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

Volumn 785, Issue 1, 2017, Pages 359-372

  Kalimuthu, Kandasamy ^a,b   Panneerselvam, Chellasamy ^b   Chou, Chi ^d   Lin, Showe Mei ^a   Tseng, Li Chun ^a   Tsai, Kun Hsien ^e   Murugan, Kadarkarai ^c   Hwang, Jiang Shiou ^a,f  

^a NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^b UNIVERSITY OF TABUK   (Saudi Arabia)

^c BHARATHIAR UNIVERSITY   (India)

^d MACKAY MEMORIAL HOSPITAL   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Aedes aegypti; Gracilaria firma; Megacyclops formosanus; Red algae; Silver nanoparticles (AgNPs)

Indexed keywords

AQUATIC ECOSYSTEM; BIOASSAY; BIOLOGICAL CONTROL; CELLS AND CELL COMPONENTS; DISEASE VECTOR; EPIDEMIOLOGY; MOSQUITO; NANOPARTICLE; PREDATION; RED ALGA; SEAWEED; SILVER; TOXICITY;

AEDES AEGYPTI; COPEPODA; CYCLOPOIDA; GRACILARIA FIRMA; MEGACYCLOPS; RHODOPHYTA;

EID: 84990944676     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-016-2943-z     Document Type: Article

References (64)

1. Abbott, W. S., 1925. A method of computing the effectiveness of insecticides. Journal of Economic Entomology 18: 267–269.
2. 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.
3. Alder, H. L. & E. B. Rossler, 1977. Introduction to Probability and Statistics, 6th ed. WH Freeman Company, San Francisco: 246.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. Benn, T. & P. Westerhoff, 2008. Nanoparticle silver released into water from commercially available sock fabrics. Environmental Science and Technology 42: 4133–4139.
12. 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.
13. 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.
14. 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.
15. Finney, D. J., 1971. Probit Analysis. Cambridge University Press, London: 68–78.
16. 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.
17. Halstead, S. B., 2012. Dengue vaccine development: a 75% solution? Lancet 380: 1535–1536.
18. 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.
19. 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.
20. Hwang, J. S. & K. Martens (eds), 2011. Zooplankton behavior and ecology. Hydrobiologia 666: 179–338.
21. Hwang, J. S. & J. R. Strickler, 2001. Can copepods differentiate prey from predator hydromechanically? Zoological Studies 40: 1–6.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Marten, G. G. & J. W. Reid, 2007. Cyclopoid copepods. Journal of the American Mosquito Control Association 23: 65–92.
39. Marten, G. G., E. S. Bordes & M. Nguyen, 1994. Use of cyclopoid copepods for mosquito control. Hydrobiologia 292(293): 491–496.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. Shrivastava, S. & D. Dash, 2010. Label-free colorimetric estimation of proteins using nanoparticles of silver. Nano–Micro Letters 2: 164–168.
56. Smith, A. J., 2004. Medicinal and pharmaceutical uses of seaweed natural products: a review. Journal of Applied Phycology 16: 245–262.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. World Health Organization, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. WHO/HTM/NTD/DEN/2009.1. WHO, Geneva.
63. 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.
64. 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.