Evaluation of the Entomopathogenic Fungus Beauveria bassiana on Different Stages of Phlebotomus papatasi (Diptera: Psychodidae), Vector of Zoonotic Cutaneous Leishmaniasis in Iran
Abstract
Background: Zoonotic cutaneous leishmaniasis is a major public health problem in Iran with the main vector of Phlebotomus papatasi. The use of entomopathogenic fungi for biological control of the vector is a potential substitute for the current methods which are being used. The purpose of the current study was to assess the virulence of two local isolates of Beauveria bassiana (OZ2 and TV) against Ph. papatasi.
Methods: To perform the bioassay test, fungal suspensions were applied for every stage of the sand fly life cycle. The mortality rate, longevity, and number of eggs laid were determined. Also, the probability of fungal survival on the surface of rodent’s body was assessed.
Results: The longevity of infected adult sand flies with both isolates of B. bassiana was significantly lower (P< 0.05) in comparison to the negative control. The estimated Lethal concentration 50 (LC50) values for adult female and male sand flies treated with OZ2 isolate were 1.4×106 and 2.2×107 conidia/ml, respectively, while they were 6.8×106 and 2.3×108 conidia/ml for TV isolate, respectively. Both isolates of B. bassiana exhibited nonsignificant mortality rates in sand fly larvae and pupae and fecundity rate (P> 0.05). According to our findings for both isolates, the fungus continued to spread throughout the surface of the rodent's body for 144 hours after spraying.
Conclusion: The current study demonstrated that both isolates of B. bassiana have considerable biological control capacity against adult sand flies.
2. World Health Organization (2023) Availa-ble at: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis, updated 12 January 2023.
3. Yaghoobi-Ershadi M (2012) Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their role on Leishmania transmis-sion. J Arthropod Borne Dis. 6(1): 1–17.
4. Yaghoobi-Ershadi MR, Akhavan AA, Mohe¬bali M (1996) Meriones libycus and Rhom¬bomys opimus (Rodentia: Gerbillidae) are the main reservoir hosts in a new focus of zoonotic cutaneous leishmaniasis in Iran. Trans R Soc Trop Med Hyg. 90(5): 503–504.
5. Nadim A, Tahvildari Bidruni G (1977) Ep-idemiology of cutaneous leishmaniasis in Iran: B. Khorassan. Part VI: Cutane¬ous leishmaniasis in Neishabur, Iran. Bull Soc Pathol Exot Filiales. 70(2): 171–177.
6. Jafari R, Abdoli H, Arandian MH, Shareghi N, Ghanei M, Jalali-Zand N, Nekoeian S, Veysi A, Montazeri A, Ghasemi A, Ram¬azanpour J, Fadaei R, Akhavan AA (2020) Emerging of cuta-neous leishmaniais due to Leishmania major in a new focus in Es¬fahan Prov-ince, Central Iran. J Arthropod Borne Dis. 14(2): 134–143.
7. Yaghoobi-Ershadi MR, Javadian E, Tah¬vil-dare-Bidruni GH (1995) Leishmania ma¬jor MON-26 isolated from naturally in¬fected Phlebotomus papatasi (Diptera: Psy¬chodidae) in Isfahan Province, Iran. Acta Trop. 59(4): 279–282.
8. Maleki-Ravasan N, Oshaghi MA, Afshar D, Arandian MH, Hajikhani S, Akhavan AA, Yakhchali B, Shirazi MH, Rassi Y, Jafari R, Aminian K, Fazeli-Varzaneh RA, Dur¬vasula R (2015) Aerobic bacte-rial flo¬ra of biotic and abiotic compart-ments of a hy¬perendemic Zoonotic Cu-taneous Leish¬man¬iasis (ZCL) focus. Parasit Vectors. 8: 63.
9. Nezamzadeh-Ezhiyeh H, Mirhendi H, Jafa¬ri R, Veysi A, Rassi Y, Oshaghi MA, Aran¬dian MH, Abdoli H, Bahrami S, Zahraei Ramazani AR, Fadaei R, Rama-zanpoor J, Farsi M, Aminian K, Saeidi Z, Yaghoobi-Ershadi MR, Akhavan AA (2021) An Eco-Epidemiological Study on Zoonotic Cutaneous Leishmaniasis in Central Iran. Iran J Public Health. 50(2): 350–359.
10. Killick-Kendrick R (1999) The biology and control of phlebotomine sand flies. Clin Dermatol. 17(3): 279–289.
11. Alexander B (2000) Sampling methods for phlebotomine sandflies. Med Vet Ento-mol. 14(2): 109–122.
12. El-Sadawy HA, Ramadan MY, Abdel Me¬geed KN, Ali HH, El Sattar SA, Elaka¬bawy LM (2020) Biological con-trol of Phlebotomus papatasi larvae by using en¬tomopathogenic nematodes and its sym¬biotic bacterial toxins. Trop Bi-omed. 37 (2): 288–302.
13. Rassi Y, Asadollahi H, Abai MR, Kayedi MH, Vatandoost H (2020) Efficiency of two capture methods providing live sand flies and assessment the susceptibility sta¬tus of Phlebotomus papa¬tasi (Diptera: Psy¬chodidae) in the foci of cutaneous leish¬maniasis, Lorestan Prov¬ince, Western Iran. J Arthropod Borne Dis. 14(4): 408–415.
14. Wilson C, Tisdell C (2001) Why farmers continue to use pesticides despite envi-ronmental, health and sustainability costs. Ecol Econ. 39(3): 449–462.
15. Angel-Sahagún CA, Lezama-Gutiérrez R, Molina-Ochoa J, Galindo-Velasco E, López-Edwards M, Rebolledo-Domínguez O, Cruz-Vázquez C, Reyes-Velázquez WP, Skoda SR, Foster JE (2005) Susceptibil¬ity of biological stag¬es of the horn fly, Haematobia irritans, to entomopathogen¬ic fungi (Hyphomy-cetes). J Insect Sci. 5: 50.
16. Lacey LA, Frutos R, Kaya H, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Con¬trol. 21(3): 230–248.
17. Ngure PK, Kasili S, Anjili CO, Karanja RM, Kaburi J, Mwangi M, Kinuthia G, Kiarie M, Nzau A, Kepha S, Maniania NK (2015) Effects of Metarhizium an-isopliae on sand fly populations in their natural habitats in Marigat sub-County, Baringo County, Kenya. Afr J Health Sci. 29: 398–407.
18. Ghassemi M, Akhavan AA, Zahraei-Ram-azani A, Yakhchali B, Arandian MH, Jafa¬ri R, Akhlaghi M, Shirani-Bidabadi L, Azam K, Koosha M, Oshaghi MA (2023) Rodents as vehicle for delivery of trans¬genic bacteria to make paratransgenic sand fly vectors of cutaneous leishmaniasis in field condi-tion. Sci Rep. 13(1): 14912.
19. Rajula J, Rahman A, Krutmuang P (2020) Entomopathogenic fungi in Southeast Asia and Africa and their possible adop-tion in biological control. Biol Control. 151: 104399.
20. Araújo JP, Hughes DP (2016) Diversity of entomopathogenic fungi: which groups conquered the insect body? Adv Genet. 94: 1–39.
21. Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beau-veria bassiana and Beauveria brongniartii. Bi¬ocontrol Sci Technol. 17(6): 553–596.
22. Kaufman PE, Reasor C, Rutz DA, Ketzis JK, Arends JJ (2005) Evaluation of Beau¬veria bassiana applications against adult house fly, Musca domestica, in com¬mer¬cial caged-layer poultry facilities in New York state. Biol Control. 33(3): 360–367.
23. Amóra SS, Bevilaqua CM, Feijó FM, Pe-reira RH, Alves ND, Freire FA, Kami-mura MT, de Oliveira DM, Luna-Alves Lima EA, Rocha MF (2010) The effects of the fungus Metarhizium anisopliae var. acridum on different stages of Lutzomy¬ia longipalpis (Diptera: Psychodidae). Ac¬ta Trop. 113(3): 214–220.
24. Reithinger R, Davies CR, Cadena H, Al-exander B (1997) Evaluation of the fun-gus Beauveria bassiana as a potential bi-ological control agent against phlebotom¬ine sand flies in Colombian coffee plan¬tations. J Invertebr Pathol. 70(2): 131–135.
25. Warburg A (1991) Entomopathogens of phlebotom¬ine sand flies: laboratory ex-per¬iments and natural infections. J Inver-tebr Pathol. 58(2): 189–202.
26. Seyedi RM, Nadim A (1992) The genus Phlebotomus (Diptera: Psychodidsae) of the countries of the Eastern Medi¬terra-ne¬an region. Iran J Public Health. 21: 11–50.
27. Theodor O, Mesghali A (1964) On the phlebotom¬inae of Iran. J Med Entomol. 1(3): 285–300.
28. Killick-Kendrick M, Killick-Kendrick R (1991) The initial establishment of sand¬-fly colonies. Parassitologia. 33: 315–320.
29. Modi GB, Tesh RB (1983) A simple tech-nique for mass rearing Lutzomyia long¬i-palpis and Phlebotomus papatasi (Dip-tera: Psychodidae) in the laboratory. J Med Entomol. 20(5): 568–569.
30. Seyed-talebi FS, Safavi SA, Talaei-Has-sanloui R, Bandani A (2020) Variable in¬duction of cuticle-degrading enzymes of Beauveria bassiana isolates in the pres¬ence of different insect cuticles. J Crop Protect. 9(4): 563–576.
31. Lacey LA (2012) (Ed.): Manual of tech-niques in invertebrate pathology. Aca-dem¬ic Press.
32. Forlani L, Pedrini N, Girotti JR, Mijailov-sky SJ, Cardozo RM, Gentile AG, Her-nández-Suárez CM, Rabinovich JE, Juá-rez MP (2015) Biological control of the Chagas disease vector Triatoma in-festans with the entomopathogenic fungus Beau¬veria bassiana combined with an aggre¬gation cue: field, laboratory and mathe¬matical modeling assessment. PLoS Negl Trop Dis. 9(5): e0003778.
33. Bukhari T, Takken W, Koenraadt CJ (2011) Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Par¬asit Vectors. 4: 1–14.
34. Evans HC, Elliot SL, Barreto RW (2018) Entomopathogenic fungi and their po-ten¬tial for the management of Aedes ae-gypti (Diptera: Culicidae) in the Americas. Mem Inst Oswaldo Cruz. 113: 206–214.
35. Golzan SR, Talaei-Hassanloui R, Homayoon¬zadeh M, Safavi SA (2023) Role of cuticle-degrading enzymes of Beau¬veria bassiana and Metarhizium an-isopliae in virulence on Plodia inter¬punc-tella (Lepidoptera, Pyralidae) larvae. J Asia Pac Entomol. 26(2): 102038.
36. Torkaman Z, Talaei-Hassanloui R, Khorramnejad A, Pashaei MR (2023) Ef¬fects of endophytism by Beauveria bas¬si¬ana (Cordycipitaceae) on plant growth, Fusarium (Nectriaceae) disease, and Sunn pest Eurygaster integriceps (Hemiptera: Scutelleridae) in wheat (Poaceae). Can En¬tomol. 155: e12.
37. Ngumbi PM, Irungu LW, Ndegwa PN, Ma¬niania NK (2011) Pathogenicity of Me¬tarhizium anisopliae (Metch) Sorok and Beauveria bassiana (Bals) Vuill to adult Phlebotomus duboscqi (Neveu-Lemaire) in the laboratory. J Vector Borne Dis. 48 (1): 37– 40.
38. Amóra SSA, Bevilaqua CML, Feijó FMC, Silva MA, Pereira RHMA, Silva SC, Alves ND, Freire FAM, Oliveira DM (2009) Evaluation of the fungus Beau-veria bassiana (Deuteromycotina: Hyphomy¬cetes), a potential biological control agent of Lutzomyia longipalpis (Diptera, Psy¬cho¬didae). Biol Control. 50(3): 329–335.
39. Farooq M, Freed S (2016) Infectivity of housefly, Musca domestica (Diptera: Mus¬cidae) to different entomopathogenic fungi. Braz J Microbiol. 47(4): 807–816.
40. Darbro JM, Johnson PH, Thomas MB, Ritch¬ie SA, Kay BH, Ryan PA (2012) Effects of Beauveria bassiana on sur-vival, blood-feeding success, and fecun-dity of Aedes aegypti in laboratory and semi-field conditions. Am J Trop Med Hyg. 86(4): 656–664.
41. Lee JY, Woo RM, Choi CJ, Shin TY, Gwak WS, Woo SD (2019) Beauveria bassi¬ana for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults shows high conidia persistence and productivity. AMB Express. 9(1): 206.
42. Scholte EJ, Takken W, Knols BG (2007) Infection of adult Aedes aegypti and Ae. albopictus mosquitoes with the ento-mopath¬ogenic fungus Metarhizium an-isopliae. Acta Trop. 102(3): 151–158.
43. Rocha LF, Rodrigues J, Martinez JM, Pe-reira TC, Neto JR, Montalva C, Humber RA, Luz C (2022) Occurrence of ento-mopathogenic hypocrealean fungi in mos¬quitoes and their larval habitats in Cen¬tral Brazil, and activity against Aedes aegypti. J Invertebr Pathol. 194: 107803.
44. Ramayanti I, Herlinda S, Muslim A, Hasyim H (2023) Entomopathogenic fungi from South Sumatra (Indonesia) patho¬genic¬ity to egg, larvae, and adult of Aedes ae¬gypti. HAYATI J. Biosci. 30(1): 35–47.
45. Cisneros-Vázquez LA, Navarro RPP, Rodríguez AD, Ordóñez-González JG, Valdez-Delgado KM, Danis-Lozano R, Vázquez-Martínez G (2023) Ento-mopath¬ogenic fungi for the control of larvae and adults of Aedes aegypti (Diptera: Cu¬licidae) vector of Dengue, Chikungunya and Zika viruses in Mexico. Salud Pub¬lica Mex. 65: 144–150.
46. Lecuona RE, Turica M, Tarocco F, Cre¬spo DC (2005) Microbial control of Mus¬ca domestica (Diptera: Muscidae) with selected isolates of Beauveria bassiana. J Med Entomol. 42(3): 332–336.
47. Geden CJ (2012) Status of biopesticides for control of house flies. J Biopest. 5: 1–11.
48. Zayed A, Soliman MM, El-Shazly MM (2013) Infectivity of Metarhizium an-isopli¬ae (Hypocreales: Clavicipitaceae) to Phleboto¬mus papatasi (Diptera: Psy-cho¬didae) under laboratory conditions. J Med Entomol. 50(4): 796–803.
49. Fitzwater WD, Prakash I (1969) Obser¬va-tions on the burrows, behavior and home range of the Indian desert gerbil, Mer-iones hurrianae Jerdon. Mamm. 33(4): 598–606.
50. Ogden G, Melby P (2009) Leishmania. In: Schaechter M (Eds): Encyclopedia of Mi¬crobiology. Elsevier, Ames¬terdam, pp. 663–673.
51. Wu S, Toews MD, Oliveira-Hofman C, Behle RW, Simmons AM, Shapiro-Ilan DI (2020) Environmental tolerance of en¬tomopathogenic fungi: A new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fun¬gal strains. Insects. 11(10): 711.
52. Deng SQ, Zou WH, Li DL, Chen JT, Huang Q, Zhou LJ, Tian XX, Chen YJ, Peng HJ (2019) Expression of Bacillus thu¬rin¬giensis toxin Cyt2Ba in the ento-mopath¬ogenic fungus Beauveria bassiana in¬creases its virulence towards Aedes mos¬quitoes. PLoS Negl Trop Dis. 13(7): 75–90.
Files | ||
Issue | Vol 17 No 3 (2023) | |
Section | Original Article | |
DOI | https://doi.org/10.18502/jad.v17i3.14986 | |
Keywords | ||
Biological control Beauveria bassiana Sand fly Rhombomys opimus Burrow |
Rights and permissions | |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |