Skip to main content

Advertisement

SpringerLink
Log in

Predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector, Aedes aegypti, in an aquatic environment treated with mosquitocidal nanoparticles

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Aedes aegypti is a primary vector of dengue and chikungunya. The use of synthetic insecticides to control Aedes populations often leads to high operational costs and adverse non-target effects. Botanical extracts have been proposed for rapid extracellular synthesis of mosquitocidal nanoparticles, but their impact against predators of mosquito larvae has not been well studied. We propose a single-step method for the biosynthesis of silver nanoparticles (AgNP) using the extract of Artemisia vulgaris leaves as a reducing and stabilizing agent. AgNP were characterized by UV–vis spectroscopy, Fourier transform infrared spectroscopy (FTIR), scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX), and X-ray diffraction (XRD). SEM and XRD showed that AgNP were polydispersed, crystalline, irregularly shaped, with a mean size of 30–70 nm. EDX confirmed the presence of elemental silver. FTIR highlighted that the functional groups from plant metabolites capped AgNP, stabilizing them over time. We investigated the mosquitocidal properties of A. vulgaris leaf extract and green-synthesized AgNP against larvae and pupae of Ae. aegypti. We also evaluated the predatory efficiency of Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against larvae of Ae. aegypti, under laboratory conditions and in an aquatic environment treated with ultra-low doses of AgNP. AgNP were highly toxic to Ae. aegypti larval instars (I–IV) and pupae, with LC50 ranging from 4.4 (I) to 13.1 ppm (pupae). In the lab, the mean number of prey consumed per tadpole per day was 29.0 (I), 26.0 (II), 21.4 (III), and 16.7 (IV). After treatment with AgNP, the mean number of mosquito prey per tadpole per day increased to 34.2 (I), 32.4 (II), 27.4 (III), and 22.6 (IV). Overall, this study highlights the importance of a synergistic approach based on biocontrol agents and botanical nano-insecticides for mosquito control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahmad A, Mukherjee M, Mandal D, Senapati S, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Coll Surf B Biointerf 28:313–318

    Article  CAS  Google Scholar 

  • Amer A, Mehlhorn H (2006a) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera: Culicidae). Parasitol Res 99:466–472

    Article  PubMed  Google Scholar 

  • Amer A, Mehlhorn H (2006b) Repellency effect of forty-one essential oils against Aedes, Anopheles, and Culex mosquitoes. Parasitol Res 99:478–490

    Article  PubMed  Google Scholar 

  • Amerasan D, Nataraj T, Murugan K, Madhiyazhagan P, Panneerselvam C, Nicoletti M, Benelli G (2015) Myco-synthesis of silver nanoparticles using Metarhizium anisopliae against the rural malaria vector Anopheles culicifacies Giles (Diptera: Culicidae). J Pest Sci. doi:10.1007/s10340-015-0675-x

  • Arjunan NK, Murugan K, Rejeeth C, Madhiyazhagan P, Barnard DR (2012) Green synthesis of silver nanoparticles for the control of mosquito vectors of malaria, filariasis and dengue. Vector-Born Zoon Dis 12:262–268

    Article  Google Scholar 

  • Bar H, Dipak Bhui KR, Gobinda Sahoo P, Sarkar P (2009) Green synthesis of silver nanoparticles using latex of Jatropha curcas. Cool Surf A Physicochem Eng Asp 339:134–139

    Article  CAS  Google Scholar 

  • Benelli G, Bedini S, Cosci F, Toniolo C, Conti B, Nicoletti M (2015a) Larvicidal and ovideterrent properties of neem oil and fractions against the filariasis vector Aedes albopictus (Diptera: Culicidae): a bioactivity survey across production sites. Parasitol Res 114:227–236

    Article  PubMed  Google Scholar 

  • Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015b) 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

    Article  PubMed  Google Scholar 

  • Bouyer J, Lefrançois T (2014) Boosting the sterile insect technique to control mosquitoes. Tr Parasitol 30:271–273

    Article  Google Scholar 

  • Bowatte G, Perera P, Senevirathne G, Meegaskumbura S, Meegaskumbura M (2013) Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biol Control 67:469–474

    Article  Google Scholar 

  • Chandra G, Bhattacharjee I, Chatterjee SN, Ghosh A (2008) Mosquito control by larvivorous fish. Indian J Med Res 127:13–27

    CAS  PubMed  Google Scholar 

  • Chantraine JM, Laurent D, Ballivian C, Saavedra G, Ibanez R, Vilaseca LA (1998) Insecticidal activity of essential oils on Aedes aegypti larvae. Phytother Res 12:350–354

    Article  CAS  Google Scholar 

  • Chitra G, Balasubramani G, Ramkumar R, Sowmiya R, Perumal P (2015) Mukia maderaspatana (Cucurbitaceae) extract-mediated synthesis of silver nanoparticles to control Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Parasitol Res. doi:10.1007/s00436-015-4320-7

    PubMed  Google Scholar 

  • Cho K, Park J, Osaka T, Park S (2005) The study of antimicrobial activity and preservative effects of nanosilver ingredient. Electrochim Acta 51:956–960

    Article  CAS  Google Scholar 

  • Cooke (1970) The effects of DDT, when used as a mosquito larvicide, on tadpoles of the frog Rana temporaria. Environ Poll 5:259–273

    Article  Google Scholar 

  • Cui S D (1989) Codex of Chinese Traditional Medicine. Hei Long-jiang Science and Technology Press, Ha Er-bin

  • 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

    Article  PubMed  Google Scholar 

  • Dubey M, Seema B, Kushwah BS (2009) Green synthesis of nano silver particles from extract of Eucalyptus hybrida (safeda) leaf. Dig J Nanomat Biostruc 4:537–543

    Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, London, pp 68–78

    Google Scholar 

  • Gillespie GR (2001) The role of introduced trout in the decline of the spotted tree frog (Litoria spenceri) in south-eastern Australia. Biol Cons 100:187–198

    Article  Google Scholar 

  • Goodsell JA, Kats LB (1999) Effect of introduced mosquito fish on Pacific tree frogs and the role of alternative prey. Cons Biol 13:921–924

    Article  Google Scholar 

  • Haldar KM, Haldar B, Chandra G (2013) Fabrication, characterization and mosquito larvicidal bioassay of silver nanoparticles synthesized from aqueous fruit extract of putranjiva, Drypetes roxburghii (Wall.). Parasitol Res 112:1451–1459

    Article  PubMed  Google Scholar 

  • Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391

    Article  CAS  PubMed  Google Scholar 

  • Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110

    Article  Google Scholar 

  • Komak S, Crossland MR (2000) An assessment of the introduced mosquito fish (Gambusia affinis holbrooki) as a predator of eggs, hatchlings and tadpoles of native and non-native anurans. Wildlife Res 27:185–189

    Article  Google Scholar 

  • Kumar D, Chawla R, Dhamodaram P, Balakrishnan N (2014) Larvicidal activity of Cassia occidentalis (Linn.) against the larvae of bancroftian filariasis vector mosquito Culex quinquefasciatus. J Parasitol Res article ID 236838:5

  • Marian MP, Christopher MSM, Selvaraj AM, Pandian TJ (1983) Studies on predation of the mosquito Culex fatigans by Rana tigrina tadpoles. Hydrobiologia 106:59–63

    Article  Google Scholar 

  • Mehlhorn H, Al-Rasheid KA, Al-Quraishy S, Abdel-Ghaffar F (2012) Research and increase of expertise in arachno-entomology are urgently needed. Parasitol Res 110:259–265

  • Mittal AK, Chisti Y, Banerjee UC (2013) Synthesis of metallic nanoparticles using plant extracts. Biotechnol Adv 31:346–356

    Article  CAS  PubMed  Google Scholar 

  • Morgan LA, Buttemer WA (1996) Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentate tadpoles. Aust Zool 30:143–149

    Article  Google Scholar 

  • Murrell S, Wu SC, Butler M (2011) Review of dengue virus and the development of a vaccine. Biotechnol Adv 29:239–247

    Article  CAS  PubMed  Google Scholar 

  • 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. Parasitol Res. doi:10.1007/s00436-015-4417-z

    Google Scholar 

  • 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. doi:10.1016/j.exppara.2015.03.017

    PubMed  Google Scholar 

  • Muthukumaran U, Govindarajan M, Rajeswary M, Hoti SL (2015) Synthesis and characterization of silver nanoparticles using Gmelina asiatica leaf extract against filariasis, dengue, and malaria vector mosquitoes. Parasitol Res. doi: 10.1007/s00436-015-4368-4: 14748:7e

  • Oliva CF, Damiens D, Benedict MQ (2014) Male reproductive biology of Aedes mosquitoes. Acta Trop 132S:S512–S519

    Google Scholar 

  • Patil CD, Patil SV, Borase HP, Salunke BK, Salunkhe RB (2012a) Larvicidal activity of silver nanoparticles synthesized using Plumeria rubra plant latex against Aedes aegypti and Anopheles stephensi. Parasitol Res 110:1815–1822

    Article  PubMed  Google Scholar 

  • Patil CD, Borase HP, Patil SV, Salunkhe RB, Salunke BK (2012b) Larvicidal activity of silver nanoparticles synthesized using Pergularia daemia plant latex against Aedes aegypti and Anopheles stephensi and nontarget fish Poecillia reticulata. Parasitol Res 111:555–562

    Article  PubMed  Google Scholar 

  • Priyadarshini KA, Murugan K, Panneerselvam C, Ponarulselvam S, Hwang JS, Nicoletti M (2012) Biolarvicidal and pupicidal potential of silver nanoparticles synthesized using Euphorbia hirta against Anopheles stephensi Liston (Diptera: Culicidae). Parasitol Res 111:997–1006

    Article  PubMed  Google Scholar 

  • Raghavendra K, Sharma P, Dash AP (2008) Biological control of mosquito populations through frogs: opportunities and constrains. Indian J Med Res 128:22–25

    CAS  PubMed  Google Scholar 

  • Ramanibai R, Velayutham K (2015) Bioactive compound synthesis of Ag nanoparticles from leaves of Melia azedarach and its control for mosquito larvae. Res Vet Sci 98:82–88

    Article  CAS  PubMed  Google Scholar 

  • Rawani A, Ghosh A, Chandra G (2013) Mosquito larvicidal and antimicrobial activity of synthesized nano-crystalline silver particles using leaves and green berry extract of Solanum nigrum L. (Solanaceae: Solanales). Acta Trop 128:613–622

    Article  CAS  PubMed  Google Scholar 

  • Salunkhe RB, Patil SV, Patil CD, Salunke BK (2011) Larvicidal potential of silver nanoparticles synthesized using fungus Cochliobolus lunatus against Aedes aegypti (Linnaeus, 1762) and Anopheles stephensi Liston (Diptera; Culicidae). Parasitol Res 109:823–831

    Article  PubMed  Google Scholar 

  • Sathyavathi R, Balamurali Krishna M, Venugopal Rao S, Saritha R, Narayana Rao D (2010) Biosynthesis of silver nanoparticles using Coriandrum sativum leaf extract and their application in nonlinear optics. Adv Sci Lett 3:1–6

    Article  Google Scholar 

  • Shahverdi AR, Minaeian S, Shahverdi HR, Jamalifar H, Nohi AA (2007) Rapid synthesis of silver nanoparticles using culture supernatants of Enterobacteria: a novel biological approach. Proc Biochem 42:919–923

    Article  CAS  Google Scholar 

  • 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 Coll Interf Sci 275:496–502

    Article  CAS  Google Scholar 

  • Sinha B (2010) An appraisal of the traditional post-harvest pest management methods in Northest Indian uplands. Ind J Trad Knowl 9:536–543

    Google Scholar 

  • Sivapriyajothi S, Mahesh Kumar P, Kovendan K, Subramaniam J, Murugan K (2014) Larvicidal and pupicidal activity of synthesized silver nanoparticles using Leucas aspera leaf extract against mosquito vectors, Aedes aegypti and Anopheles stephensi. J Entomol Acarol Res 46:1787

    Article  Google Scholar 

  • Song JY, Jang HK, Kim BS (2009) Biological synthesis of gold nanoparticles using Magnolia kobus and Diospyros kaki leaf extracts. Proc Biochem 44:1133–1138

    Article  CAS  Google Scholar 

  • Subarani S, Sabhanayakam S, Kamaraj C (2013) Studies on the impact of biosynthesized silver nanoparticles (AgNPs) in relation to malaria and filariasis vector control against Anopheles stephensi Liston and Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol Res 112:487–499

    Article  PubMed  Google Scholar 

  • 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

  • Suresh U, Murugan K, Benelli G, Nicoletti M, Barnard DR, Panneerselvam C, Mahesh Kumar P, Subramaniam J, Dinesh D, Chandramohan B (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). Parasitol Res 114:1551–1562

    Article  PubMed  Google Scholar 

  • Wang J, Zhu F, Zhou XM, Iu CY, Lei CL (2006) Repellent and fumigant activity of essential oil from Artemisia vulgaris to Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J Stor Prod Res 42:339–347

    Article  CAS  Google Scholar 

  • Webb C, Joss J (1997) Does predation by the fish Gambusia holbrooki (Atheriniformes: Poeciliidae) contribute to declining frog populations? Aust Zool 30:316–326

    Article  Google Scholar 

  • WHO (2015) Dengue and severe dengue. Fact sheet N°117. World Health Organization, Geneva

    Google Scholar 

Download references

Acknowledgments

The Authors are grateful to the Department of Science and Technology (New Delhi, India), Project No. DST/SB/EMEQ-335/2013, for providing financial support. This work was also supported by King Saud University, Deanship of Scientific Research, and College of Sciences Research Centre. Funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Heinz Mehlhorn and two anonymous reviewers improved an earlier version of the manuscript.

Conflicts of interest

The authors declare no conflicts of interest. Dr. Giovanni Benelli is currently an Editorial Board Member of Parasitology Research, but this does not alter the authors’ adherence to all the Parasitology Research policies on sharing data and materials.

Compliance with ethical standards

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.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Author information

Authors and Affiliations

  1. Division of Entomology, Department of Zoology, School of Life sciences, Bharathiar University, Coimbatore, 641 046, Tamil Nadu, India

    Kadarkarai Murugan, Vishwanathan Priyanka, Devakumar Dinesh, Pari Madhiyazhagan, Chellasamy Panneerselvam, Jayapal Subramaniam, Udaiyan Suresh, Balamurugan Chandramohan & Mathath Roni

  2. Department of Environmental Biology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185, Rome, Italy

    Marcello Nicoletti

  3. Department of Botany and Microbiology, College of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Abdullah A. Alarfaj & Murugan A. Munusamy

  4. Department of Reproduction, National Research Institute for Child Health and Development, Tokyo, 157-8535, Japan

    Akon Higuchi

  5. Department of Parasitology, Faculty of Veterinary Medicine, Benha University, Moshtohor, Toukh, 13736, Egypt

    Hanem F. Khater

  6. Kauai Agricultural Research Center, University of Hawaii at Manoa, 7370 Kuamo’o Road, Kapaa, 97646, HI, USA

    Russell H. Messing

  7. Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124, Pisa, Italy

    Giovanni Benelli

Authors
  1. Kadarkarai Murugan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vishwanathan Priyanka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Devakumar Dinesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pari Madhiyazhagan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chellasamy Panneerselvam
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jayapal Subramaniam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Udaiyan Suresh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Balamurugan Chandramohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mathath Roni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marcello Nicoletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Abdullah A. Alarfaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Akon Higuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Murugan A. Munusamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hanem F. Khater
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Russell H. Messing
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Giovanni Benelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giovanni Benelli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murugan, K., Priyanka, V., Dinesh, D. et al. Predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector, Aedes aegypti, in an aquatic environment treated with mosquitocidal nanoparticles. Parasitol Res 114, 3601–3610 (2015). https://doi.org/10.1007/s00436-015-4582-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4582-0

Keywords

Search

Navigation