Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T14:04:29.092Z Has data issue: false hasContentIssue false
  • English
  • Français

Biological responses of Tetranychus urticae (Acari: Tetranychidae) to sub-lethal concentrations of the entomopathogenic fungus Beauveria bassiana

Published online by Cambridge University Press:  25 August 2021

Katayoon Kheradmand Open the ORCID record for Katayoon Kheradmand [Opens in a new window] ,
Mahmoud Heidari ,
Amin Sedaratian-Jahromi ,
Reza Talaei-Hassanloui  and
Mohammadreza Havasi
Katayoon Kheradmand*
Affiliation:
Department of Entomology and Plant Pathology, College of Aburaihan, University of Tehran, Tehran, Iran
Mahmoud Heidari
Affiliation:
Department of Entomology and Plant Pathology, College of Aburaihan, University of Tehran, Tehran, Iran
Amin Sedaratian-Jahromi
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Yasouj University, Yasouj, Iran
Reza Talaei-Hassanloui
Affiliation:
Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran
Mohammadreza Havasi
Affiliation:
Department of Plant Protection, Faculty of Agriculture, University of Tehran, Karaj, Iran
*
Author for correspondence: Katayoon Kheradmand, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Tetranychus urticae (Acari: Tetranychidae) is one of the most important pests of agricultural crops with worldwide distribution causing considerable damage to different products. Application of chemical acaricides is one of the most important strategies used for the control of this pest. Entomopathogenic fungi, however, have been proposed as alternative control agents. In this study, sub-lethal effects (LC10 = 6.76 × 102, LC20 = 8.74 × 103, and LC30 = 55.38 × 103 conidia ml−1) of Beauveria bassiana strain TV on the life table parameters of T. urticae were evaluated under laboratory conditions. The results demonstrated that by increasing the concentration, a significant decline was observed in adult longevity of both male and female individuals. Total fecundity of T. urticae was calculated as 45.16, 36.28, 23.98, and 18.21 eggs in control, LC10, LC20, and LC30 treatments, respectively. Sub-lethal concentrations drastically affected the population parameters of this mite pest. The intrinsic rate of increase (r) ranged from 0.1983 to 0.1688 day−1 for the mites treated with distilled water and LC20 treatments, respectively. The net reproductive rate (R0) was affected by the sub-lethal concentrations (lower value at LC30 concentration: 11.19 offspring/individual). Considering the detrimental effects of B. bassiana on some biological parameters of T. urticae, it can be concluded that this product can be used to develop targeted interventions aimed at integrated pest management of this pest.

Keywords

Biological controlentomopathogenic fungipopulation parametersspider mites
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 1 , February 2022 , pp. 70 - 77
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abou El-Ela, AA (2014) Efficacy of five acaricides against the two-spotted spider mite Tetranychus urticae Koch and their side effects on some natural enemies. The Journal of Basic & Applied Zoology 67, 13–18.CrossRefGoogle Scholar
Afifi, AAM, Mabrouk, AM and Asran, AA (2010) Effect of the entomopathogenic fungus Beauveria bassiana on three acarine pests. In Sabelis M and Bruin J (eds), Trends in Acarology. Dordrecht: Springer, pp. 439–440.CrossRefGoogle Scholar
Antonio, TM, Batista, AS and Janeiro, NP (1999) Patogenicidade De Beauveria bassiana (Bals.) Vuill. AO ÁCARO Tetranychus urticae Koch. Scientia Agricola 56, 285–288.Google Scholar
Arthurs, S and Thomas, MB (2000) Effects of a Mycoinsecticide on feeding and fecundity of the Brown locust Locustana pardalina. Biocontrol Science and Technology 10, 321329.CrossRefGoogle Scholar
Azadi-Qoort, A, Sedaratian-Jahromi, A, Haghani, M and Ghane-Jahromi, M (2019) Biological responses of Tetranychus urticae (Acari: Tetranychidae) to different host plants: an investigation on bottom-up effects. Systematic & Applied Acarology 24, 659–674.CrossRefGoogle Scholar
Baverstock, J, Roy, HE, Clark, SJ, Alderson, PG and Pell, JK (2006) Effect of fungal infection on the reproductive potential of aphids and their progeny. Journal of invertebrate pathology 91, 136–139.CrossRefGoogle ScholarPubMed
Biondi, A, Zappala, L, Stark, JD and Desneux, N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8, 1–11.CrossRefGoogle ScholarPubMed
Blanford, S and Thomas, MB (2001) Adult survival, maturation, and reproduction of the desert locust Schistocerca gregaria infected with the fungus Metarhizium anisopliae var acridum. Journal of Invertebrate Pathology 78, 1–8.CrossRefGoogle ScholarPubMed
Blay, S and Yuval, B (1999) Oviposition and fertility in the Mediterranean fruit fly (Diptera: Tephritidae): effects of male and female body size and the availability of sperm. Annals of Entomological Society of America 89, 486–492.Google Scholar
Campbell, RJ, Mobley, KN and Marini, RP (1990) Growing conditions influence mite damage on apple and peach leaves. HortScience 25, 445–448.CrossRefGoogle Scholar
Chandler, D, Davidson, G, Pell, JG, Ball, BV, Shaw, K and Sunderland, KD (2000) Fungal biocontrol of Acari. Biocontrol Science and Technology 10, 357–384.CrossRefGoogle Scholar
Chen, Q, Liang, X, Wu, C, Gao, J, Chen, Q and Zhang, Z (2019) Density threshold-based acaricide application for the two-spotted spider mite Tetranychus urticae on cassava: from laboratory to the field. Pest Management Science 75, 2634–2641.CrossRefGoogle ScholarPubMed
Chi, H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology 17, 26–34.CrossRefGoogle Scholar
Chi, H (2019) Twosex-Mschart: A Computer Program for the Agestage, Two-sex Life Table Analysis. Taichung: National Chung Hsing University. http://140.120197.Google Scholar
Chi, H and Liu, H (1985) Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology Academia Sinica 24, 225–240.Google Scholar
Cira, TM, Burkness, EC, Koch, RL and Hutchison, WD (2017) Halyomorpha halys mortality and sublethal feeding effects following insecticide exposure. Journal of Pest Science 90, 1257–1268.CrossRefGoogle Scholar
Croft, BA (1990) Arthropod Biological Control Agents and Pesticides. New York: John Wiley.Google Scholar
Efron, B and Tibshirani, RJ (1993) Permutation tests. In An Introduction to the Bootstrap. New York, NY: Chapman & Hall, Inc., pp. 202–219.CrossRefGoogle Scholar
Fazeli-Dinan, M, Talaei-Hassanloui, R and Goettel, M (2016) Virulence of the entomopathogenic fungus Lecanicillium longisporum against the greenhouse whitefly, Trialeurodes vaporariorum and its parasitoid Encarsia formosa. International Journal of Pest Management 62, 251–260.CrossRefGoogle Scholar
Gatarayiha, MC, Laing, MD and Miller, RM (2010) Effects of adjuvant and conidial concentration on the efficacy of Beauveria bassiana for the control of the two spotted spider mite, Tetranychus urticae. Experimental and Applied Acarology 50, 217–229.CrossRefGoogle ScholarPubMed
Geroh, M, Gulati, R and Tehri, K (2015) Determination of lethal concentration and lethal time of entomopathogen Beauveria bassiana (Balsamo) Vuillemin against Tetranychus urticae Koch. International Journal of Agriculture Science 7, 523–528.Google Scholar
Ghaffari, S, Karimi, J, Kamali, S and Moghadam, EM (2017) Biocontrol of Planococcus citri (Hemiptera: Pseudococcidae) by Lecanicillium longisporum and Lecanicillium lecanii under laboratory and greenhouse conditions. Journal of Asia-Pacific Entomology 20, 605–612.CrossRefGoogle Scholar
Goettel, MS and Inglis, GD (1997) Fungi: hyphomycetes. In Lacey, LA (ed.), Manual of Techniques in Insect Pathology. San Diego: Academic Press, pp. 213–251.CrossRefGoogle Scholar
He, Y, Zhao, J, Zheng, Y, Weng, Q, Biondi, A, Desneux, N and Wu, K (2013) Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. International Journal of Biological Sciences 9, 246–255.CrossRefGoogle ScholarPubMed
Hornbostel, VL, Ostfeld, RS, Zhioua, E and Benjamin, MA (2004) Sublethal effects of Metarhizium anisopliae (Deuteromycetes) on engorged larval, nymphal, and adult Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology 41, 922–929.CrossRefGoogle Scholar
Huang, YB and Chi, H (2012) Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett)(Diptera: Tephritidae). Journal of Agriculture and Food Research 61, 37–45.Google Scholar
Huang, Z, Ali, S, Ren, SX and Wu, JH (2010) Effect of Isaria fumosoroseus on mortality and fecundity of Bemisia tabaci and Plutella xylostella. Insect Science 17, 140–148.CrossRefGoogle Scholar
Inglis, GD, Goettel, MS, Butt, TM and Strasser, H (2001) Use of hyphomycetous fungi for managing insect pests. In Fungi as Biocontrol Agents: Progress Problems and Potential, Wallingford, UK: CABI, pp. 23–69.Google Scholar
Irigaray, FJSC, Marco-Mancebon, V and Perez-Moreno, I (2003) The entomopathogenic fungus Beauveria bassiana and its compatibility with triflumuron: effects on the two-spotted spider mite Tetranychus urticae. Biological Control 26, 168–173.CrossRefGoogle Scholar
Kaplan, P, Yorulmaz, S and Ay, R (2012) Toxicity of insecticides and acaricides to the predatory mite Neoseiulus californicus (McGregor)(Acari: Phytoseiidae). International Journal of Acarology 38, 699–705.CrossRefGoogle Scholar
Khanamani, M, Fathipour, Y and Hajiqanbar, H (2013) Population growth response of Tetranychus urticae to eggplant quality: application of female age-specific and age-stage, two-sex life tables. International Journal of Acarology 39, 638–648.CrossRefGoogle Scholar
Latifian, M, Soleimannejadian, E, Ghazavi, M, Mosadegh, MS and Hayati, J (2010) Effects of sublethal concentrations of fungus Beauveria bassiana on the reproductive potentials of sawtoothed beetle Oryzaephilus surinamensis on commercial date cultivars. Plant Protection Journal 2, 277–290.Google Scholar
Liu, JF, Zhang, ZQ, Beggs, JR, Paderes, E, Zou, X and Wei, XY (2019) Lethal and sublethal effects of entomopathogenic fungi on tomato/potato psyllid, Bactericera cockerelli (Šulc) (Hemiptera: Triozidae) in capsicum. Crop Protection 129, 105023.CrossRefGoogle Scholar
Maina, UM, Galadima, IB, Gambo, FM and Zakaria, D (2018) A review on the use of entomopathogenic fungi in the management of insect pests of field crops. Journal of Entomology and Zoology Studies 6, 27–32.Google Scholar
Maleknia, B, Fathipour, Y and Soufbaf, M (2016) How greenhouse cucumber cultivars affect population growth and two-sex life table parameters of Tetranychus urticae (Acari: Tetranychidae). International Journal of Acarology 42, 70–78.CrossRefGoogle Scholar
Maniania, N, Bugeme, D, Wekesa, V, Delalibera, I and Knapp, M (2008) Role of entomopathogenic fungi in the control of Tetranychus evansi and Tetranychus urticae (Acari: Tetranychidae), pests of horticultural crops. Experimental and Applied Acarology 46, 259–274.CrossRefGoogle Scholar
Meck, ED, Walgenbach, JF and Kennedy, GG (2012) Association of Tetranychus urticae (Acari: Tetranychidae) feeding and gold fleck damage on tomato fruit. Crop Protection 42, 24–29.CrossRefGoogle Scholar
Meck, ED, Kennedy, GG and Walgenbach, JF (2013) Effect of Tetranychus urticae (Acari: Tetranychidae) on yield, quality, and economics of tomato production. Crop Protection 52, 84–90.CrossRefGoogle Scholar
Migeon, A and Dorkeld, F (2006–2017) Spider mites web: a comprehensive database for the Tetranychidae. Available at http://www.montpellier.inra.fr/CBGP/spmweb (Accessed 20 June 2017).Google Scholar
Mollaloo, MG, Kheradmand, K, Sadeghi, R and Talebi, AA (2017) Demographic analysis of sublethal effects of spiromesifen on Neoseiulus californicus (Acari: Phytoseiidae). Acarologia 57, 571–580.CrossRefGoogle Scholar
Nawaz, M, Cai, W, Jing, Z, Zhou, X, Mabubu, JI and Hua, H (2017) Toxicity and sublethal effects of chlorantraniliprole on the development and fecundity of a non-specific predator, the multicolored Asian lady beetle, Harmonia axyridis (Pallas). Chemosphere 178, 496–503.CrossRefGoogle Scholar
Park, YL and Lee, JH (2002) Leaf cell and tissue damage of cucumber caused by twospotted spider mite (Acari: Tetranychidae). Journal of Economic Entomology 95, 952–957.CrossRefGoogle Scholar
Posada, F, Aime, MC, Peterson, SW, Rehner, SA and Vega, FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycological research 111, 748–757.CrossRefGoogle Scholar
Quesada-Moraga, E, Santos-Quiros, R, Valverde-Garcia, P and Santiago-Alvarez, C (2004) Virulence, horizontal transmission, and sublethal reproductive effects of Metarhizium anisopliae (Anamorphic fungi) on the German cockroach (Blattodea: Blattellidae). Journal of Invertebrate Pathology 87, 51–58.CrossRefGoogle Scholar
Rashki, M and Shirvani, A (2013) The effect of entomopathogenic fungus, Beauveria bassiana on life table parameters and behavioural response of Aphis gossypii. Bulletin of Insectology 66, 85–91.Google Scholar
Sedaratian, A, Fathipour, Y and Moharramipour, S (2009) Evaluation of resistance in 14 soybean genotypes to Tetranychus urticae (Acari: Tetranychidae). Journal of Pest Science 82, 163–170.CrossRefGoogle Scholar
Sedaratian, A, Fathipour, Y and Moharramipour, S (2011) Comparative life table analysis of Tetranychus urticae (Acari: Tetranychidae) on 14 soybean genotypes. Insect Science 18, 541–553.CrossRefGoogle Scholar
Sedaratian, A, Fathipour, Y, Talaei-Hassanloui, R and Jurat-Fuentes, JL (2013) Fitness costs of sublethal exposure to Bacillus thuringiensis in Helicoverpa armigera: a carryover study on offspring. Journal of Applied Entomology 137, 540–549.CrossRefGoogle Scholar
Sedaratian, A, Fathipour, Y and Talaei-Hassanloui, R (2014) Deleterious effects of Bacillus thuringiensis on biological parameters of Habrobracon hebetor parasitizing Helicoverpa armigera. BioControl 59, 89–98.CrossRefGoogle Scholar
Seiedy, M, Saboori, A, Allahyari, H, Talaei-Hassanloui, R and Tork, M (2010) Laboratory investigation on the virulence of two isolates of the entomopathogenic fungus Beauveria bassiana against the two spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). International Journal of Acarology 36, 527–532.CrossRefGoogle Scholar
Seyed-Talebi, FS, Kheradmand, K, Talaei-Hassanloui, R and TalebiJahromi, K (2012) Sublethal effects of Beauveria bassiana on life table parameters of two-spotted spider mite, Tetranychus urticae (Acari:Tetranychidae). Biocontrol Science and Technology 22, 293–303.CrossRefGoogle Scholar
Seyed-Talebi, FS, Kheradmand, K, Talaei-Hassanloui, R and Talebi-Jahromi, K (2014) Synergistic effect of Beauveria bassiana and spirodiclofen on the two-spotted spider mite (Tetranychus urticae). Phytoparasitica 42, 405–412.CrossRefGoogle Scholar
Shahid, AA, Rao, QA, Bakhsh, A and Husnain, T (2012) Entomopathogenic fungi as biological controllers: new insights into their virulence and pathogenicity. Archives of Biological Sciences 64, 21–42.CrossRefGoogle Scholar
Shi, WB and Feng, MG (2009) Effect of fungal infection on reproductive potential and survival time of Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology 48, 229–237.CrossRefGoogle Scholar
Shi, WB, Jiang, Y and Feng, MG (2005) Compatibility of ten acaricides with Beauveria bassiana and enhancement of fungal infection to Tetranychus cinnabarinus (Acari: Tetranychidae) eggs by sublethal application rates of pyridaben. Applied Entomology and Zoology 40, 659–666.CrossRefGoogle Scholar
Song, Z, Zhang, B, Li, D and Zheng, Y (2013) Effects of abamectin on the survival and development of Neoseiulus fallacis (Garman). Chinese Journal of Biological Control 29, 349–353.Google Scholar
Stark, JD and Banks, JE (2003) Population level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology 48, 505–519.CrossRefGoogle ScholarPubMed
Sumikarsih, E, Herlinda, S and Pujiastuti, Y (2019) Conidial density and viability of Beauveria bassiana isolates from Java and Sumatra and their virulence against Nilaparvata lugens at different temperatures. AGRIVITA. Journal of Agricultural Science 41, 335–350.Google Scholar
Tomczyk, A and Kropczynska, D (1985) Effects on the host plant. In Helle, W and Sabelis, MW (eds), Spider Mites: Their Biology, Natural Enemies and Control. New York, NY: Elsevier Science Publisher, pp. 317–327.Google Scholar
Ullah, MS and Lim, UT (2017) Synergism of Beauveria bassiana and Phytoseiulus persimilis in control of Tetranychus urticae on bean plants. Systematic and Applied Acarology 22, 1924–1936.CrossRefGoogle Scholar
van Leeuwen, T, Vontas, J, Tsagkarakou, A, Dermauw, W and Tirry, L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important acari: a review. Insect Biochemistry and Molecular Biology 40, 563–572.CrossRefGoogle ScholarPubMed
Wei, M, Chi, H, Guo, Y, Li, X, Zhao, L and Ma, R (2020) Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. Journal of Economic Entomology 113, 2343–2353.CrossRefGoogle ScholarPubMed
Wekesa, VW, Knapp, M, Maniania, NK and Boga, HI (2006) Effects of Beauveria bassiana and Metarhizium anisopliae on mortality, fecundity and egg fertility of Tetranychus evansi. Journal of Applied Entomology 130, 155–159.CrossRefGoogle Scholar
Wekesa, VW, Hountondji, FCC and Dara, SK (2015) Mite pathogens and their use in biological control. In Carrillo, D, José de Moraes, G and Peña, JE (eds), Prospects for Biological Control of Plant Feeding Mites and Other Harmful Organisms, vol. 19. Cham: Springer International Publishing, pp. 309–328.CrossRefGoogle Scholar
Wu, S, Gao, Y, Zhang, Y, Wang, E, Xu, X and Lei, Z (2014) An entomopathogenic strain of Beauveria bassiana against Frankliniella occidentalis with no detrimental effect on the predatory mite Neoseiulus barkeri: evidence from laboratory bioassay and scanning electron microscopic observation. PLoS ONE 9, e84732.CrossRefGoogle ScholarPubMed
Wu, S, Xie, H, Li, M, Xu, X and Lei, Z (2016) Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Experimental and Applied Acarology 70, 421–435.CrossRefGoogle ScholarPubMed
Yang, X, Sun, L, Chi, H, Kang, G and Zheng, C (2020) Demography of Thrips palmi (Thysanoptera: Thripidae) reared on Brassica oleracea (Brassicales: Brassicaceae) and Phaseolus vulgaris (Fabales: Fabaceae) with discussion on the application of the bootstrap technique in life table research. Journal of Economic Entomology 113, 2390–2398.CrossRefGoogle ScholarPubMed
Yuan, HG, Wu, SY, Lei, ZR, Rondon, SI and Gao, YL (2018) Sub-lethal effects of Beauveria bassiana (Balsamo) on field populations of the potato tuberworm Phthorimaea operculella Zeller in China. Journal of Integrative Agriculture 17, 911–918.CrossRefGoogle Scholar
Zhang, T, Reitz, SR, Wang, H and Lei, Z (2015) Sublethal effects of Beauveria bassiana (Ascomycota: Hypocreales) on life table parameters of Frankliniella occidentalis (Thysanoptera: Thripidae). Journal of Economic Entomology 108, 975–985.CrossRefGoogle Scholar
Zhou, F, Ali, S and Huang, Z (2010) Influence of the entomopathogenic fungus Isaria fumosorosea on Axinoscymnus cardilobus (Coleoptera: Coccinellidae) under laboratory conditions. Biocontrol Science and Technology 20, 709–722.CrossRefGoogle Scholar