The effect of the pathogenic fungus, Beauveria bassiana, on the biological characteristics of the parasitoid wasp, Habrobracon hebetor

Document Type : Complete paper

Authors

Department of Plant Protection, College of Agriculture, Isfahan University of Technology, Isfahan, Iran

Abstract

Knowledge about natural enemy’s interactions in biological pest control programs in agricultural systems is important to increase their effectiveness. In this research, the effect of the pathogenic fungus, Beauveria bassiana (Hypocreales: Cordycipitaceae), on the fertility-life table parameters of the parasitoid wasp, Habrobracon hebetor (Say) (Hym.: Braconidae) was investigated. The experiment was conducted in a fully randomized design using 12 treatments in Twenty-five replications. The flour moth larvae were contaminated by four different conidia concentration (0, 103, 106, and 109 conidia/ml) of B. bassiana, then these larvae in three periods of 24, 48 and 72 hours after contamination were used as the host for female wasps. Based on results, larval and pupal periods of the wasps significantly increased under fungus application, so with increasing conidia concentration, larval and pupal periods increased from 2.94 and 6.36 days to 4.13 and 7.45 days, respectively. The adult longevity of female wasps decreased significantly from 18.97 days to 16.27 days by using B. bassiana. The intrinsic rate of population increase (r) and the finite rate of population increase (λ) of wasps showed a decrease with increasing the concentration of fungus and increasing time, while the mean generation time (T) increased from 16 days to 19 days by increasing conidia concentrations. Our results indicate that infection of host larvae with pathogenic fungus has a negative effect on the biological characteristics of parasitoid wasps and can reduce the efficiency of H. hebetor in pest control.

Keywords

Main Subjects

Extended Abstract

Introduction

Since the interspecific interactions among natural enemies released for the biological control of different pests of a crop can affect the success of controlling each pest, knowing the relationships between natural enemy species in an agricultural system is very important. The fungus, Beauveria bassiana, is one of the most well-known entomopathogenic fungus that has broad host range and the low cost mass production and currently is widely used for pest management in greenhouses and outdoor crops.  This fungus is used to control the tomato leaf miner, Tuta absoluta, in tomato cultivation. The ectoparasitoid wasp, Habrobracon hebetor plays an important role in controlling many native and invasive pests, especially Pyralidae and Noctuidae moths, in agricultural products due to its high search ability, suitable adaptation and wide host range. In Iran, its mass production is done on Ephestia kuehniella, and adult wasps are released to parasitize Helicoverpa armigera larvae in cotton and tomato fields. The aim of this study is to evaluate the possible effects of B. bassiana on the biological characteristics of H. hebetor wasps.

 

Materials and Methods

The fertility-life table parameters of H. hebetor wasps were studied on the E. kuehniella larvae that were treated with the B. bassiana suspensions in three different concentrations (103, 106 and 109 conidia/ml). In order to determine the effect of the duration of host infection with the fungus before parasitization on the fitness parameters of the H. hebetor, treated larvae at three times; one day, two days, and three days after the treatment with the fungus, were exposed to wasps. The experiment was carried out in laboratory conditions in an incubator at 25 ± 1°C, 65 ± 5% relative humidity, and 16L:8D photoperiod. Length of different life stages, number of eggs per female and population parameters including the net reproductive rate (R0), the gross reproductive rate (GRR), the intrinsic rate of population increase (r), the finite rate of population increase (λ), the age-specific survival rate (lX), the age-specific fecundity (mX), and the mean generation time (T) were calculated by checking daily.

 

Results and Discussion

Our results showed that the embryonic period of wasps is not affected by the host infection with fungus, but the larval and pupal periods were significantly different in different treatments. Our results showed that the embryonic period of bees is not affected by the infection of the host with fungi, but the larval and pupal periods were significantly different in different treatments, so that with the increase of the infection time and the concentration of B. bassiana fungus, the length of the larval and pupal periods have increased. Also, the lifespan in female adult wasps that reared on infected host significantly decreased compared by others that reared on un-infected host. The amount of reduction in the adult lifespan was in line with the increase in the concentration of the fungus and the host infection duration. The amount of eggs per female decreased significantly with the increase in the host infection time and the concentration of the fungus. The fertility life table parameters of the parasitoid, H. hebetor, were significantly affected by different concentrations of B. bassiana in three different host infection times, so that with the increase in the concentration of the fungus and host infection time, amount of the intrinsic rate of population increase and the finite rate of population increase were decreased.

In conclusion, considering the negative effects of B. bassiana on the performance of H. hebetor, the time of using the entomopathogenic fungus and the release of parasitoid wasps should be chosen very carefully in order to minimize these negative effects in their combined application in biological control programs.

References

عسکری، حسن و عجم­حسنی، مریم (1387). بررسی تاثیر قارچ Lecanicillim longisporum (Deut.: Moniliales) روی طول عمر، باروری و رفتار جفت­گیری زنبور پارازیتوئید. آفات و بیماری­های گیاهی، 76(2)، 15-31.
REFERENCES
Aiuchi, D., Saito, Y., Tone, J., Kanazawa, M., Tani, M., & Koike, M. (2012). The effect of entomopathogenic Lecanicillium spp. (Hypocreales: Cordycipitaceae) on the aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiinae). Applied Entomology and Zoology, 47, 351-357. https://doi.org/10.1007/s13355-012-0125-7
Askary, H., & Ajam-Hassani, M. (2008). Effect of Lecanicillim longisporum (Deut.: Moniliales) on longevity, fecundity and mating behavior of Aphidius nigripes (Hym.: Aphilinidae). Journal of Plant Pests and Disease, 76(2), 15-29. (In Persian).
Askary, H., & Brodeur, J. (1999). Susceptibility of larval stages of the aphid parasitoid Aphidius nigripesto the Entomopathogenic fungus Verticillium lecanii. Journal of Invertebrate Pathology, 73(1), 129-132. https://doi.org/10.1006/jipa.1998.4824
Chi, H. (2009). TWOSEX-MSChart: A computer program for the age-stage, two-sex life table analysis, http://140.120.197.173/Ecology//Download/Twosex-MSChart.zip.
Clifton, E. H., Hajek, A. E., Jenkins, N. E., Roush, R. T., Rost, J. P., & Biddinger, D. J. (2020). Applications of Beauveria bassiana (Hypocreales: Cordycipitaceae) to control populations of spotted lanternfly (Hemiptera: Fulgoridae), in semi-natural landscapes and on grapevines. Environmental Entomology, 49, 854–864. https://doi.org/10.1093/ee/nvaa064
Darwish, E., El-Shazly, M., & El-Sherif, H. (2003). The choice of probing sites by Bracon hebetor Say (Hymenoptera: Braconidae) foraging for Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Journal of Stored Products Research, 39(3), 265-276. https://doi.org/10.1016/S0022-474X(02)00023-1
Ezz, N. (2012). Entomopathogenic fungi associated with certain scale insects (Hemiptera: Coccoidea) in Egypt. Egyptian Academic Journal of Biological Sciences, 5(3), 211-221. https://dx.doi.org/10.21608/eajbsa.2012.14287
Fatiha, L., Huang, Z., Ren, S. X., & Ali, S. (2008). Effect of Verticillium lecanii on biological characteristics and life table of Serangium japonicum (Coleoptera: Coccinellidae), a predator of whiteflies under laboratory conditions. Insect Science. 15(4), 327-333. https://doi.org/10.1111/j.1744-7917.2008.00217.x
Fransen, J. J., & Van Lenteren, J. C. (1993). Host selection and survival of the parasitoid Encarsia formosa on greenhouse whitefly, Trialeurodes vaporariorum, in the presence of hosts infected with the fungus Aschersonia aleyrodis. Entomologia Experimentalis et Applicata, 69(3), 239-249. https://doi.org/10.1111/j.1570-7458.1993.tb01747.x
Gao, Y. P., Luo, M., Wang, X. Y., He, X. Z., Lu, W., & Zheng, X. L. (2022). Pathogenicity of Beauveria bassiana PfBb and immune responses of a non-target host, Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects, 13(10), 914. https://doi.org/10.3390/insects13100914
Hentz, M. G., Ellsworth, P. C., Naranjo, S. E., & Watson, T. F. (1998). Development, longevity, and fecundity of Chelonus sp. nr. curvimaculatus (Hymenoptera: Braconidae), an egg–larval parasitoid of pink bollworm (Lepidoptera: Gelechiidae). Environmental Entomology, 27(2), 443-449. https://doi.org/10.1093/ee/27.2.443
James, R. R., & Lighthart, B. (1994). Susceptibility of the convergent lady beetle (Coleoptera: Coccinellidae) to four entomogenous fungi. Environmental Entomology, 23(1), 190-192. https://doi.org/10.1093/ee/23.1.190
Jarrahi, A., & Safavi, S. A. (2016). Sublethal effects of Metarhizium anisopliae on life table parameters of Habrobracon hebetor parasitizing Helicoverpa armigera larvae at different time intervals. BioControl, 61, 167-175. https://doi.org/10.1007/s10526-015-9707-y
Lacey, L. A., Mesquita, A. L., Mercadier, G., Debire, R., Kazmer, D. J., & Leclant, F. (1997). Acute and sublethal activity of the entomopathogenic fungus Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) on adult Aphelinus asychis (Hymenoptera: Aphelinidae). Environmental Entomology, 26(6), 1452-1460. https://doi.org/10.1093/ee/26.6.1452
Letourneau, D. K., Jedlicka, J. A., Bothwell, S. G., & Moreno, C. R. (2009). Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics, 40, 573-592. https://doi.org/10.1146/annurev.ecolsys.110308.120320
Ma, X. M., Liu, X. X., Ning, X., Zhang, B., Han, F., Guan, X. M., Tan, Y. F., & Zhang, Q. W. (2008). Effects of Bacillus thuringiensis toxin Cry1Ac and Beauveria bassiana on asiatic corn borer (Lepidoptera: Crambidae). Journal of Invertebrate Pathology, 99, 123–128. https://doi.org/10.1016/j.jip.2008.06.014
Madurappulige, D. (2005). Effect of Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) on Diadegma semiclausum (Hellen) (Hym.: Ichneumonidae), a parasitoid of Plutella xylostella (Lep: Yponomeutidae). [M.Sc. Lincoln University], NewZealand.
Mesquita, A. L., & Lacey, L. A. (2001). Interactions among the entomopathogenic fungus, Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes), the parasitoid, Aphelinus asychis (Hymenoptera: Aphelinidae), and their aphid host. Biological Control, 22(1), 51-59. https://doi.org/10.1006/bcon.2001.0950
Mills, N. J. (1981). The mortality and fat content of Adalia bipunctata during hibernation. Entomologia Experimentalis et Applicata, 30(3), 265-268. https://doi.org/10.1111/j.1570-7458.1981.tb03109.x
Navaei, A. N., Taghizadeh, M., Javanmoghaddam, H., Oskoo, T., & Attaran, M. R. (2002). Efficiency of parasitoid wasps, Trichogramma pintoii and Habrobracon hebetor against Ostrinia nubilalis and Helicoverpa sp. on maize in Moghan. Proceedings of 15th Iranian Plant Protection Congress, Razi University of Kermanshah, Iran. (In Persian).
Powell, W., Wilding, N., Brobyn, P. J., & Clark, S. J. (1986). Interference between parasitoids [Hym.: Aphidiidae] and fungi [Entomophthorales] attacking cereal aphids. Entomophaga, 31, 293-302. https://doi.org/10.1007/BF02373339
Qazzaz, F. O., Al-Masri, M. I., & Barakat, R. M. (2015). Effectiveness of Beauveria bassiana native isolates in the biological control of the Med-iterranean fruit fly (Ceratitis capitata). Advances in Entomology, 3(02), 44. http://dx.doi.org/10.4236/ae.2015.32006
Rashki, M., Kharazi-Pakdel, A., Allahyari, H., & Van Alphen, J. J. M. (2009). Interactions among the entomopathogenic fungus, Beauveria bassiana (Ascomycota: Hypocreales), the parasitoid, Aphidius matricariae (Hymenoptera: Braconidae), and its host, Myzus persicae (Homoptera: Aphididae). Biological Control, 50(3), 324-328. https://doi.org/10.1016/j.biocontrol.2009.04.016
Roy, H. E., & Pell, J. K. (2000). Interactions between entomopathogenic fungi and other natural enemies: implications for biological control. Biocontrol Science and Technology, 10(6), 737-752. https://doi.org/10.1080/09583150020011708
Scopes, N. E. A. (1970). Control of Myzus persicae on year‐round chrysanthemums by introducing aphids parasitized by Aphidius matricariae into boxes of rooted cuttings. Annals of Applied Biology, 66(2), 323-327. https://doi.org/10.1111/j.1744-7348.1970.tb06439.x
Stiling, P., & Cornelissen, T. (2005). What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological control, 34(3), 236-246. https://doi.org/10.1016/j.biocontrol.2005.02.017
Straub, C. S., Finke, D. L., & Snyder, W. E. (2008). Are the conservation of natural enemy biodiversity and biological control compatible goals? Biological Control, 45(2), 225-237. https://doi.org/10.1016/j.biocontrol.2007.05.013
Tamayo-Mejía, F., Tamez-Guerra, P., Guzmán-Franco, A. W., & Gomez-Flores, R. (2016). Developmental stage affects survival of the ectoparasitoid Tamarixia triozae exposed to the fungus Beauveria bassiana. Biological Control, 93, 30-36. https://doi.org/10.1016/j.biocontrol.2015.11.006
Wang, H. H., Liu, S., Wang, S. Y., & Lei, Z. R. (2020). Research and development of wettable powder of Beauveria bassiana and its control and application to Frankliniella occidentalis.  Chinese Journal of Biological Control, 36, 858–861. (In Chinese).
Wekesa, V. W., Moraes, G. D., Knapp, M., & Delalibera, Jr. I. (2007). Interactions of two natural enemies of Tetranychus evansi, the fungal pathogen Neozygites floridana (Zygomycetes: Entomophthorales) and the predatory mite, Phytoseiulus longipes (Acari: Phytoseiidae). Biological Control, 41(3), 408-414. https://doi.org/10.1016/j.biocontrol.2007.03.003
Wraight, S. P., Carruthers, R., Bradley, C. A., Jaronski, S. T., Lacey, L. A., Wood, P., & Galaini-Wraight, S. (1998). Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silver leaf whitefly, Bemisia argentifolii. Journal of Invertebrate Pathology, 71(3), 217-226. https://doi.org/10.1006/jipa.1997.4734
Zemek, R., Konopická, J., Jozová, E., Skoková, H. O. (2021). Virulence of Beauveria bassiana strains isolated from cadavers of Colorado potato beetle, Leptinotarsa decemlineata. Insects, 12, 1077. https://doi.org/10.3390/insects12121077
BIOLOGICAL CONTROL OF PESTS AND PLANT DISEASES
Volume 11, Issue 1
June 2023
Pages 15-28

Files

Share

How to cite

Statistics