Abstract
Background
The geothermal greenhouses in Southern Tunisia are an important axis of agricultural development. This sector faces many abiotic and biotic constraints that could threat its sustainability. Thus, the heated greenhouses encounter destructive pests such as the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and the two-spotted spider mite Tetranychus urticae (Koch) (Acari: Tetranychidae).
Results
This study aimed to assess the effect of the entomopathogenic fungi (EPF) Beauveria bassiana (strain ATCC and strain R444) and Lecanicillium muscarium strain Ve6 on simultaneous existence of T. urticae and B. tabaci in the host plants. The EPF had a significant effect on eggs and larvae of B. tabaci and on eggs and mobile forms of T. urticae in particular. The use of B. bassiana ATCC, B. bassiana R444 and L. muscarium strains Ve6 showed significant efficacies against B. tabaci larvae and eggs compared to untreated control. Indeed, the reduction percent of B. tabaci eggs varied between 42.65 and 58.52%. Thus, the efficacy against the number of B. tabaci larvae was in order to 65.04, 60.26 and 55.52% of B. bassiana strain ATCC, B. bassiana strain R444 and L. muscarium strain Ve6, respectively. In addition, these EPF were very effective on T. urticae eggs with a percentage reduction greater than 92.86%, whereas the percentage reduction in the T. urticae mobile forms varied between 95.11 and 98.52%.
Conclusions
Use of EPF will be an imperative to develop directed interventions at the integrated management of these two pests in protected and geothermal crops.
Similar content being viewed by others
Background
The whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is an important agricultural and economic pest distributed worldwide. It can feed on more than 600 species of plants (De Barro et al. 2011). B. tabaci is a biting-sucking insect that causes the formation of small yellow spots on leaves or fruits and secretes honeydew which provides a medium for the growth of sooty mold, reducing photosynthesis activities (Solanki and Jha 2018). This pest is a vector for large categories of viruses (Jones 2003) most of which belong to the genus Begomovirus, in particular the virus TYLCV «Tomato Yellow Leaf Curl Virus» (Navas-Castillo et al. 2011). In Southern Tunisia, this whitefly species causes harmful damage to crops heated by geothermal waters (Bel Kadhi 2004).
The spider mite Tetranychus urticae (Koch) (Acari: Tetranychidae) is one of the most destructive pests, feeding on over 1100 plant species; including vegetable, fruit and ornamental crops (Bensoussan et al. 2018). T. urticae is a native to the temperate zone; it is frequently introduced into intensively cultivated regions in the tropics. Due to its fast growth rate and high reproductive potential, this mite can colonize crops quickly (Farazmand and Amir-Maafi 2018). T. urticae damages plants by feeding on the contents of leaf mesophyll cells using a stylet (Park and Lee 2002).
The excessive use of chemical pesticides has led to many problems for human health and the environment. In addition, the development of pest resistance and the destruction of non-target organisms was studied (Wang et al. 2018). B. tabaci has developed resistance to most of the insecticides used (Basit 2019). According to Wu et al. (2016), the widespread use of pesticides has reduced the number of natural enemies of the predatory mites of T. urticae (Nouran et al. 2021). In recent years, research has been developed to use biological control agents, particularly entomopathogenic fungi (EPF) as an ecological alternative to chemical control (Vega 2018). Different isolates of Lecanicillium muscarium and Beauveria bassiana were effective against sap-sucking insects (Hesketh et al. 2008), especially B. tabaci (Abdel-Raheem and Al-Keridis 2017). These EPF were developed as an alternative to synthetic miticides and can manage mite populations naturally (Maniania et al. 2008).
The aim of this study was to test the efficacy of commercial EPF B. bassiana (ATCC 74,040, R444) and L. muscarium Ve6 against two major pests of cucurbit crops, B. tabaci and T. urticae, which co-exist on the same host plants.
Methods
Cultures of Bemisia tabaci and Tetranychus urticae
Bemisia tabaci and T. urticae were collected from a greenhouse at the Technical Center for Protected Crops and Geothermal TCPCG in Gabes, Tunisia. Rearing was placed on Cucumis melon plants grown in 0.5 L/ pots. Plants were inoculated with these two pests from the stage of the 5–6 leaves.
Entomopathogenic fungi
Three commercial EPF-based biopesticides were tested: Naturalis® (B. bassiana strain ATCC 74,040 (2.3 × 109spores/ml)), Bb-Protec® WP (B. bassiana strain R444 (≥ 2 × 109 spores/gram), and Mycotal® WG (Lecanicillium muscarium strain Ve6 (19–79) (1010 spores/gram)). These EPF were cultured on Potato Dextrose Agar (PDA) medium and incubated at 25 ± 1 °C for 7 days to confirm their viability before being used (Nouran et al. 2021).
Experimental protocol
Efficacy study of EPF against B. tabaci and T. urticae was carried out on melon plants by comparing it with the chemical insecticide, Pegasus® containing the active substance Diafenthiuron (500 g/l) (approved against whitefly and dust mites with a dose of 60 ml/hl) as well as an untreated control. This experiment was conducted in a tunnel-type greenhouse, at an area of 500 m2, 45 days after pest infestation. Temperature and relative humidity inside the greenhouse were recorded using a portable data logger (Fig. 1).
The Randomized Complete Blocks Design (RCBD) was used for this experiment with five treatments and three replicates. Each experimental unit contains 12 melon plants infested with B. tabaci and T. urticae. The experimental units were treated with B. bassiana strain R 444 (1 g/1 l), B. bassiana strain ATCC (1 ml/1 l), L. muscarium strain Ve6 (1 g/1L), Diafenthiuron (60 ml/hl) and an untreated control. The treatments were applied using a portable sprayer with a volume of 1.5 L. Treatment was carried out on June 3, 2021.
Sampling
Fifteen leaves were sampled randomly from each treatment for examination using a Leica® EZ4E microscopy model to follow the development of B. tabaci and T. urticae. The different stages of development of B. tabaci and T. urticae were calculated for each sample. In order to evaluate the efficacy of this EPF, the rate of reduction for developmental stages of B. tabaci and T. urticae in melon leaves was calculated according to the formula (Henderson and Tilton 1955), where
Statistical analysis
For the analysis of variance (ANOVA), the number of eggs, larvae of B. tabaci and the number of eggs, mobile forms of T. urticae as well as the rate of reduction after treatments were subjected to a unidirectional analysis associated with a Duncan test (P < 0.05) using XLSTAT 2019, Excel® 2013.
Results
Evaluation of the ovicidal effect of EPF against B. tabaci and T. urticae
Number of surviving eggs of B. tabaci and T. urticae on melon leaves decreased rapidly on plants treated with EPF B. bassiana strain ATCC, B. bassiana strain R444 and L. muscarium Ve6 as well as plants treated with Diafenthiuron. Over the monitoring period, the number of surviving eggs of B. tabaci for the untreated plants (control) was relatively high; it exceeded 25.33 eggs/leaf, whereas it decreased to an average of 5.53, 6.86 and 6.6 eggs 3 days after treatment with B. bassiana ATCC, B. bassiana R444 and L. muscarium, respectively. Similar to EPF, Diafenthiuron reduced the number of eggs of B. tabaci from 12.26 to only 4.26 eggs/leaf 3 days after treatment (Fig. 2A). After 15 days post-treatment, the number of B. tabaci eggs started to increase at all treatments but remained significantly lower compared to those in untreated control (F = 6.412; P = < 0.0001).
In addition, the number of surviving eggs of T. urticae for the untreated control lots was high, varying between 4.4 and 12.4 eggs/leaf. Indeed, the number of T. urticae eggs was 13.93 eggs/leaf before the treatments, which led to a regular decrease of 0.06, 0.06, 0.4 and 0.2 eggs/leaf on the 15th day after treatment for B. bassiana ATCC, B. bassiana R444 and L. muscarium Ve 6, respectively. Similarly, for plants treated with Diafenthiuron, the number of T. urticae eggs per leaf decreased from 15.86 before treatment to only 0.2 eggs/leaf on the 15th day after treatment (Fig. 2A). According to the statistical analysis, the three commercial products based on EPF significantly reduced the number of T. urticae eggs even as the chemical treatment over time (F = 5.764; P < 0.0001).
The percentages of reduction in the total number of live eggs of B. tabaci were of 58.52%, 50.45% and 42.65% for the B. bassiana strain ATCC, B. bassiana strain R444, L. muscarium strain Ve6, respectively and 66.03% after treatment with Diafenthiuron (Table 1). The ANOVA analysis of the reduction in B. tabaci eggs showed that no significant effect (F = 1.281; P = 0.325) between the EPF treatment and the chemical treatment based on Diafenthiuron.
T. urticae egg reduction rates were generally higher than B. tabaci egg reduction rates exceeding 92.86% (Table 1). The analysis of variance showed that B. bassiana ATCC and B. bassiana strains R444 had a more effective effect than L. muscarium strain Ve6 15 days after treatments.
Evaluation of the treatments effects on the larval stages of B. tabaci and the mobile forms of T. urticae
Density of B. tabaci larvae decreased from 10.73, 10.26 and 11.73 larvae per leaf before treatment to 3.26, 3.93 and 4.26 larvae 3 days after treatments with B. bassiana strain ATCC, B. bassiana strain R444 and L. muscarium strain Ve6, respectively. Similarly, the substance Diafenthiuron reduced the number of B. tabaci larvae from 12.13 to 3.26 larvae per melon leaf 3 days after treatment (Fig. 3A). The ANOVA analysis of the numbers of B. tabaci larvae highlighted a significant effect after the EPF treatments by comparing to the untreated control (F = 4.851; P = 0.001).
In addition, during the monitoring period, the total number of surviving mobile forms of T. urticae for the untreated control plants increased and varied between 6.2 and 13.73 mobile forms/leaf. On the other hand, the number of larvae, protonymphs, deutonymphs and adults of T. urticae decreased rapidly for plants treated with B. bassiana (strain ATCC and strain R444) and L. muscarium strain Ve6 as well as those treated with Diafenthiuron until their abandon (Fig. 3B). The EPF affected significantly (F = 12.845; P < 0.0001) the number of mobile forms of T. urticae.
The evaluation of the efficacy of the EPF tested is based on the calculation of reduction rates against B. tabaci larvae and mobile forms of T. urticae. This test consisted of studying the effectiveness of EPFs and comparing them to that of a Pegasus® insecticide (Diafenthiuron) approved against B. tabaci and T. urticae and an untreated control.
The calculation of the reduction percentages against the total number of B. tabaci larvae showed a reduction exceeding 54.09% in the plants treated with EPF as well as those treated with Diafenthiuron. In addition, the percentages of efficacy against mobile forms of T. urticae were of 98.52, 99.48 and 95.11%, following treatment with B. bassiana strain ATCC, B. bassiana strain R444 and L. muscarium strain Ve6, respectively (Table 2).
Discussion
The treatments with B. bassiana (strain ATCC and strain R444) and L. muscarium strain Ve6 showed a very significant efficacy against different stages of both pests B. tabaci and T. urticae than the untreated control. In fact, they can reduce the number of B. tabaci eggs by up to 65% and the number of B. tabaci larvae by up to 58% compared to untreated plants. In this context, Assadi et al. (2021) demonstrated that B. bassiana strain R444 and L. muscarium strain Ve6 were significantly effective on all developmental stages of B. tabaci under controlled conditions. In addition, several studies have shown that EPF are very effective against the whitefly. According to Keerio et al. (2020), two strains of B. bassiana (BB-72 and BB-252) and one strain of L. lecanii (V-2) caused a maximum mortality of B. tabaci after 12 days of treatment at different temperatures. Wari et al. (2020) showed that B. bassiana strain GHA caused a significant reduction in different life stages of B. tabaci under greenhouse conditions. Application of several B. bassiana isolates against B. tabaci development stages on different host plants showed significant efficacy that affected the reproductive rates (Zafar et al. 2016). Others, B. bassiana and M. anisopliae caused the highest larval mortality of B. tabaci under greenhouse conditions (Sain et al. 2021).
In addition, the tested EPF showed very high efficacy against eggs and motile forms of T. urticae with a reduction percentage greater than 92%. Chandler et al. (2005) found that B. bassiana (Naturalis-L) reduced the number of T. urticae adults, larvae and eggs by up to 97%. Additionally, fungal isolates of M. anisopliae and B. bassiana were pathogenic against the mite females, which were more virulent at 25, 30, and 35 °C than at 20 °C (Bugeme et al. 2009). Indeed, these EPF are highly capable of causing mortality for all stages of T. urticae. Several studies have shown that spider mites are susceptible to and affected by EPF. B. bassiana strains showed a high virulence for T. urticae eggs and adults (Hassan et al. 2017). M. anisopliae isolates with potential for the control of T. urticae (Elhakim et al. 2020), especially for adult females (Castro et al. 2018). Al Khoury et al. (2020) showed that following the application of B. bassiana against all life stages of T. urticae, where the mortality rate was 52, 67.9 and 95.3% in eggs, mobile forms and adults, respectively. Moreover, the two isolates of B. bassiana and 17 isolates of M. anisopliae caused a mortality rate of 80% against Tetranychus evansi Baker & Pritchard (Wekesa et al. 2005). Thus, the use of B. bassiana on bean plants led to a reduction in adult populations of T. urticae by significantly affecting the fecundity of females (Wu et al. 2020) and adverse effects on certain other biological parameters of this mite (Kheradmand et al. 2021).
Bean seed treatment with B. bassiana and M. robertsii isolates resulted in endophyte colonization and reduced T. urticae populations under greenhouse conditions (Canassa et al. 2019). However, EPF had no obvious pathogenicity for the phytoseiid predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Dogan et al. 2017). In addition, mortality of T. urticae was obtained when predatory mites carried conidia B. bassiana or M. anisopliae. Predatory mites that were able to control T. urticae could be associated with EPF (Castillo-Ramírez et al. 2020).
Conclusion
In conclusion, it appears that EPF treatment can be used as a mean of controlling B. tabaci and T. urticae in protected and geothermal crops. They are very effective, especially on the eggs and mobile forms of T. urticae. This finding inspires us to apply this fungus on the first clutches. It can be considered as an innovative biological control tool for managing these two pests of cucurbits in heated greenhouses in Southern Tunisia. Since these pests are found on the same host plants, the use of this EPF can reduce the number of chemical applications.
Availability of data and materials
All data of the study have been presented in the manuscript, and high-quality and grade materials were used in this study.
Abbreviations
- EPF:
-
Entomopathogenic fungi
- TCPG:
-
The technical center for protected and geothermal crops in Chenchou
- PDA:
-
Potato dextrose agar
- RCBD:
-
Randomized complete blocks design
- ANOVA:
-
Analysis of variance
- DAT:
-
Day after treatment
- P:
-
P Value
References
Abdel-Raheem M, Al-Keridis LA (2017) Virulence of three entomopathogenic fungi against whitefly, Bemisia tabaci (Gennadius)(Hemiptera: Aleyrodidae) in tomato crop. J Entomol 14:155–159. https://doi.org/10.3923/je.2017.155.159
Al Khoury C, Guillot J, Nemer N (2020) Susceptibility and development of resistance of the mite Tetranychus urticae to aerial conidia and blastospores of the entomopathogenic fungus Beauveria bassiana. Syst Appl Acarol 25:429–443
Assadi BH, Chouikhi S, Ettaib R, M’hamdi NB, Belkadhi MS (2021) Effect of the native strain of the predator Nesidiocoris tenuis Reuter and the entomopathogenic fungi Beauveria bassiana and Lecanicillium muscarium against Bemisia tabaci (Genn.) under greenhouse conditions in Tunisia. Egypt J Biol Pest Control 31:1–11. https://doi.org/10.1186/s41938-021-00395-5
Basit M (2019) Status of insecticide resistance in Bemisia tabaci: resistance, cross-resistance, stability of resistance, genetics and fitness costs. Phytoparasitica 47:207–225. https://doi.org/10.1007/s12600-019-00722-5
Bel Kadhi MS (2004) Etude bioécologique de Bemisia tabaci (Homoptera: Aleyrodidae) dans les serres géothermiques du sud tunisien. Possibilité de son contrôle biologique au moyen de parasitoïdes indigènes, Paul Cezanne Aix-Marseille
Bensoussan N, Zhurov V, Yamakawa S, O’Neil CH, Suzuki T, Grbić M, Grbić V (2018) The digestive system of the two-spotted spider mite, Tetranychus urticae Koch, in the context of the mite-plant interaction. Front Plant Sci 9:1206. https://doi.org/10.3389/fpls.2018.01206
Bugeme DM, Knapp M, Boga HI, Wanjoya AK, Maniania NK (2009) Influence of temperature on virulence of fungal isolates of Metarhizium anisopliae and Beauveria bassiana to the two-spotted spider mite Tetranychus urticae. Mycopathologia 167:221–227. https://doi.org/10.1007/s11046-008-9164-6
Canassa F, Tall S, Moral RA, de Lara IA, Delalibera I Jr, Meyling NV (2019) Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites. Biol Control 132:199–208. https://doi.org/10.1016/j.biocontrol.2019.02.003
Castillo-Ramírez O, Guzmán-Franco AW, Santillán-Galicia MT, Tamayo-Mejía F (2020) Interaction between predatory mites (Acari: Phytoseiidae) and entomopathogenic fungi in Tetranychus urticae populations. Biocontrol. https://doi.org/10.1007/s10526-020-10004-3
Castro T, Eilenberg J, Delalibera I (2018) Exploring virulence of new and less studied species of Metarhizium spp. from Brazil for two-spotted spider mite control. Exp Appl Acarol 74:139–146. https://doi.org/10.1007/s10493-018-0222-6
Chandler D, Davidson G, Jacobson R (2005) Laboratory and glasshouse evaluation of entomopathogenic fungi against the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), on tomato, Lycopersicon esculentum. Biocontrol Sci Tech 15:37–54. https://doi.org/10.1080/09583150410001720617
De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. https://doi.org/10.1146/annurev-ento-112408-085504
Dogan YO, Hazir S, Yildiz A, Butt TM, Cakmak I (2017) Evaluation of entomopathogenic fungi for the control of Tetranychus urticae (Acari: Tetranychidae) and the effect of Metarhizium brunneum on the predatory mites (Acari: Phytoseiidae). Biol Control 111:6–12. https://doi.org/10.1016/j.biocontrol.2017.05.001
Elhakim E, Mohamed O, Elazouni I (2020) Virulence and proteolytic activity of entomopathogenic fungi against the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae). Egypt J Biol Pest Control 30:1–8. https://doi.org/10.1186/s41938-020-00227-y
Farazmand A, Amir-Maafi M (2018) A population growth model of Tetranychus urticae Koch (Acari: Tetranychidae). Persian J Acarol. https://doi.org/10.22073/pja.v7i2.36245
Hassan D, Rizk MA, Sobhy HM, Mikhail WZ, Nada MS (2017) Virulent entomopathogenic fungi against the two-spotted spider mite Tetranychus urticae and some associated predator mites as non target organisms. Egypt Acad J Biol Sci Entomol 10:37–56. https://doi.org/10.21608/eajb.2017.12124
Henderson CF, Tilton EW (1955) Tests with acaricides against the brown wheat mite. J Econ Entomol 48:157–161
Hesketh H, Alderson PG, Pye BJ, Pell JK (2008) The development and multiple uses of a standardised bioassay method to select hypocrealean fungi for biological control of aphids. Biol Control 46:242–255. https://doi.org/10.1016/j.biocontrol.2008.03.006
Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219. https://doi.org/10.1023/A:1022846630513
Keerio AU, Nazir T, Abdulle YA, Jatoi GH, Gadhi MA, Anwar ST, Qiu D (2020) In vitro pathogenicity of the fungi Beauveria bassiana and Lecanicillium lecanii at different temperatures against the whitefly, Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae). Egypt J Biol Pest Control. https://doi.org/10.1186/s41938-020-00247-8
Kheradmand K, Heidari M, Sedaratian-Jahromi A, Talaei-Hassanloui R, Havasi M (2021) Biological responses of Tetranychus urticae (Acari: Tetranychidae) to sub-lethal concentrations of the entomopathogenic fungus Beauveria bassiana. Bull Entomol Res. https://doi.org/10.1017/S0007485321000523
Maniania NK, Bugeme DM, Wekesa VW, Delalibera I, Knapp M (2008) Role of entomopathogenic fungi in the control of Tetranychus evansi and Tetranychus urticae (Acari: Tetranychidae), pests of horticultural crops. Dis Mites Ticks. https://doi.org/10.1007/978-1-4020-9695-2_21
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248. https://doi.org/10.1146/annurev-phyto-072910-095235
Nouran Saad AA, Yousef AH (2021) Side effect of indigenous entomopathogenic fungi on the predatory mite, Cydnoseius negevi (Swirski and Amitai) (Acari: Phytoseiidae). J Plant Prot Pathol 12(3):215–223. https://doi.org/10.21608/jppp.2021.66659.1020
Park YL, Lee JH (2002) Leaf cell and tissue damage of cucumber caused by twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 95:952–957. https://doi.org/10.1093/jee/95.5.952
Sain SK, Monga D, Hiremani NS, Nagrale DT, Kranthi S, Kumar R, Kranthi KR, Tuteja O, Waghmare VN (2021) Evaluation of bioefficacy potential of entomopathogenic fungi against the whitefly (Bemisia tabaci Genn.) on cotton under polyhouse and field conditions. J Invertebr Pathol 183:107618
Solanki R, Jha S (2018) Population dynamics and biology of whitefly (Bemisia tabaci Gennadius) on sunflower (Helianthus annuus L.). J Pharmacogn Phytochem 7:3055–3058
Vega FE (2018) The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110:4–30. https://doi.org/10.1080/00275514.2017.1418578
Wang Z, Cang T, Wu S, Wang X, Qi P, Wang X, Zhao X (2018) Screening for suitable chemical acaricides against two-spotted spider mites, Tetranychus urticae, on greenhouse strawberries in China. Ecotoxicol Environ Saf 163:63–68. https://doi.org/10.1016/j.ecoenv.2018.07.058
Wari D, Okada R, Takagi M, Yaguchi M, Kashima T, Ogawara T (2020) Augmentation and compatibility of Beauveria bassiana with pesticides against different growth stages of Bemisia tabaci (Gennadius); an in vitro and field approach. Pest Manag Sci 76:3236–3252. https://doi.org/10.1002/ps.5881
Wekesa VW, Maniania NK, Knapp M, Boga HI (2005) Pathogenicity of Beauveria bassiana and Metarhizium anisopliae to the tobacco spider mite Tetranychus evansi. Exp Appl Acarol 36:41–50. https://doi.org/10.1007/s10493-005-0508-3
Wu S, Xie H, Li M, Xu X, Lei Z (2016) Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Exp Appl Acarol 70:421–435. https://doi.org/10.1007/s10493-016-0090-x
Wu S, Sarkar SC, Lv J, Xu X, Lei Z (2020) Poor infectivity of Beauveria bassiana to eggs and immatures causes the failure of suppression on Tetranychus urticae population. Biocontrol 65:81–90. https://doi.org/10.1007/s10526-019-09970-0
Zafar J, Freed S, Khan BA, Farooq M (2016) Effectiveness of Beauveria bassiana against cotton whitefly, Bemisia tabaci (Gennadius)(Aleyrodidae: Homoptera) on different host plants. Pak J Zool 48:91–99
Acknowledgements
The authors are especially grateful to “Zina fresh” company for providing all the resources needed for this study.
Funding
This research was funded by “Zina fresh” company and by the Technical Center for Protected and Geothermal Crops Gabes.
Author information
Authors and Affiliations
Contributions
SC and MSB conceived and designed the experiments. SC and BHA performed the experiments. SC analyzed the data. SC, KLG, and MSB wrote the paper. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Chouikhi, S., Assadi, B.H., Lebdi, K.G. et al. Efficacy of the entomopathogenic fungus, Beauveria bassiana and Lecanicillium muscarium against two main pests, Bemisia tabaci (Genn.) and Tetranychus urticae (Koch), under geothermal greenhouses of Southern Tunisia. Egypt J Biol Pest Control 32, 125 (2022). https://doi.org/10.1186/s41938-022-00627-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s41938-022-00627-2