Skip to main content
SpringerLink
Log in

Pathogenicity of native isolates of entomopathogenic fungi Beauveria and Metharizium genera on Microcerotermes diversus (Blattodea: Termitidae) in the laboratory

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

Microcerotermes diversus Silvestri (Blattodea: Termitidae) is a worldwide destructive termite whose control by conventional methods is often difficult. Biological control using entomopathogenic fungi could be an alternative management strategy. Two species of entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana, isolated from natural habitats of Mashhad and Lahijan regions, Iran. The fungi were characterized based on sequences of ITS gene as well as classic data. Then, the infectivity of both isolates of M. anisopliae and B. bassiana in different concentrations (1 × 104, 1 × 105, 1 × 106, 1 × 107, and 1 × 108 conidia/ml) were evaluated under laboratory conditions by two methods, including spray and pipetting against termite, M. diversus. Both entomopathogenic fungi species were capable of infecting and killing M. divesrus. In the pipetting method, the LC50 value for B. bassiana and M. anisopliae calculated 8.03 × 105 (conidia/ml) and 1.03 × 106 (conidia/ml), respectively. But in the spray method, the effect of M. anisopliae on M. diversus was more than B. bassiana. The LC50 value in the spray method for B. bassiana and M. anisopliae was 3.52 × 107 (conidia/ml) and 1.65 × 106 (conidia/ml). The mortality caused by the fungus was dose-dependent, with the highest mortality recorded at the highest concentration. In the pipetting method, the mortality rate for B. bassiana and M. anisopliae was 0 to 97.5% and 0 to 100% at 8 day post infection. In the spray method, the mortality percentage for B. bassiana was from 2.5 to 72.5% and for M. anisopliae was 0 to100% by 4 days post-infection. The results of this study indicated that B. bassiana and M. anisopliae are potentially useful biological control agents for M. diversus. Future studies with field trails will provide a confident approach toward termite management.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbott W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Google Scholar 

  • Almeida JEM, Alves SB, Pereira RM (1997) Selection of Beauveria spp. isolates for control of the termite Heterotermes tenuis (Hagen 1858). J Appl Entomol 121:539–543

    Google Scholar 

  • Arora K, Arora SS (1995) Lindane as termiticide—a review. In: Singh Y (ed) termite management in buildings. Tata McGraw-hill publishing company limited, New Delhi, pp 56–59. Bull Entomol Res 80:309–330

    Google Scholar 

  • Balachander M, Remadevi OK, Sasidharan TO, Bai S (2009) Infectivity of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) isolates to the arboreal termite Odontotermes sp. (Isoptera: Termitidae). Int J Trop Insect Sc 29(04):202–207

    Google Scholar 

  • Burges HD (1981) Strategy for the microbial control of pests in 1980 and beyond. In: Burges HD (ed) Microbial control of pests and plant diseases, 1970–1980. Academic, London, pp 797–836

    Google Scholar 

  • Cheraghi A, Habbibpour B, Mossadegh MS, Sharififard M (2012) Horizontal transmission of the entomopathogen fungus Metarhizium anisopliae in Microcerotermes diversus groups. Insects 3:709–718. https://doi.org/10.3390/insects3030709

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheraghi A, Habibpour B, Saied Mossadegh M (2013) Application of bait treated with the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin for the control of Microcerotermes diversus Silv. Psyche 5 page, https://doi.org/10.1155/2013/865102

  • Chouvenc T, Su NY, Elliott ML (2008) Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. J Econ Entomol 101:885–893

  • Culliney TW, Grace JK (2000) Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. B Entomol Res 90:9–21

    CAS  Google Scholar 

  • Darsouei R, Karimi J, Ghadamyari M, Hosseini M (2018) Diverse natural enemies of the sugar beet army worm, Spodoptera exigua in north east of Iran. Entomol News 127(5):446–464

    Google Scholar 

  • Dong C, Zhang J, Huang H, Chen W, Hu Y (2009) Pathogenicity of new China variety of Metarhizium anisopliae (Manisopliae var. dcjhyium) to subterranean termite Odontotermes formosanus. Microbiol Res 164:27–35

    CAS  PubMed  Google Scholar 

  • Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. Biocontrol 46:387–400

    Google Scholar 

  • Felsenstein J (1985) Confidence intervals on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Fernandes PM (1991) Controle microbiano de Cornitermes cumulans (Kollar, 1832) Utilizando Beauveria bassiana (Bals) Vuill and Metarhizium anisopliae (metsch) Sorok. PhD dissertation, ESALQ-Universidade de Sao Paulo, Piracicaba, Brazil

  • Ghayourfar R (2005) Three new species of termites from Iran. Zool Middle East 34:61–66

    Google Scholar 

  • Ghayourfar R, Mohammadpour K (2009) An investigation on the subterranean termite control in date palm orchard of Saravan region using baiting system. App Entomol Phytopath 87:1–17

    Google Scholar 

  • Grace JK (1993) Microbial termite control: effect of entomogenous fungi on the Formosan subterranean termite (Isoptera: Rhinotermitidae). In:Wildey KB, Robinson WH (eds) Proceedings of 1st international conference on insect pest in the urban environment, St John’s College, Cambridge, 30 June–3 July 1993, Organizing committee of the international conference on insect pests in the urban environment, Exeter, pp 474

  • Grace JK, Zoberi MH (1992) Experimental evidence for transmission of Beauveria bassiana by Reticuliitermes flavipes workers (Isoptera: Rhinotermitidae). Sociobiology 20:23–28

  • Habibpour B (1994) Termites (Isoptera) fauna, economic importance and their biology in Khuzestan, (Iran). M.S. thesis, College of Agriculture, Shahid-Chamran University of Ahvaz, Iran. 120 pp

  • Habibpour B (2006) Laboratory and field evaluation of bait-toxicants for suppression subterranean termite populations in Ahvaz (Iran) [Ph.D. thesis], Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Khuzestan

  • Hamill RL, Higgins CE, Boaz HE, Gorman M (1969) The structure of beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahedron Lett (49):4255–5258

  • Jones WE, Grace JK, Tamashiro M (1996) Virulence of seven isolates of Beauveria bassiana and Metarhizium anisopliae to Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ Entomol 25:481–487

    Google Scholar 

  • Karimi J, Darsouei R (2014) Presence of the endosymbiont Wolbachia among some fruit flies (dip., Tephritidae) from Iran and its evolutionary history. J Asia Pac Entomol 17:105–112

    CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    CAS  PubMed  Google Scholar 

  • Kramm KR, West DF, Rockenbach PG (1982) Termite pathogens: transfer of the entomopathogen Metarhizium anisopliae between Reticulitermes species termites. J Invertebr Pathol 40:1–6

    Google Scholar 

  • Kramm KR, West DF, Rokenback PG (1992) Termite pathogens trasfer of the entomopathogen Metarhizium anisopliae between Reticulitermitidae. J Invertebr Pathol 39:1–5

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacey LA, Kaya HK (2000) Eds. Springer: London, UK, 2000; pp. 153–177

  • Lai PY, Tamashiro M, Fujii JK (1982) Pathogenicity of six strains of entomogenous fungi to Coptotermes formosanus. J Invertebr Pathol 39:1–5

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  PubMed  Google Scholar 

  • Logan JWM, Cowie RH, Wood TG (1990) Termite (Isoptera) control in agriculture and forestry by non-chemical methods: a review. Bull Entomol Res 80:309–330

    Google Scholar 

  • Milner RJ (2000) Improved formulation of Metarhizium for biological control of termites CSIRO division of termites. Entomol Tech Rep 86:37

    Google Scholar 

  • Milner RJ, Staples JA (1996) Biological control of termites: results and experiences within a CSIRO project in Australia. Biocontrol Sci Tech 6:3–9

    Google Scholar 

  • Milner RJ, Staples JA, Lutton GG (1998) The selection of an isolate of the hyphomycete fungus, Metarhizium anisopliae, for the control of termites in Australia. Biol Control 11:240–247

    Google Scholar 

  • Neves PJ, Alves SB (2000) Selection of Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) Sorok strains for control of Cornitermes cumulans (Kollar). Braz Arch Biol Technol 43:373–378

    Google Scholar 

  • Pais M, Das BC, Ferron P (1981) Depspeptides from Metarhizium anisopliae. Phytochemistry 20:715–723

    CAS  Google Scholar 

  • Pell JK, Eilenberg J, Hajek AE, Steinkraus DC (2001) In: butt, T.M., Jackson, C., Magan, N. (Eds.), Fungi as biocontrol agents: Progress, problems and potential. CAB International, Wallingford, pp 71–153

    Google Scholar 

  • Pik-Kheng H, Choon-Fah J, Bong KJ, Amartalingam R (2009) Evaluation of Metarhizium anisopliae var. anisopliae (Deuteromycotina: Hyphomycete) isolates and their effects on subterranean termite Coptotermes curvignathus (Isoptera: Rhinotermitidae). Am J Agric Biol Sci 4(4):289–297

    Google Scholar 

  • Rahimzadeh AR, Rashid M, Sheikhi Garjan A, Naseri B (2012) Laboratory evaluation of Metarhizium anisopliae (Metschnikoff) for controlling Amitermes vilis (Hagen) and Microcerotermes gabrielis (Weidner) (Isoptera: Termitidae). J Crop Prot 1(1):27–34

    Google Scholar 

  • Ramakrishnan R, Suiter DR, Nakatsu CH, Humber RA, Bennett GW (1999) Imidacloprid-enhanced Reticulitermes lavipes (Isoptera: Rhinotermitidae) susceptibility to the entomopathogen Metarhizium anisopliae. J Econ Entomol 92(5):1125–1132

    CAS  Google Scholar 

  • Rath AC (2000) The use of entomopathogenic fungi for control of termites. Biocontrol Sci Tech 10:563–581

  • Ravindran K, Qiu D, Sivaramakrishnan S (2015) Sporulation characteristics and virulence of Metarhizium anisopliae against subterranean termites (Coptotermes formosanus). Int J Microbiol Res 6(1):1–4

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sajap AS, Kaur K (1990) Histopathology of Metarhizium anisopliae, an entomopathogenic fungus, infection in the termite, Coptotermes curvignathus. Pertanika 13:331–334

    Google Scholar 

  • SAS Institute (1989) SAS/STAT user's guide, release 6.03. SAS Institute, Cary

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction "primers". Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Singha D, Singha B, Dutta BK (2011) Potential of Metarhizium anisopliae and Beauveria bassiana in the control of tea termite Microtermes obesi Holmgren in vitro and under field conditions. J Pest Sci 84:69–75

    Google Scholar 

  • Toumanoff C, Rombaut J (1965) Action de divers champignons entomophage cultives sur les milieu appropries attractifs, sur le termite de Saintonge Reticulitermes santonensis. Annales de Parasitologie 40:605–609

    Google Scholar 

  • Vargo EL, Husseneder C, Grace JK (2003) Colony and population genetic structure of the Formosan subterranean termite, Coptotermes fomosanus, in Japan. Mol Ecol 12(10):2599–2608

    CAS  PubMed  Google Scholar 

  • Vega FE, Dowd PF, Lacey LA, Pell JK, Jackson DM, Klein MG (2000) Dissemination of beneficial microbial agents by insects. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Kluwer, London, pp 153–177

    Google Scholar 

  • Wells JD, Fuxa JR, Henderson G (1995) Virulence of four fungal pathogens to Coptotermes formosanus (Isoptera: Rhinotermitidae). J Entomol Sci 30:208–215

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wright SW, Raina AK, Lax AR (2005) Strain of the fungus Metarhizium anisopliae for controlling subterranean termites. J Econ Entomol 98(5):1451–1458

    PubMed  Google Scholar 

  • Yanagawa A, Shimizu S (2005) Defense strategy of the termite, Coptotermes foumosanus Shiraki to entomopathogenic fungi. JpnJ Environ Entomol Zool 16:17–22

    Google Scholar 

  • Yanagawa A, Shimizu S (2007) Resistance of the termite, Coptotermes formosanus Shiraki to Metarhizium anisopliae due to grooming. BioControl 52:75–85

    Google Scholar 

  • Zoberi MH (1995) Metarhizium anisopliae, a fungal pathogen of Reticultermes flavipes (Isoptera: Rhinotermitidae). Mycologia 87:354–359

    Google Scholar 

  • Zoberi MH, Grace JK (1990) Isolation of the pathogen Beauveria bassiana from Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 16:289–296

    Google Scholar 

Download references

Acknowledgements

The authors appreciate from Ferdowsi University of Mashhad (FUM) for financial support of MSc thesis of first author under supervision of JK (P3/48588).

Author information

Authors and Affiliations

  1. Department of Plant Protection, School of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Haydar Al-Farhani, Reyhaneh Darsouei, Shokoofeh Kamali, Gholamhossein Moravvej & Javad Karimi

Authors
  1. Haydar Al-Farhani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reyhaneh Darsouei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shokoofeh Kamali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gholamhossein Moravvej
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Javad Karimi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javad Karimi.

Ethics declarations

Conflict of interest

The authors confirm they don’t have any conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Farhani, H., Darsouei, R., Kamali, S. et al. Pathogenicity of native isolates of entomopathogenic fungi Beauveria and Metharizium genera on Microcerotermes diversus (Blattodea: Termitidae) in the laboratory. Int J Trop Insect Sci 41, 1493–1503 (2021). https://doi.org/10.1007/s42690-020-00347-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-020-00347-w

Keywords

Search

Navigation