-silver nanocomposite. Applied Nanoscience 2: 299–303.CrossRefGoogle Scholar
  34. Govindarajan, M. & G. Benelli, 2016a. α-Humulene and β-elemene from Syzygium zeylanicum (Myrtaceae) essential oil: highly effective and eco-friendly larvicides against Anopheles subpictus, Aedes albopictus and Culex tritaeniorhynchus (Diptera: Culicidae). Parasitology Research 115: 2771–2778.CrossRefPubMedGoogle Scholar
  35. Govindarajan, M. & G. Benelli, 2016b. Eco-friendly larvicides from Indian plants: effectiveness of lavandulyl acetate and bicyclogermacrene on malaria, dengue and Japanese encephalitis mosquito vectors. Ecotoxicology and Environmental Safety 133: 395–402.CrossRefPubMedGoogle Scholar
  36. Govindarajan, M. & G. Benelli, 2016c. Artemisia absinthium-borne com- pounds as novel larvicides: effectiveness against six mosquito vectors and acute toxicity on non-target aquatic organisms. Parasitology Research 115: 4649–4661.CrossRefPubMedGoogle Scholar
  37. Govindarajan, M., H. F. Khater, C. Panneerselvam & G. Benelli, 2016a. One- pot fabrication of silver nanocrystals using Nicandra physalodes: a novel route for mosquito vector control with moderate toxicity on non-target water bugs. Research in Veterinary Science 107: 95–101.CrossRefPubMedGoogle Scholar
  38. Govindarajan, M., M. Nicoletti & G. Benelli, 2016b. Bio-physical characterization of poly-dispersed silver nanocrystals fabricated using Carissa spinarum: a potent tool against mosquito vectors. Journal of Cluster Science 27: 745–761.CrossRefGoogle Scholar
  39. Gow, N. A. R. & G. W. Gooday, 1983. Ultrastructure of chitin in hyphae of Candida albicans and other dimorphic and mycelial fungi. Protoplasma 115: 52–58.CrossRefGoogle Scholar
  40. Huang, M., E. Khor & L. Y. Lim, 2004. Uptake and cytotoxicity of chitosan molecules and nanoparticles: effects of molecular weight and degree of deacetylation. Pharmaceutical Research 21: 344–353.CrossRefPubMedGoogle Scholar
  41. Jaganathan, A., K. Murugan, C. Panneerselvam, P. Madhiyazhagan, D. Dinesh, C. Vadivalagan, A. T. Aziz, B. Chandramohan, U. Suresh, R. Rajaganesh, J. Subramaniam, M. Nicoletti, A. Higuchi, A. A. Alarfaj, M. A. Munusamy, S. Kumar & G. Benelli, 2016. Earthworm-mediated synthesis of silver nanoparticles: a potent tool against hepatocellular carcinoma, pathogenic bacteria, Plasmodium parasites and malaria mosquitoes. Parasitology International 65: 276–284.CrossRefPubMedGoogle Scholar
  42. Julkapli, N.M., Z. Ahmad & H. M. Akil, 2009. X-ray diffraction studies of cross linked chitosan with different cross linking agents for waste water treatment application. In Saat, A., H. A. Kassim, M. H. H. Jumali, J. M. Saleh, M. R. Othman, A. Ibrahim, F. M. Idris & M. H. A.-R. M. Ahmad (eds) Neutron and X-Ray Scattering. Advancing Materials Research, Kuala Lumpur, Malaysia: 106–111.Google Scholar
  43. Kalimuthu, K., S. M. Lin, L. C. Tseng, K. Murugan & J. S. Hwang, 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.CrossRefGoogle Scholar
  44. Kaur, P., R. Thakur & A. Choudhary, 2012. An in-vitro study of antifungal activity of silver/chitosan nanoformulations against important seed borne pathogens. International Journal of Science & Technology Research 1: 83–86.Google Scholar
  45. Kaviya, S., J. Santhanalakshmi, B. Viswanathan, J. Muthumary & K. Srinivasan, 2011. Biosynthesis of silver nanoparticles using Citrus sinensis peel extract and its antibacterial activity. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 79: 594–598.CrossRefGoogle Scholar
  46. Krishna Rao, K. S. V., P. Ramasubba Reddya, Y.-I. Lee & C. Kim, 2012. Synthesis and characterization of chitosan–PEG–Ag nanocomposites for antimicrobial application. Carbohydrate Polymers 87: 920–925.CrossRefGoogle Scholar
  47. Lamarque, G., J. M. Lucas, C. Viton & A. Domard, 2005. Physicochemical behavior of homogeneous series of acetylated chitosans in aqueous solution: role of various structural parameters. Biomacromolecules 6: 131–142.CrossRefPubMedGoogle Scholar
  48. Lee, D. S., C. R. Gilbert, C. H. Hocutt, R. E. Jenkins & D. E. McAllister, 1980. Atlas of North American Freshwater Fishes. North Carolina State Museum of Natural History, Raleigh, NC.Google Scholar
  49. Lertsutthiwong, P., N. C. How, S. Chandrkrachang & W. F. Stevens, 2002. Effect of chemical treatment on the characteristics of shrimp chitosan. Journal of Metals, Materials and Minerals 12: 11–18.Google Scholar
  50. Madhiyazhagan, P., K. Murugan, A. N. Kumar, T. Nataraj, D. Dinesh, C. Panneerselvam, J. Subramaniam, P. Mahesh Kumar, U. Suresh, M. Roni, M. Nicoletti, A. A. Alarfaj, A. Higuchi, M. A. Munusamy & G. Benelli, 2015. Sargassum muticum-synthesized silver nanoparticles: an effective control tool against mosquito vectors and bacterial pathogens. Parasitology Research 114: 4305–4317.CrossRefPubMedGoogle Scholar
  51. Magudapathy, P., P. Gangopadhyay, B. Panigrahi, K. Nair & S. Dhara, 2001. Electrical transport studies of Ag nanoclusters embedded in glass matrix. Physica B: Condensed Matter 299(1–2): 142–146.CrossRefGoogle Scholar
  52. Mehlhorn, H., 2008. Encyclopedia of Parasitology, 3rd ed. Springer, Heidelberg.CrossRefGoogle Scholar
  53. Mohamed, E., I. Badawy & A. F. EL-Aswad, 2012. Insecticidal activity of chitosans of different molecular weights and chitosan–metal complexes against cotton leafworm Spodoptera littoralis and oleander aphid Aphis nerii. Plant Protection Science 48: 131–141.Google Scholar
  54. Muhammed Rafeeq, P. E., V. Junise, R. Saraswathi, P. N. Krishnan & C. Dilip, 2010. Development and characterization of chitosan nanoparticles loaded with isoniazid for the treatment of tuberculosis. Research Journal of Pharmaceutical, Biological and Chemical Science 1: 383–390.Google Scholar
  55. Murugadoss, A. & A. Chattopadhyay, 2008. A ‘green’ chitosansilver nanoparticle composite as a heterogeneous as well as micro-heterogeneous catalyst. Nanotechnology 19: 015603.CrossRefPubMedGoogle Scholar
  56. Murugan, K., R. Vahitha, I. Baruah & S. C. Das, 2003. Integration of botanical and microbial pesticides for the control of the filarial vector, Culex quinquefasciatus. Annals of Medical Entomology 12: 12–23.Google Scholar
  57. Murugan, K., M. Aamina Labeeba, C. Panneerselvam, D. Dinesh, U. Suresh, J. Subramaniam, P. Madhiyazhagan, J.-S. Hwang, L. Wang, M. Nicoletti & G. Benelli, 2015a. Aristolochia indica green-synthesized silver nanoparticles: a sustainable control tool against the malaria vector Anopheles stephensi? Research Veterinary Science 102: 127–135.CrossRefGoogle Scholar
  58. Murugan, K., N. Aarthi, K. Kovendan, C. Panneerselvam, B. Chandramohan, P. M. Kumar, D. Amerasan, M. Paulpandi, R. Chandirasekar, D. Dinesh, U. Suresh, J. Subramaniam, A. Higuchi, A. A. Alarfaj, M. Nicoletti, H. Mehlhorn & G. Benelli, 2015b. Mosquitocidal and antiplasmodial activity of Senna occidentalis (Cassiae) and Ocimum basilicum (Lamiaceae) from Maruthamalai hills against Anopheles stephensi and Plasmodium falciparum. Parasitology Research 114: 3657–3664.CrossRefPubMedGoogle Scholar
  59. Murugan, K., G. Benelli, S. Ayyappan, D. Dinesh, C. Panneerselvam, M. Nicoletti, J.-S. Hwang, P. M. Kumar, J. Subramaniam & U. Suresh, 2015c. Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus. Parasitology Research 14: 2243–2253.CrossRefGoogle Scholar
  60. Murugan, K., J. S. E. Venus, C. Panneerselvam, S. Bedini, B. Conti, M. Nicoletti, S. K. Sarkar, J.-S. Hwang, J. Subramaniam, P. Madhiyazhagan, P. M. Kumar, D. Dinesh, U. Suresh & G. Benelli, 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? Environmental Science and Pollution Research 22: 17053–17064.CrossRefPubMedGoogle Scholar
  61. Murugan, K., A. Jaganathan, D. Dinesh, U. Suresh, R. Rajaganesh, B. Chandramohan, J. Subramaniam, M. Paulpandi, C. Vadivalagan, L. Wang, J. S. Hwang, H. Wei, M. Saleh Alsalhi, S. Devanesan, S. Kumar, K. Pugazhendy, A. Higuchi, M. Nicoletti & G. Benelli, 2016. Synthesis of nanoparticles using chitosan from crab shells: implications for control of malaria mosquito vectors and impact on non-target organisms in the aquatic environment. Ecotoxicology and Environmental Safety 132: 318–328.CrossRefPubMedGoogle Scholar
  62. Muthukumaran, U., M. Govindarajan & M. Rajeswary, 2015. Mosquito larvicidal potential of silver nanoparticles synthesized using Chomelia asiatica (Rubiaceae) against Anopheles stephensi, Aedes aegypti, and Culex quinquefasciatus (Diptera: Culicidae). Parasitology Research 114: 989–999.CrossRefPubMedGoogle Scholar
  63. Muzzarelli, R. A. A. & R. Rochetti, 1985. Determination of the degree of deacetylation of chitosan by first derivative ultraviolet spectrophotometry. Journal of Carbohydrate Polymers 5: 461–472.CrossRefGoogle Scholar
  64. Page, L. M. & B. M. Burr, 1991. A Field Guide to Freshwater Fishes of North America North of Mexico. The Peterson Field Guide Series, vol. 42. Houghton Mifflin Company, Boston.Google Scholar
  65. Panneerselvam, C., K. Murugan, K. Kovendan, P. Mahesh Kumar & J. Subramaniam, 2013. Mosquito larvicidal and pupicidal activity of Euphorbia hirta Linn. (Family: Euphorbiaceae) and Bacillus sphaericus against Anopheles stephensi Liston (Diptera: Culicidae). Asian Pacific Journal of Tropical Medicine 6: 102–109.CrossRefPubMedGoogle Scholar
  66. Patil, S. V., H. P. Borase, C. D. Patil & B. K. Salunke, 2012a. Biosynthesis of silver nanoparticles using latex from few Euphorbian plants and their antimicrobial potential. Applied Biochemistry Biotechnology 167: 776–790.CrossRefPubMedGoogle Scholar
  67. Patil, C. D., H. P. Borase, S. V. Patil, R. B. Salunkhe & B. K. Salunke, 2012b. Larvicidal activity of silver nanoparticles synthesized using Pergularia daemia plant latex against Aedes aegypti and Anopheles stephensi and nontarget fish Poecillia reticulate. Parasitology Research 111: 555–562.CrossRefPubMedGoogle Scholar
  68. Patil, C. D., S. V. Patil, H. P. Borase, B. K. Salunke & R. B. Salunkhe, 2012c. Larvicidal activity of silver nanoparticles synthesized using Plumeria rubra plant latex against Aedes aegypti and Anopheles stephensi. Parasitology Research 110: 1815–1822.CrossRefPubMedGoogle Scholar
  69. Prasanna Kumar, K., K. Murugan, K. Kovendan, J.-S. Hwang & D. R. Barnard, 2012. Combined effect of seaweed Sargassum wightii greville and Bacillus thuringiensis var. israelensis against coastal mosquito vector, Anopheles sundaicus (L.) Tamil Nadu. India. Science Asia 38: 141–146.CrossRefGoogle Scholar
  70. Rabea, E. I., M. E. I. Badawy, T. M. Rogge, C. V. Stevens & G. Smagghe, 2005. Insecticidal and fungicidal activity of new synthesized chitosan derivatives. Pest Management Science 61: 951–960.CrossRefPubMedGoogle Scholar
  71. Rai, M., A. Yadav & A. Gade, 2009. Silver nanoparticles as a new generation of antimicrobials. Biotechnology Advances 27: 76–83.CrossRefPubMedGoogle Scholar
  72. Rao, J. V. & P. Kavitha, 2010. In vitro effects of chlorpyrifos on the acetylcholinesterase activity of euryhaline fish, Oreochromis mossambicus. Zeitschrift für Naturforschung C 65: 303–306.Google Scholar
  73. Roy, K., C. K. Sarkar & C. K. Ghosh, 2015. Plant-mediated synthesis of silver nanoparticles using parsley (Petroselinum crispum) leaf extract: spectral analysis of the particles and antibacterial study. Applied Nanoscience 5: 945–951.CrossRefGoogle Scholar
  74. Ruparelia, J. P., A. K. Chatterjee, S. P. Duttagupta & S. Mukherji, 2008. Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomaterialia 4: 707–716.CrossRefPubMedGoogle Scholar
  75. Sabbour, M. M., 2013. Entomotoxicity assay of nanoparticle 4-(silica gel Cab-O-Sil-750, silica gel Cab-O-Sil-500) against Sitophilus oryzae under laboratory and store conditions in Egypt. Science Research Report 1: 67–74.Google Scholar
  76. Sahab, A. F., A. I. Waly, M. M. Sabbour & L. S. Nawar, 2015. Synthesis, antifungal and insecticidal potential of Chitosan (CS)-g-poly (acrylic acid) (PAA) nanoparticles against some seed borne fungi and insects of soybean. International Journal of Chem Tech Research 8: 589–598.Google Scholar
  77. Sanpui, P., A. Murugadoss, P. V. Prasad, S. S. Ghosh & A. Chattopadhyay, 2008. The antibacterial properties of a novel chitosan–Ag–nanoparticle composite. International Journal of Food Microbiology 124: 142–146.CrossRefPubMedGoogle Scholar
  78. Saraswathy, G., S. Pal, C. Rose & T. P. Sastry, 2001. A novel bio-inorganic bone implant containing deglued bone, chitosan and gelatin. Bulletin of Materials Science 24: 415–420.CrossRefGoogle Scholar
  79. Sorlier, P., A. Denuziere, C. Viton & A. Domard, 2001. Relation between the degree of acetylation and the electrostatic properties of chitin and chitosan. Biomacromolecules 2: 765–772.CrossRefPubMedGoogle Scholar
  80. Souza, B. W. S., M. A. Cerqueira, J. T. Martins, A. Casariego, J. A. Teixeira & A. A. Vicente, 2010. Influence of electric fields on the structure of chitosan edible coatings. Food Hydrocolloids 24: 330–335.CrossRefGoogle Scholar
  81. Stuart, B. H., 2002. Polymer Analysis. Wiley, Chichester.Google Scholar
  82. Subramaniam, J., K. Murugan, C. Panneerselvam, K. Kovendan, P. Madhiyazhagan, P. M. Kumar, D. Dinesh, B. Chandramohan, U. Suresh, M. Nicoletti, A. Higuchi, J. S. Hwang, S. Kumar, A. A. Alarfaj, M. A. Munusamy, R. H. Messing & G. Benelli, 2015. Eco-friendly control of malaria and arbovirus vectors using the mosquitofish Gambusia affinis and ultra-low dosages of Mimusops elengi-synthesized silver nanoparticles: towards an integrative approach? Environmental Science and Pollution Research 22: 20067–20083.CrossRefPubMedGoogle Scholar
  83. Subramaniam, J., K. Murugan, C. Panneerselvam, K. Kovendan, P. Madhiyazhagan, D. Dinesh, P. Mahesh Kumar, B. Chandramohan, U. Suresh, R. Rajaganesh, M. Saleh Alsalhi, S. Devanesan, M. Nicoletti, A. Canale & G. Benelli, 2016. Multipurpose effectiveness of Couroupita guianensis-synthesized gold nanoparticles: high antiplasmodial potential, field efficacy against malaria vectors and synergy with Aplocheilus lineatus predators. Environmental Science and Pollution Research 23: 7543–7558.CrossRefPubMedGoogle Scholar
  84. Sukumar, K., M. J. Perich & L. R. Booba, 1991. Botanical derivatives in mosquito control: a review. Journal of the American Mosquito Control Association 7: 210–237.PubMedGoogle Scholar
  85. Suman, T. Y., S. R. Radhika Rajasree, A. Kanchana & S. B. Elizabeth, 2013. Biosynthesis, characterization and cytotoxic effect of plant mediated silver nanoparticles using Morinda citrifolia root extract. Colloids and Surfaces B: Biointerfaces 106: 74–78.CrossRefPubMedGoogle Scholar
  86. Suresh, U., K. Murugan, G. Benelli, M. Nicoletti, D. R. Barnard, C. Panneerselvam, P. M. Kumar, J. Subramaniam, D. Dinesh & B. Chandramohan, 2015. Tackling the growing threat of dengue: Phyllanthus niruri-mediated synthesis of silver nanoparticles and their mosquitocidal properties against the dengue vector Aedes aegypti (Diptera: Culicidae). Parasitology Research 114: 1551–1562.CrossRefPubMedGoogle Scholar
  87. Tan, X. L., S. Wang, X. Li & G. Zhang, 2010. Optimizing and application of micro-encapsulated artificial diet for Orius sauteri (Hemiptera: Anthocoridae). Acta Entomologica Sinica 53: 891–900.Google Scholar
  88. Templeton, A. C., W. P. Wuelfing & R. W. Murray, 2000. Monolayer-protected cluster molecules. Accounts of Chemical Research 33: 27–36.CrossRefPubMedGoogle Scholar
  89. Tiwari, D. K. & J. Behari, 2009. Biocidal nature of treatment of Ag-nanoparticle and ultrasonic irradiation in Escherichia coli dh5. Advances in Biological Research 3: 89–95.Google Scholar
  90. Trung, T. S., W. W. Thein-Han, N. T. Qui, C.-H. Ng & W. F. Stevens, 2006. Functional characteristics of shrimp chitosan and its membranes as affected by the degree of deacetylation. Bioresource Technology 97: 659–663.CrossRefPubMedGoogle Scholar
  91. Twu, Y. K., Y. W. Chen & C. M. Shih, 2008. Preparation of silver nanoparticles using chitosan suspensions. Powder Technology 185: 251–257.CrossRefGoogle Scholar
  92. Usha, C. & D. G. A. Rachel, 2014. Biogenic synthesis of silver nanoparticles by Acacia nilotica and their antibacterial activity. International Journal of Scientific Research 3: 27–29.CrossRefGoogle Scholar
  93. Walker, T., C. I. Jeffries, K. L. Mansfield & N. Johnson, 2014. Mosquito cell lines: history, isolation, availability and application to assess the threat of arboviral transmission in the United Kingdom. Parasites & Vectors 7: 1–9.CrossRefGoogle Scholar
  94. Ward, M. & G. Benelli, 2017. Avian and simian malaria: do they have a cancer connection? Parasitology Research. doi: 10.1007/s00436-016-5352-3.Google Scholar
  95. Wazed Ali, S., S. Rajendran & M. Joshi, 2001. Synthesis and characterization of chitosan and silver loaded chitosan nanoparticles for bioactive polyesters. Carbohydrate Polymers 83: 438–446.Google Scholar
  96. Wei, D., W. Sun, W. Qian, Y. Ye & X. Ma, 2009. The synthesis of chitosan-based silver nanoparticles and their antibacterial activity. Carbohydrate Research 344: 2375–2382.CrossRefPubMedGoogle Scholar
  97. WHO, 2014. Malaria. Fact sheet No. 94.Google Scholar
  98. Yang, K., N. S. Xu & W. W. Su, 2010. Co-immobilized enzymes in magnetic chitosan beads for improved hydrolysis of macromolecular substrates under a time-varying magnetic field. Journal of Biotechnology 148: 119–127.CrossRefPubMedGoogle Scholar
  99. Yoshizuka, K., Z. Lou & K. Inoue, 2000. Silver-complexed chitosan microparticles for pesticide removal. Reactive Functional Polymers 44: 47–54.CrossRefGoogle Scholar
  100. Zhang, M. I., T. Tan, H. Yuan & C. Rui, 2003. Insecticidal and fungicidal activities of chitosan and oligochitosan. Journal of Bioactive Compatible Polymers 18: 391–400.CrossRefGoogle Scholar
  101. Zhao, G. J. & S. E. Stevens, 1998. Multiple parameters for the comprehensive evaluation of the susceptibility of Escherichia coli to the silver ion. Biometals 11: 27–32.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Kadarkarai Murugan
    • 1
  • Jaganathan Anitha
    • 1
  • Udaiyan Suresh
    • 1
  • Rajapandian Rajaganesh
    • 1
  • Chellasamy Panneerselvam
    • 2
  • Al Thabiani Aziz
    • 2
  • Li-Chun Tseng
    • 3
  • Kandasamy Kalimuthu
    • 3
  • Mohamad Saleh Alsalhi
    • 4
  • Sandhanasamy Devanesan
    • 4
  • Marcello Nicoletti
    • 5
  • Santosh Kumar Sarkar
    • 6
  • Giovanni Benelli
    • 7
    Email author
  • Jiang-Shiou Hwang
    • 3
    Email author
  1. 1.Division of Entomology, Department of Zoology, School of Life SciencesBharathiar UniversityCoimbatoreIndia
  2. 2.Department of Biology, Faculty of ScienceUniversity of TabukTabukSaudi Arabia
  3. 3.Institute of Marine BiologyNational Taiwan Ocean UniversityKeelungTaiwan
  4. 4.Department of Physics and Astronomy, Laser Diagnosis of CancerKing Saud UniversityRiyadhKingdom of Saudi Arabia
  5. 5.Department of Environmental BiologySapienza University of RomeRomeItaly
  6. 6.Department of Marine ScienceUniversity of CalcuttaCalcuttaIndia
  7. 7.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly

Personalised recommendations