Abstract
Vector control is a critical requirement in epidemic disease management, and improved mosquito control methods that are economic and effective are necessary. Cyclopoid copepods are common predators in numerous aquatic ecosystems and have been used as biological agents in programs to control mosquito larvae. In this study, we proposed a green synthesis of silver nanoparticles (AgNPs) using the seaweed, Gracilaria firma, and combined them with the copepod, Megacyclops formosanus, for controlling the dengue vector, Aedes aegypti. The green synthesis of AgNPs was characterized by UV–Vis spectroscopy, Fourier transform infrared spectroscopy, transmission electron microscopy, and energy-dispersive X-ray spectroscopy. In mosquitocidal assays, the LC50 of G. firma extract against A. aegypti ranged from 0.091 (instar I) to 2.417 (pupae). LC50 of G. firma-synthesized AgNPs ranged from 25.895 (instar I) to 351.419 (pupae). Furthermore, we evaluated the predatory efficiency of copepod M. formosanus against the larvae of A. aegypti. The most characteristic effects were midgut columnar cell vacuolization, epithelium cell contents passing into the midgut lumen, and, finally, cell death. These results suggest that synthesized AgNPs in combination with copepods constitute ecofriendly and potential mosquito larvicidal agents.
Similar content being viewed by others
References
Abbott, W. S., 1925. A method of computing the effectiveness of insecticides. Journal of Economic Entomology 18: 267–269.
Ahmad, A., P. Mukherjee, D. Mandal, S. Senapati, M. I. Khan, R. Kumar & M. Sastry, 2003. Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids and Surfaces, Part B: Biointerface 28: 313–318.
Alder, H. L. & E. B. Rossler, 1977. Introduction to Probability and Statistics, 6th ed. WH Freeman Company, San Francisco: 246.
Al-Mehmadi, R. M. & A. A. Al-Khalaf, 2010. Larvicidal and histological effects of Melia azedarach extract on Culex quinquefasciatus Say larvae (Diptera: Culicidae). Journal of King Saud University-Science 22: 77–85.
Alves, S. N., J. E. Serrao & A. L. Melo, 2010. Alterations in the fat body and midgut of Culex quinquefasciatus larvae following exposure to different insecticides. Micron 41: 592–597.
Ankamwar, B., C. Damle, A. Absar & S. Mural, 2005. Biosynthesis of gold and silver nanoparticles using Emblica officinalis fruit extract, their phase transfer and transmetallation in an organic solution. Journal of Nanoscience and Nanotechnology 10: 1665–1671.
Arjunan, N. K., K. Murugan, C. Rejeeth, P. Madhiyazhagan & D. R. Barnard, 2012. Green synthesis of silver nanoparticles for the control of mosquito vectors of malaria, filariasis, and dengue. Vector-Borne and Zoonotic Diseases 12: 262–268.
Awasthi, A. K., C. H. Wu, K. H. Tsai, C. C. King & J. S. Hwang, 2012. How does the ambush predatory copepod Megacyclops formosanus (Harada, 1931) capture mosquito larvae of Aedes aegypti? Zoological Studies 51: 927–936.
Awasthi, A. K., J. C. Molinero, C. H. Wu, K. H. Tsai, C. C. King & J. S. Hwang, 2015. Behavioural changes in mosquito larvae induced by copepods predation. Hydrobiologia. doi:10.1007/s10750-014-2154-4.
Benelli, G., B. Conti, R. Garreffa & M. Nicoletti, 2014. Shedding light on bioactivity of botanical by-products: neem cake compounds deter oviposition of the arbovirus vector Aedes albopictus (Diptera: Culicidae) in the field. Parasitology Research 113: 933–940.
Benn, T. & P. Westerhoff, 2008. Nanoparticle silver released into water from commercially available sock fabrics. Environmental Science and Technology 42: 4133–4139.
Chandran, S. P., M. Chaudhary, R. Pasricha, A. Ahmad & M. Sastry, 2006. Synthesis of gold nanotriangles and silver nanoparticles using Aloe vera plant extract. Biotechnology Progress 22: 577–583.
Chitra, T., K. Murugan, A. N. Kumar, P. Madhiyazhagan, T. Nataraj, D. Indumathi, et al., 2013. Laboratory and field efficacy of Pedalium murex and predatory copepod Mesocyclops longisetus on rural malaria vector Anopheles culicifacies. Asian Pacific Journal of Tropical Disease 3: 111–118.
Dhanker, R., R. Kumar & J. S. Hwang, 2012. Predation by Pseudodiaptomus annandalei (Copepoda: Calanoida) on rotifer prey: size selection, egg predation and effect of algal diet. Journal of Experimental Marine Biology and Ecology 414–415: 44–53.
Finney, D. J., 1971. Probit Analysis. Cambridge University Press, London: 68–78.
Guzman, M. G., S. B. Halstead, H. Artsob, P. Buchy, J. Farrar, D. J. Gubler, E. Hunsperger, A. Kroeger, H. S. Margolis, E. Martinez, M. B. Nathan, J. L. Pelegrino, C. Simmons, S. Yoksan & R. W. Peeling, 2010. Dengue: a continuing global threat. Nature Reviews Microbiology 8: S7–S16.
Halstead, S. B., 2012. Dengue vaccine development: a 75% solution? Lancet 380: 1535–1536.
Hamouda, L. S., W. M. Elyassaki & M. S. Hamed, 1996. Toxicity and histopathological effect of Artemisia judaic and Anagallis arvensis extracts on Culex pipiens larvae. Journal of Egyptian German Society of Zoology 20: 43–60.
Huang, X., K. J. Prashant, H. E. I. S. Ivan & A. E. I. S. Mostafa, 2007. Focus: nanoparticles for cancer diagnosis and therapeutics – review. Nanomedicine 5: 681–693.
Hwang, J. S. & K. Martens (eds), 2011. Zooplankton behavior and ecology. Hydrobiologia 666: 179–338.
Hwang, J. S. & J. R. Strickler, 2001. Can copepods differentiate prey from predator hydromechanically? Zoological Studies 40: 1–6.
Hwang, J. S., R. Kumar & C. S. Kuo, 2009. Impact of predation by the copepod Mesocyclops pehpeiensis on life table demography and population dynamics of four cladocerans species: a comparative laboratory study. Zoological Studies 48: 738–752.
Jang, Y. S., M. K. Kim, Y. S. Ahn & H. S. Lee, 2002. Larvicidal activity of Brazilian plant against Aedes aegypti and Culex pipiens (Diptera: Culicidae). Agricultural Chemistry and Biotechnology 4: 131–134.
Jayaseelan, C., A. A. Rahuman, G. Rajakumar, A. Vishnu Kirthi, T. Santhoshkumar, S. Marimuthu, A. Bagavan, C. Kamaraj, A. A. Zahir & G. Elango, 2011. Synthesis of pediculocidal and larvicidal silver nanoparticles by leaf extract from heartleaf moonseed plant, Tinospora cordifolia Miers. Parasitology Research 109: 185–194.
Kalimuthu, K., C. Panneerselvam, K. Murugan & J. S. Hwang, 2013a. Green synthesis of silver nanoparticles using Cadaba indica lam leaf extract and its larvicidal and pupicidal activity against Anopheles stephensi and Culex quinquefasciatus. Journal of Entomology and Acarological Research 45: e11.
Kalimuthu, K., K. Murugan, L. C. Tseng & J. S. Hwang, 2013b. Mosquitocidal activity of Hedychium coronarium rhizome extract and copepod Megacyclops formosanus for the control of dengue vector Aedes aegypti. Journal of Marine Science and Technology 21: 258–266.
Kalimuthu, K., C. H. Wang, S. M. Liu, L. C. Tseng, K. Murugan & J. S. Hwang, 2013c. Mosquito larvicidal activity of Broussonetia papyrifera compound marmesin by blocking protein AESCP-2, docking strategies, and combined effect of copepod Megacyclops formosanus against dengue vector Aedes aegypti (Diptera: Culicidae). Journal of Marine Science and Technology 21: 308–315.
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.
Kumar, V., S. C. Yadav & S. K. Yadav, 2010. Syzygium cumini leaf and seed extract mediated biosynthesis of silver nanoparticles and their characterization. Journal of Chemical Technology and Biotechnology 85: 1301–1309.
Kumar, R., S. Souissi & J. S. Hwang, 2012a. Vulnerability of carp larvae to copepod predation as a function of larval age and body length. Aquaculture 338–341: 274–283.
Kumar, K. P., K. Murugan, K. Kovendan, A. N. Kumar, J. S. Hwang & D. R. Barnard, 2012b. Combined effect of seaweed (Sargassum wightii) and Bacillus thuringiensis var. israelensis on the coastal mosquito, Anopheles sundaicus, in Tamil Nadu, India. Science Asia 38: 141–146.
Lardeux, F., F. Riviere, Y. Séchan & S. Loncke, 2002. Control of the Aedes vector of the dengue viruses and Wuchereria bancrofti: the French Polynesian experience. Annals of Tropical Medicine and Parasitology 96: S105–S116.
Madhiyazhagan, P., K. Murugan, A. Naresh 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. doi:10.1007/s00436-015-4671-0.
Mahesh Kumar, P., K. Murugan, K. Kovendan, C. Panneerselvam, K. Prasanna Kumar, D. Amerasan, J. Subramaniam, K. Kalimuthu & T. Nataraj, 2012. Mosquitocidal activity of Solanum xanthocarpum fruit extract and copepod Mesocyclops thermocyclopoides for the control of dengue vector Aedes aegypti. Parasitology Research 111: 609–618.
Mahitha, B., B. Deva Prasad Raju, G. R. Dillip, C. Madhukar Reddy, K. Mallikarjuna, L. Manoj, S. Priyanka, K. Jayantha Rao & N. John Sushma, 2011. Biosynthesis, characterization and antimicrobial studies of AgNPs extract from Bacopa monnieri whole plant. Digest Journal of Nanomaterials and Biostructures 6: 135–142.
Mano Priya, M., B. Karunai Selvi & J. A. John Paul, 2011. Green synthesis of silver nanoparticles from the leaf extracts of Euphorbia hirta and Nerium indicum. Digest Journal of Nanomaterials and Biostructures 6: 869–877.
Marimuthu, S., A. A. Rahuman, G. Rajakumar, T. Santhoshkumar, A. V. Kirthi, C. Jayaseelan, A. Bagavan, A. A. Zahir, G. Elango & C. Kamaraj, 2010. Evaluation of green synthesized silver nanoparticles against parasites. Parasitology Research 108: 1541–1549.
Marten, G. G. & J. W. Reid, 2007. Cyclopoid copepods. Journal of the American Mosquito Control Association 23: 65–92.
Marten, G. G., E. S. Bordes & M. Nguyen, 1994. Use of cyclopoid copepods for mosquito control. Hydrobiologia 292(293): 491–496.
Murugan, K., J. S. Hwang, K. Kovendan, K. Prasanna Kumar, C. Vasugi & A. Naresh Kumar, 2011. Use of plant products and copepods for control of the dengue vector, Aedes aegypti. Hydrobiologia 666: 331–338.
Murugan, K., K. Kalimuthu, P. Mahesh Kumar, J. S. Hwang & M. Nicoletti, 2013. Larval and pupal toxicity effects of Plectranthus amboinicus, Bacillus sphaericus and predatory copepods for the control of the dengue vector, Aedes aegypti. Phytoparasitica 41: 307–316.
Murugan, K., C. M. Samidoss, C. Panneerselvam, A. Higuchi, M. Roni, U. Suresh, B. Chandramohan, J. Subramaniam, P. Madhiyazhagan, D. Dinesh, R. Rajaganesh, A. A. Alarfaj, M. Nicoletti, S. Kumar, H. Wei, A. Canale, H. Mehlhorn & G. Benelli, 2015. Seaweed-synthesized silver nanoparticles: an eco-friendly tool in the fight against Plasmodium falciparum and its vector Anopheles stephensi? Parasitology Research 114: 4087–4097.
Murugan, K., C. Panneerselvam, J. Subramaniam, P. Madhiyazhagan, J. S. Hwang, L. Wang, D. Dinesh, U. Suresh, M. Roni, A. Higuchi, M. Nicoletti & G. Benelli, 2016. Eco-friendly drugs from the marine environment: spongeweed-synthesized silver nanoparticles are highly effective on Plasmodium falciparum and its vector Anopheles stephensi, with little non-target effects on predatory copepods. Environmental Science and Pollution Research. doi:10.1007/s11356-016-6832-9.
Nam, V. S., N. T. Yen, B. H. Kay, G. G. Marten & J. W. Reid, 1998. Eradication of Aedes aegypti from a village in Vietnam, using copepods and community participation. American Journal of Tropical Medicine and Hygiene 59: 657–660.
Panneerselvam, C., K. Murugan, M. Roni, A. T. Aziz, U. Suresh, R. Rajaganesh, P. Madhiyazhagan, J. Subramaniam, D. Dinesh, M. Nicoletti, A. Higuchi, A. A. Alarfaj, M. A. Munusamy, S. Kumar, N. Desneux & G. Benelli, 2016. Fern-synthesized nanoparticles in the fight against malaria: LC/MS analysis of Pteridium aquilinum leaf extract and biosynthesis of silver nanoparticles with high mosquitocidal and antiplasmodial activity. Parasitology Research 115: 997–1013.
Priyadarshini, A. K., K. Murugan, C. Panneerselvam, S. Ponarulselvam, J. S. Hwang & M. Nicoletti, 2012. Biolarvicidal and pupicidal potential of silver nanoparticles synthesized using Euphorbia hirta against Anopheles stephensi Liston (Diptera: Culicidae). Parasitology Research 111: 997–1006.
Rajakumar, G. & A. Abdul Rahuman, 2011. Larvicidal activity of synthesized silver nanoparticles using Eclipta prostrata leaf extract against filariasis and malaria vectors. Acta Tropica 118: 196–203.
Rey, D., M. P. Pautou & J. C. Meyran, 1999. Histopathological effects of tannic acid on the midgut epithelium of some aquatic diptera larvae. Journal of Invertebrate Pathology 73: 173–181.
Roni, M., K. Murugan, C. Panneerselvam, J. Subramaniam, M. Nicoletti, P. Madhiyazhagan, D. Dinesh, U. Suresh, H. F. Khater, H. Wei, A. Canale, A. A. Alarfaj, M. A. Munusamy, A. Higuchi & G. Benelli, 2015. Characterization and biotoxicity of Hypnea musciformis-synthesized silver nanoparticles as potential eco-friendly control tool against Aedes aegypti and Plutella xylostella. Ecotoxicology and Environmental Safety 121: 31–38.
Sabchareon, A., D. Wallace, C. Sirivichayakul, K. Limkittikul, P. Chanthavanich, S. Suvannadabba, V. Jiwariyavej, W. Dulyachai, K. Pengsaa, T. A. Wartel, A. Moureau, M. Saville, A. Bouckenooghe, S. Viviani, N. G. Tornieporth & J. Lang, 2012. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 380: 1559–1567.
Sadeghi, B. & F. A. Gholamhoseinpoor, 2015. Study on the stability and green synthesis of silver nanoparticles using Ziziphora tenuior (Zt) extract at room temperature. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 134: 310–315.
Sahayaraj, K. & S. Kalidas, 2011. Evaluation of nymphicidal and ovicidal effect of seaweed, Padina pavonica (Linn.) (Phaeophyceae) on cotton pest, Dysdercus cingulatus (Fab.). Indian Journal of Geo-marine Sciences 40: 125–129.
Salunkhe, R. B., S. V. Patil, C. D. Patil & B. K. Salunke, 2011. Larvicidal potential of silver nanoparticles synthesized using fungus Cochliobolus lunatus against Aedes aegypti (Linnaeus, 1762) and Anopheles stephensi Liston (Diptera; Culicidae). Parasitology Research 109: 823–831.
Schaper, S. & F. Hernández, 1998. La Lucha contrael dengue Mesocyclops thermocyclopoides: un posible control biologico para larvas de Aedes aegypti. Revista de la Cost Ciencias Medicas 19: 119–125.
Shrivastava, S. & D. Dash, 2010. Label-free colorimetric estimation of proteins using nanoparticles of silver. Nano–Micro Letters 2: 164–168.
Smith, A. J., 2004. Medicinal and pharmaceutical uses of seaweed natural products: a review. Journal of Applied Phycology 16: 245–262.
Songa, J. Y., H. K. Janga & B. S. Kim, 2009. Biological synthesis of gold nanoparticles using Magnolia kobus and Diopyros kaki leaf extracts. Process Biochemistry 44: 1133–1138.
Suresh, U., K. Murugan, G. Benelli, M. Nicoletti, D. R. Barnard, C. Panneerselvam, P. Mahesh 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.
Tripathi, A., N. Chandrasekaran, A. M. Raichur & A. Mukherjee, 2009. Antibacterial applications of silver nanoparticles synthesized by aqueous extract of Azadirachta indica (Neem) leaves. Journal of Biomedicine and Nanotechnology 5: 93–98.
Wandscheer, C. B., J. E. Duque, M. A. N. da Silva, Y. Fukuyama, J. L. Wohlke, J. Adelmann & J. D. Fontana, 2004. Larvicidal action of ethanolic extracts from fruit endocarps of Melia azedarach and Azadirachta indica against the dengue mosquito Aedes aegypti. Toxicon 44: 829–835.
World Health Organization, 1996. Report of the WHO Informal Consultation on the Evaluation on the Testing of Insecticides, CTD/WHO PES/IC/96.1. WHO, Geneva: 69.
World Health Organization, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. WHO/HTM/NTD/DEN/2009.1. WHO, Geneva.
World Health Organization, 2010. Dengue Transmission Research in WHO Bulletin [available on internet at http://whqlibdoc.who.int/hq/2005/WHO_CDS_WHOPES_GCDPP_2005.13.pdf]. Accessed 25 June 2010.
Wu, C. H., H. U. Dahms, E. J. Buskey, J. R. Strickler & J. S. Hwang, 2010. Behavioral interactions of the copepod Temora turbinata with potential ciliate prey. Zoological Studies 49: 157–168.
Acknowledgments
The authors thank the Ministry of Science and Technology of Taiwan for supporting this research via Grant Nos. NSC98-2621-B-019-001-MY3, NSC101-2621-B-019-002, NSC102-2923-B-019-001-MY3, MOST 104-2621-M-019-002, and MOST 105-2621-M-019-001 to J. S. Hwang, as well as the Grant Nos. NSC 102-2811-M-019-006, MOST 103-2811-M-019-005, and MOST 104-2811-M-019-005 to L.-C. Tseng.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Juan Carlos Molinero
Rights and permissions
About this article
Cite this article
Kalimuthu, K., Panneerselvam, C., Chou, C. et al. Predatory efficiency of the copepod Megacyclops formosanus and toxic effect of the red alga Gracilaria firma-synthesized silver nanoparticles against the dengue vector Aedes aegypti . Hydrobiologia 785, 359–372 (2017). https://doi.org/10.1007/s10750-016-2943-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-016-2943-z