Skip to main content

Advertisement

Log in

Insecticidal potency of Aspergillus terreus against larvae and pupae of three mosquito species Anopheles stephensi, Culex quinquefasciatus, and Aedes aegypti

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Microbial control agents offer alternatives to chemical pest control, as they can be more selective than chemical insecticides. The present study evaluates the mosquito larvicidal and pupicidal potential of fungus mycelia using ethyl acetate and methanol solvent extracts produced by Aspergillus terreus against Anopheles stephensi, Culex quinquefasciatus, and Aedes aegypti. The A. terreus mycelia were extracted after 15 days from Sabouraud dextrose broth medium. The ethyl acetate extracts showed lethal concentration that kills 50 % of the exposed larvae (LC50) and lethal concentration that kills 90 % of the exposed larvae (LC90) values of the first, second, third, and fourth instar larvae of An. stephensi (LC50 = 97.410, 102.551, 29.802, and 8.907; LC90 = 767.957, 552.546, 535.474, and 195.677 μg/ml), Cx. quinquefasciatus (LC50 = 89.584, 74.689, 68.265, and 67.40; LC90 = 449.091, 337.355, 518.793, and 237.347 μg/ml), and Ae. aegypti (LC50 = 83.541, 84.418, 80.407, and 95.926; LC90 = 515.464, 443.167, 387.910, and 473.998 μg/ml). Pupicidal activity of mycelium extracts was tested against An. stephensi (LC50 = 25.228, LC90 = 140.487), Cx. quinquefasciatus (LC50 = 54.525, LC90 = 145.366), and Ae. aegypti (LC50 = 10.536, LC90 = 63.762 μg/ml). At higher concentration (500 μg/ml), mortality starts within the first 6 h of exposure. One hundred percent mortality occurs at 24-h exposure. The overall result observed that effective activity against selected mosquito larvae and pupae after 24 h was a dose and time-dependent activity. These ensure that the resultant mosquito population reduction is substantial even where the larvicidal and pupicidal potential is minimal. The FTIR spectra of ethyl acetate extract reflect prominent peaks (3448.32, 3000.36, 2914.59, 2118.73, 1668.21, 1436.87, 1409.02, 954.33, 901.13, and 704.67 cm−1). The spectra showed a sharp absorption band at 1314.66 cm−1 assigned to wagging vibration of the C–H group. The band at 1023.59 cm−1 developed for C–O and C=N, respectively, and was commonly found in carboxylic acid and amine groups. GC–MS analysis of ethyl acetate extracts showed the presence of six compounds, of which the major compounds were identified as n-hexadecanoic acid (15.31 %) and methyl 12,15-octadecadienoate (31.989 %), based on their peak molecular weight. The HPLC analysis result highlights that the A. terreus ethyl acetate extract was compared with pure n-hexadecanoic acid which resulted in similar retention time of 19.52 and 19.38, respectively. Thus, the active compound produced by this species would be more useful against vectors responsible for diseases of public health importance. This is the first report on mosquito larvicidal and pupicidal activity of ethyl acetate extract produced by A. terreus species.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Am Mosq Control 3:302–303

    Google Scholar 

  • Abdel-baky NF, Abdel-Salam AH (2003) Natural incidence of Cladosporium spp. as a biocontrol agent against whiteflies and aphids in Egypt. J Appl Entomol 127:228–235

    Article  Google Scholar 

  • Aparna V, Kalarickal V, Dileep Pradeep K, Mandal PK, Sadasivan C, Haridas M (2012) Anti-inflammatory property of n-hexadecanoic acid: structural evidence and kinetic assessment. Chem Biol Drug Des 80:434–439

    Article  CAS  Google Scholar 

  • Belkin JN (1968) Mosquito studies (Diptera: Culicidae) VII. The Culicidae of New Zealand. Contributions of the American Entomological Institute 3:1–181

  • Bigelis R, Arora DK (1992) Organic acids of fungi. In: Arora DK, Elander RP, Murekji KG (eds) Handbook of applied mycology vol. 4. Fungal biotechnology. Marcel Dekker Inc, New York, pp 357–376

    Google Scholar 

  • Devi NN, Prabakaran JJ (2014) Bioactive metabolites from an endophytic fungus Penicillium sp. isolated from Centella asiatica. Curr Res Environ Appl Mycol 4(1):34–43

    Google Scholar 

  • Dhanasekaran D, Sakthi V, Thajuddin N, Panneerselvam A (2010) Preliminary evaluation of Anopheles mosquito larvicidal efficacy of mangrove actinobacteria. Int J Appl Biol Pharm Technol 1(2):374–381

    Google Scholar 

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

    Google Scholar 

  • Garder JM, Pillai JS (1987) Tolypocladium cylindrosporum (Deuteromycotina: Moniales), a fungal pathogen of the mosquito Ae. australis. Mycopathology 97:83–88

    Article  Google Scholar 

  • Garret SD (1976) Soil fungi and soil fertility. Program Press, Oxford, p 165

    Google Scholar 

  • Geetha I, Manonmani AM, Prabakaran G (2011) Bacillus amyloliquefaciens: a mosquitocidal bacterium from mangrove forests of Andaman & Nicobar islands, India. Acta Trop 120(3):155–159

    Article  CAS  Google Scholar 

  • Govindrajan M, Jebamesan A, Reetha D (2005) Larvicidal effect of extracellular secondary metabolites of different fungi against the mosquito, Cx quinquefasciatus Say. Trop Biomed 22(1):1–3

    Google Scholar 

  • Hamill RL, Higgens C, Boaz ZE (1969) The structure of beauvericin, a new depsipetide antibiotic toxic to Artemia salvia. Tetrahedron Lett 49:4255–4258

    Article  CAS  Google Scholar 

  • Ignacimuthu S, Paul-raj MG (2009) Non-chemical insect pest management (report). Curr Sci 97:136–137

    Google Scholar 

  • Kaji A, Iwata T, Kiriyama N, Wakusawa S, Miyomoto K (1994) Four new metabolites of acetylaranotin and terrein as plant growth inhibitors from a strain of Aspergillus terreus. Agric Biol Chem 47:2637–2638

    Google Scholar 

  • Kamata S, Sakai H, Hirota A (1983) Isolation of acetylaranotin, bisdethiodi (methylthio)-acetylaranotin and terrein as plant growth inhibitors from a strain of Aspergillus terreus. Agri Biol Chem 47:2637–2638

  • Kerwin JL, Washino RK (1988) Field evaluation of Lagenidium giganteum (Oomycetes: Lagenidiales) and description of a natural epizootic involving a new isolates of fungus. J Med Entomol 25:452–460

    Article  CAS  Google Scholar 

  • Klich, MA, Pitt JI (1992) A laboratory guide common Aspergillus species and their teleomorphs. Published by Commonwealth Scientific and Industrial Research Organisation, Division of Food Processing

  • Knols BGJ, Bukhari T, Farenhorst M (2010) Entomopathogenic fungi as the next generation control agents against malaria mosquitoes. Future Microbiol 5:339–341

    Article  Google Scholar 

  • Kumar NR, Arasu VT, Gunasekaran P (2002) Genotyping of antifungal compounds producing plant promoting rhizobacteria, Pseudomonas fluorescens. Curr Sci 82:1463–1466

    CAS  Google Scholar 

  • Lowe DA (1992) Fungal enzymes. In: Arora DK, Elander RP, Murekji KG (eds) Handbook of applied mycology vol. 4. Fungal biotechnology. Marcel Dekker Inc, New York, pp 681–706

    Google Scholar 

  • Manilal A, Sujitha S, Selvin J, Shakir C, Seghal Kiran G (2009) Antibacterial activity of Falkenbergia hillebrandii (Born) from the Indian Coast against human pathogens. Int J Exp Biol 78:161–166

    Google Scholar 

  • Matha V, Weiser JA, Olejricek J (1988) The effect of tolypin on Tolypocladium niveum crude extract against mosquito and black fly larvae in laboratory. Folia Parasitol 35:379–381

    CAS  Google Scholar 

  • McCray EM, Womeldorf DJ, Husbands RC, Eliason DA (1973) Laboratory observations and field tests with Lagenidium against California mosquitoes. Proc Calif Mosq Control Assoc 41:123–128

    Google Scholar 

  • Merriam TL, Axtell RC (1982) Evaluation of the entomogenous fungi Culicinomyces clavosporus and Coelomomyces giganteum for control of the salt marsh mosquito, Ae. taeniorhynchus. Mosq News 42:594–602

    Google Scholar 

  • Miller PA, Thrown PW, Fulmor W, Morton GO, Karliner J (1968) An epidithiopiperazinone antiviral agent from Aspergillus terreus. Biochem Biophys Res Commun 35:219–221

  • Misra RN, Hai-yun X, Kim KS, Songfeng L, Wen-Ching H, Barbosa SA, Hunt JT, Rawlins DB, Weifang S, Ahmed SZ, Ligang Q, Bang-Chi C, Rulin Z, Bednarz MS, Kellar KA, Mulheron JG, Roberta B, Urvashi R, Amrita K, Punit M, Ranadive SA, Sack JS, Tokarski JS, Pavletich NP, Lee FY, Webster KR, David Kimball S (2004) N-(Cycloalkylamino)acyl-2-aminothiazole inhibitors of cyclin-dependent kinase2. N-[5-[[[5-(1,1-Dimethylethyl)-2-oxazolyl]methyl]thio]-2-thiazolyl]-4-piperidinecarboxamide (BMS-387032), a highly efficacious and selective antitumor agent. J Med Chem 47:1719–1728

    Article  CAS  Google Scholar 

  • Mittal PK, Adak T, Subbarao SK (2005) Inheritance of resistance to Bacillus sphaericus toxins in a laboratory selected strain of An. stephensi (Diptera: Culicidae) and its response to Bacillus thuringiensis var. israelensis. Curr Sci 89:442–443

    Google Scholar 

  • Moraes AML, Costa GL, Camargo Barcellos MZ, Oliveira RL, Oliveira PC (2001) The entomopathogenic potential of Aspergillus spp in mosquitoes vectors of tropical diseases. J Bask Microbiol 41:45–49

  • Namita S, Prakash S (2010) Effect of Chrysosporium keratinophilum metabolites against Cx. quinquefasciatus after chromatographic purification. Parasitol Res 107:1329–1336

    Article  Google Scholar 

  • Namuli A, Abdullah N, Sieo CC, Zuhainis SW, Oskoueian E (2011) Phytochemical compounds and antibacterial activity of Jatropha curcas Linn. J Med Plant Res 5(16):3982–3990

    CAS  Google Scholar 

  • Nilesh JT, Manish PP (2009) Synthesis and in vitro antimicrobial evaluation of 4H-pyrazolopyran, -benzopyran and naphthopyran derivatives of 1H-pyrazole. ARKIV 13:363–380

    Google Scholar 

  • Peng Z, Yang J, Wang H, Simons FER (1999) Production and characterization of monoclonal antibodies to two new mosquito Ae. aegypti salivary proteins. Insect Biochem Mol Biol 29:909–914

    Article  CAS  Google Scholar 

  • Peter H, Matha V, Roberts DW (1989) Enzymes involved in the synthesis of fungal toxins. In: Proceedings of international conference biopesticide, theory and practice. pp. 169–181

  • Priyanka, Srivastava JN, Prakash S (2001) Chrysosporium tropicum efficacy against Anopheles stephensi larvae in the laboratory. J Am Mosq Control Assoc 17:127–130

  • Rahuman A, Geetha Gopalakrishnan B, Saleem Ghousea S, Arumugam B (2000) Himalayan effect of Feronia limonia on mosquito larvae. Fitoterapia 71:553–555

    Article  CAS  Google Scholar 

  • Reuben R, Tewari SC, Hiriyan J, Akiyama J (1994) Illustrated keys to species Culex (Culex) associated with Japanese encephalitis in Southeast Asia (Diptera: Culicidae). Mosq Syst 26:75–96

    Google Scholar 

  • Rizna Triana D, Minarti, Akhmad D, Hanny Mulyani (2008) Emodin, an anthraquinone from ethyl acetate extract of Aspergillus terreus koji. Proceedings of the international seminar on chemistry pp.731–734

  • Rozendaal JA (1997) Vector control: methods for use individuals and communities. World Health Organization, Geneva

    Google Scholar 

  • Saurav K, Rajakumar G, Kannabiran K, Rahuman AA, Velayutham K, Elango G, Kamaraj C, Zahir AA (2011) Larvicidal activity of isolated compound 5-(2,4-dimethylbenzyl) pyrrolidin-2-one from marine Streptomyces VITSVK5 sp. against R. microplus, An. stephensi, and Cx. tritaeniorhynchus. Parasitol Res. doi:10.1007/s00436-011-2682-z

    Google Scholar 

  • Schimmel TG, Coffman AD, Parsons SJ (1998) Effect of butyrolactone I on the producing fungus, Aspergillus terreus. J Appl Environ Microbiol 64:3707–3712

  • Scholte EJ, Takken W, Knols BGJ (2007) Infection of adult Ae. aegypti and An. albopictus mosquitoes with the entomopathogenic fungus Metarhizium anisopliae. Acta Trop 102:151–158

    Article  Google Scholar 

  • Senthilkumar G, Madhanraj P, Panneerselvam S (2011) A studies on the compounds and its antifungal potentiality of fungi isolated from paddy field soils of Jenbagapuram Village, Thanjavur District, and South India. Asian J Pharm Res 1:19–21

    Google Scholar 

  • Senthilkumar N, Murugesan S, Suresh Babu D (2014) Metabolite profiling of the extracts of endophytic fungi of entomopathogenic significance, Aspergillus flavus and Nigrospora sphaerica isolated from tropical tree species of India, Tectona grandis L. J Agric Life Sci 1:108–114

    Google Scholar 

  • Shamroukh AH, Zaki MEA, Morsy EH, Abdel-Motti FM, Abdel-Megeid FME (2007) Synthesis of pyrazolo[49,39:5,6]pyrano[2,3-d]pyrimidine derivatives for antiviral evaluation. Arch Pharm Chem Life Sci 340:236–243

    Article  CAS  Google Scholar 

  • Silva RO, Silva HHG, Luz C (2004) Effect of Metarhizium anisopliae isolated from soil of the central Brazilian cerrado against Ae. aegypti larvae under laboratory conditions. Rev Patol Trop 33:207–216

    Google Scholar 

  • Singh G, Prakash S (2012) Evaluation of culture filtrates of Culicinomyces clavisporus: mycoadulticide for Culex quinquefasciatus, Aedes aegypti and Anopheles stephensi. Parasitol Res 110(1):267–272

    Article  Google Scholar 

  • Takahashi I, Ojima N, Ogura K, Seto S (1978) Purification and characterization of dimethyl pyrophosphate: aspulvinone dimethylallyl transferase from Aspergillus terreus. J Biochem 17(13):2696–2702

  • Thenmozhi M, Gopal JV, Kannabiran K, Rajakumar G, Velayutham K, Rahuman AA (2013) Ecofriendly approach using marine actinobacteria and its compounds to control ticks and mosquitoes. Parasitol Res 112(2):719–729

  • Thimiri LD, Krishnan K, Venkatesan GK, Govindasamy R, Chidambaram J, Thirunavukkarasu S, Rahuman AA (2012) Isolation and characterisation of acaricidal and larvicidal novel compound (2S,5R,6R)-2-hydroxy-3,5,6-trimethyloctan-4-one from Streptomyces sp. against blood-sucking parasites. Parasitol Res 111(3):1151–63

  • Vertesy L, Burger H, Kenja J, Knauf M, Kogler H, Paulus EF, Ramakrishna NV, Swamy KH, Vijaykumar EF, Hammann P (2000) Kodaistatin, novel inhibitor of glucose-6-phosphate translocase TI, from Aspergillus terreus thom DSM 11247, isolated and structural elucidation. Medline 53(7):677–686

    CAS  Google Scholar 

  • Vigneshwaran N, Ashtaputre NM, Varadarajan PV, Nachane RP, Paralikar KM, Balasubramanya RH (2007) Biological synthesis of silver nanoparticles using the fungus Aspergillus flavus. Mater Lett 61:1413–1418

    Article  CAS  Google Scholar 

  • Violeta M, Slavica E, Zorica D, Juranic TS, Ljubinka J, Branislav R, Marijana K, Milan D (2011) Synthesis, antitumor activity and QSAR studies of some 4-aminomethylidene derivatives of edaravone. Bioorg Chem 39:18–27

    Article  Google Scholar 

  • Vyas N, Dua KK, Prakash S (2007) Efficacy of Lagenidium giganteum metabolites on mosquito larvae with reference to non target organisms. Parasitol Res 101:385–390

    Article  Google Scholar 

  • Wei JC (1979) Fungi identification manual (in Chinese). Shanghai Scientific and Technological Press, Shanghai, p 780

    Google Scholar 

  • Weiser J, Matha V, Zizka Z, Jegorov A (1992) Ultrastructural changes in Cx. pipiens larvae treated with tolypin, the insecticidal metabolite of Tolypocladium inflatum Gams (Deuteromycetes). Cytobios 69:179–186

    CAS  Google Scholar 

  • World Health Organization (2007) Global plan to combat neglected tropical diseases 2008–2015 WHO/CDS/NTD/2007.40

  • World Health Organization (2009) Weekly epidemiological record. 84(42):437–444

  • World Health Organization (2010a) Guidelines for the treatment of malaria 2nd edition. WHO 529:909–914

    Google Scholar 

  • World Health Organization (2010b) Global programme to eliminate lymphatic filariasis-progress report on mass drug administration in 2009 weekly epidemiological record. 85:365–372

  • Xu J, Xianqun L, Wenhua Z, Junping Z, Renxiang T (2014) Characterization of volatile constituents from an endophytic Aspergillus fumigatus strain. J Chem Pharm Res 6(4):893–897

    Google Scholar 

  • Zhioua E, Heyer H, Browning M, Ginsberg HS, LeBrun RA (1999) Pathogenicity of Bacillus thurigiensis variety kurstaki to Ixodes scapularis (Acari: Ixodidae). J Med Entomol 36(6):90–902

    Google Scholar 

Download references

Acknowledgments

The first author is gratefully thankful to Periyar University for granting University Research Fellowship (URF). We would like to thank the Vellore Institute of Technology (VIT) for GC–MS analysis. We also express our heartfelt thanks to the Department of Biotechnology, Periyar University, Salem, for providing necessary infrastructural facility for carry out this research work successfully.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Devarajan Natarajan.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ragavendran, C., Natarajan, D. Insecticidal potency of Aspergillus terreus against larvae and pupae of three mosquito species Anopheles stephensi, Culex quinquefasciatus, and Aedes aegypti . Environ Sci Pollut Res 22, 17224–17237 (2015). https://doi.org/10.1007/s11356-015-4961-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4961-1

Keywords

Navigation