Biocontrol of Tuta absoluta for sustainable tomatoes production in Lebanon

Tomatoes (solanum Lycopersicum mill) are one of the most widely farmed and consumed vegetables in the world, they belong to the nightshade family, Solanaceae. According to FAOSTAT [1], the world's yearly tomato production is around 186,821,216 million metric tons: Asia producing share 54.4 %, America 17.5 %, Europe 15.7 %, and Africa 11.9 %. In addition, China was the world's greatest tomato producer in 2020, with an estimated production of 37,649,822.3 million metric tons, followed by the United States, India, Turkey, Egypt, and Italy [1]. On a global scale, the tomato (Lycopersicon esculentum) is becoming increasingly important for fresh crop consumption, including a primary component in many prepared foods, and studying the fundamental principles of plant growth and development. Moreover, it is high in nutrients such as vitamins, minerals, and antioxidants, all of which are necessary for a healthy human diet and can be grown in both open fields and greenhouses [2]. In Lebanon, tomatoes are one of the most produced agricultural commodities, with an average annual production of 305,300 tons over an area of 5,000 hectares in 2020 [1]. It is the first important vegetable crop followed by cucumber and onions with a production of 120,093 tons and 69,159 tons respectively [1]. However, their production has been hampered by several biotic and environmental restrictions. 

Pests and illnesses are prominent examples of such restrictions, as they diminish yields and the quality of marketable crops, and some are directly linked to tomato damage and productivity losses. One of them is Tuta absoluta [3]. Tuta absoluta, also known as tomato leafminer, is recognized as a significant threat to tomato production, in both greenhouse and open field circumstances. The moth originated in South America and had since moved to Europe, North Africa, Asia, and the Middle East respectively [4]. Moreover, it affects tomatoes grown for both fresh and processed markets, with larvae causing up to 100 % losses when no effective control strategies are used [5]. Tuta absoluta has a high reproductive capacity, with the ability to produce up to 12 generations per year under ideal conditions [6]. In addition, insecticide resistance has been facilitated by the extensive and regular use of pesticides on this pest, both in its native range and in newly invaded areas [7]. In Lebanon, unfortunately, the farmers’ primary method of Tuta absoluta control is blanket spraying with insecticides every 4 – 5 days per season, with a minimum and a maximum number of sprays of 8 to 25 sprays, respectively [8]. This method is certainly harmful to both humans and the environment [9]. For this, the development of control strategies based on the use of bio-insecticides as alternatives to synthetic insecticides should be supported, due to the significant effects of pesticides on insect pests, low mammalian toxicity, low persistence in the environment, and biodegradability [10]. 

In this direction, this research aimed to assess the effectiveness of various biological treatments of Tuta absoluta on Lebanese tomato variety Heirloom and compare it with the control as follows: Bacillus thurigiengis (Treatment 1); Orange essential oil (Treatment 2); Pepper extract mixed with organic olive soap (Treatment 3); Pepper and garlic extract mixed with organic olive soap (Treatment 4); Garlic extract mixed with organic olive soap (Treatment 5); Organic Olive soap (Treatment 6); and Control (Treatment 7).

Experimental Site Description: From April to August 2022, we conducted a field open trial at the Lebanese Agricultural Research Institute (LARI) in Qleiat - Keserwan station, North Beirut, at 992 m above sea level, located at Latitude: 33° 96′ 37.33″ N, and a longitude of 35° 71′ 43.69″ E. A general view of the experimental field can be seen in Figure 1.

Figure 1: Experimental field at the early stage of the growth production of tomatoes. Source: Michel Frem’s photo 

In terms of climatic conditions, the region of Mount Lebanon has a Mediterranean climate characterized by hot and dry summers from June to September and cool and rainy winters from December to mid-March, with an average annual temperature of 15°C [11]. Summers along the shore are hot and humid, with temperatures reaching 35°C in August. However, because of the sea's cooling impact, the daily temperature range is narrower than it is inland. January is the coldest month, with temperatures ranging from 5 to 10°C. At the seaside, the average annual rainfall is between 700 and 1,000 mm. Approximately 70% of the country's typical rainfall comes between November and March and is concentrated during only a few days of the rainy season, dropping in large cloudbursts or intense storms. Inland Lebanon receives more precipitation (1,600 mm) than the coast, including snow in the highlands. Figures 2 and 3 depict the meteorological data collected from a weather station located in LARI, Qleiat. As seen below, the mean average temperature is shown by a line graph coloured in blue. In the graph, the lowest temperature was in January 2021 and 2022 with a temperature of 9°C and 6°C respectively. The highest temperature was detected in August 2021 with an average temperature of 25°C, and in July 2022 with an average temperature of 22°C. The Figure 3 depicts the average precipitation for each month of the years 2021 and 2022. The maximum precipitation was recorded in the months of January 2021 and 2022, with 328 mm and 307 mm, respectively. Furthermore, there was no precipitation from August to May in 2021. However, there was precipitation in the summer season of 2022, with the lowest recorded precipitation being 2.4 mm in April 2022.

Figure 2: Monthly air temperatures (°C). Source: Our elaboration from the weather station of LARI.

 Figure 3: Monthly precipitation (mm) of the experimental site. Source: Our elaboration from the weather station of LARI. 

Statistical Experimental Design: We based the experimental on a randomized complete block design with seven treatments of the extracts and Bacillus thuringiensis replicated three times as shown in Figure 4. We intercropped tomato plants cv. Heirloom with celery plants over an area of 120 m2 area. Each plot was 1.2 m long and 4.2 m wide and contained 5 rows. Each row contained 4 tomato plants intercropped with 1 celery plant with a total of 10 plants/ plot respectively for tomato and celery. Each variable was subjected to the univariate analysis of variance, and when significant, the means were compared to 5% using Tukey’s test. In addition, IBM SPSS statistics software (version 23, 2018) was used for all statistical analyses. As such, we sued the following treatments applications: 

Treatment 1: Bacillus thuringensius (i.e., 20 g of javelin + 200 g of sugar + 200 mL of citric acid per 20 L of water), opting for a synergetic effect. As Bacillus affects the larvae of Tuta absoluta, the sugar mixed with Bacillus would increase the ingestion of the bacterium while citric acid would accentuate the degradation of the digestive tube of the larvae;

Treatment 2: Orange essential oil (i.e., 100 mL per 20 L of water);

Treatment 3: Pepper extract mixed with organic olive oil soap (250 mL + 100 g of organic olive oil soap per 20 L of water);

Treatment 4: Mixture of pepper and garlic extracts (125 g of pepper extracts+100 g of garlic extracts+ 100 g of organic olive oil soap per 20 L of water);

Treatment 5: Garlic extract mixed with organic olive oil soap (100 mL+ 100 g of organic olive oil soap per 20 L of water);

Treatment 6: Organic olive oil soap (100 g per 20 L of water);

 Treatment 7: Control 

 Figure 4: Experimental design of the field. 

Planting Pest Surveillance and Monitoring: As preventive measures against diseases, we dusted all young tomato plants (Figure 5) with yellow sulphur powder till reaching the flowering stage to protect them from potential pests and diseases. In fact, numerous sulphur compounds were advised in numerous Integrated Pest Management (IPM) publications for reasons of environmental safety programs for risk management in particular, edible plants (such as fruit trees and vegetables) from plant pathogenic illnesses and insect and mite infestations [12]. In addition, several studies suggested that the use of sulphur, especially as dustable powder, could be considered as a tool in Tuta absoluta management strategies [13]. For monitoring, we used cylindrical containers (Figure 6) filled with water to 1/3, located in the ground close to the ground to trap Tuta absoluta male moths, starting the second week of planting tomato plants. We counted the number of male moths of Tuta absoluta captured by the trap for each week by eliminating those already captured previously. We renewed the capsules of pheromone for Tuta absoluta every 4 weeks. We randomly placed three of these containers in the concerned Blocks. We observed the traps weekly starting from 11th May 2022. As such, we started harvesting the tomatoes fruits on 14th July 2022. Continuously, we recorded the health status of the tomato plants were recorded each week, mentioning any abnormalities and insect attacks as well as the possible presence of the tomato leafminer, Tuta absoluta. 

 Figure 5: Tomato plant dusted with powder sulfur

 Figure 6: Tuta absoluta male moths captured 

Treatments and Data Collection: The application of the treatments was done by manual spraying with a backpack sprayer every week regularly over a period of two months. The first treatment began three weeks after planting on 21st June. The sampling was done in each basic plot of the 8 plants. Three homogenous plants were selected from each plot. All infected leaves of Tuta absoluta were counted with the aid of a glass lens that reflected the leaflets’ underside. Moreover, the infected and non-infected fruits were counted and weighted [14]. To calculate the rate of infection the simple formula of dividing the number of mined leaves of the treated plant by the number of mined leaves of the control was used. The reduction %age in leaves of Tuta absoluta was calculated according to the following equation [15]:

 Where: A: number of larvae or mine blotches on leaves in control, and B: number of larvae or mine blotches on leaves in treatment.

To calculate the percentage of the weight loss of infested fruits on tomato by the Tuta absoluta infestation, the following formula was [15]:

Preparation of Botanical Extracts and Treatments Application: For the garlic aqueous extract, 250 g of garlic was weighed and then crushed. The crushed garlic was soaked in one litre of distilled water for 2 hours. Lastly, the garlic extract was filtered in the container. For the chili pepper aqueous extract,100 g of chili pepper was weighed and then crushed. The crushed pepper was boiled with 2 litres of distilled water for 1 hour. Lastly, the pepper extract was filtered in the container [14]. Regarding the orange essential oil, it was prepared in VWaste start-up facility. The schematic diagram (Figure 7) of the screw press machine cross-section below explains the key parts the machine contains a variable pitch screw press, connected to the screw shaft and gearbox. The screw is inserted into the machine pressing cage. At the top of the machine, there is a feed hopper. At the bottom of the pressing cage, there are nozzles. All machine components are made from food-grade stainless steel, such as 18/10, and 18/8, among others. For the oil separation from the emulsion, a lab centrifuge is needed that can provide speeds higher than 5000 rpm. The orange peels are inserted from the feed hopper. The peels are guided towards the screw press inside the machined cage. The variable pitch screw provides a gradual pressure increase on the peels, which is necessary to ensure efficient extraction of oil emulsion from the peels. The oil emulsion falls from the nozzles at the bottom of the cage and is collected into jars. The emulsion is put inside the centrifuge tubes, then the centrifuge is separated at >5000 rpm, for >10 mins. After centrifugation, the oil will float on top of the emulsion, which is collected with syringes into the final packaging for usage. 

 Figure 7: Orange essential oil preparation machine. Source: Rita Sfeir’s photo

Effect of organic treatments on the reduction of tomatoes leaves infestation: Among all the different organic treatments, the analysis of variance (Table 1) demonstrated a very high significance among the means of the reduction of infestation by Tuta absoluta on tomatoes leaves. Regarding the disease incidence, the post hoc Tukey’s Honest Significant Difference (HSD) test divided the population of treatments into four homogenous subsets (Table 2). Therefore, the tomatoes plants treated with Bacillus thuringiensis (Treatment 1) were least affected, whereas the non-treated plants were highest affected by the attack of Tuta absoluta based on the reduction of tomatoes leaves infestation. 

Table 1: Univariate analysis of variance: Effect of treatments on the reduction of tomatoes leaves infestation (in %).

^a .996 MS (Replication) + .004 MS (Error); b .992 MS (Treatment * Replication) + .008 MS(Error); c .979 MS (Treatment * Replication) + .021 MS (Error); d MS (Error) 

Furthermore, the post hoc Tukey’s HSD test (Table 2; Figure 8) showed also that Bacillus thuringiensis was able to control effectively the infestation of Tuta absoluta on tomatoes leaves. There was no statistically difference between the latter (Treatment 1), orange essential oil (Treatment 2) and the mixture of pepper and garlic extract mixed with organic olive soap (Treatment 4). As such, this homogenous subset presents a value of p = .13. Also, Table 2 reveals also that Treatments 2, 3, 4 and 5 constitute another homogeneous group (p = .63). In addition, tomatoes plants treated with organic olive soap (Treatment 6) is highly affected by the infestation, after the control, but their reduction of infestation does not significantly differ from other plants treated with: pepper extract mixed with organic olive soap (Treatment 3), pepper and garlic extract mixed with organic olive soap (Treatment 4) and, garlic extract mixed with organic olive soap (Treatment 5) as shown also in Table 2. 

Table 2: Univariate analysis of variance: Effect of treatments on the reduction of tomatoes leaves due to the infestation by Tuta absoluta (in mean %).

Means for groups in homogeneous subsets are displayed. Based on Type III Sum of Squares, the error term is Mean Square (Error) = 343.075. a Uses Harmonic Mean Sample Size = 18.808. b The group sizes are unequal. The harmonic mean of the group sizes is used. Type I error levels are not guaranteed. c Alpha = .05.

Figure 8: Mean reduction of Tuta absoluta infestation incidence (in %) on Lebanese tomatoes leaves as affected by the different organic treatments. Values marked with the same letter are not statistically different, according to the Tukey‘s HSD test (P≤ .05). 

Effect of organic treatments on the weight loss of tomatoes fruits infestation: Regarding the effect of organic treatments on the weight loss of tomatoes fruits infestation by Tuta absoluta, the analysis of variance showed a very high significance (Table 3). Across all the different organic treatments, Bacillus thuringiensis (Treatment 1) was the most effective treatment in protecting the tomatoes plants, with a least reduction in weight loss of tomatoes fruits due to the infestation by Tuta absoluta. The orange essential oil (treatment 2) resulted as the second most effective treatment. Furthermore, the pepper and garlic extract mixed with organic olive soap (Treatment 4), the pepper extract mixed with organic olive soap (Treatment 3), the garlic extract mixed with organic olive soap and, the organic olive soap are classified as the third, fourth, fifth and sixth most effective treatments, respectively in terms of the weight loss of tomatoes fruits infestation by Tuta absoluta. 

^a MS (Rep); ^b MS (Treatment ^* Replication); ^c MS (Error)

Table 3: Univariate analysis of variance: Effect of treatments on the weight loss of tomatoes fruits due to the infestation by Tuta absoluta (in mean %). 

Furthermore, the post hoc Tukey’s HSD test (Table 4) showed also that there was no statistically difference between Bacillus thuringiensis (Treatment 1) and orange essential oil (Treatment 2). Also, the mixture of pepper and garlic extract mixed with organic olive soap (Treatment 4) appears to form d distinctive subset group and present a value of p = 1.00. In addition, Table 4 reveals also that Treatments 3, 5 and 6 constitute another homogeneous group (p = .903). Consequently, Figure 9 recapitulates the distribution of the various organic treatments according to their effectiveness in terms of the reduction on the weight loss of tomatoes fruits, compared to the untreated control in the management of Tuta absoluta on Lebanese tomatoes. 

Table 4: Homogeneous subset post hoc Tukey’s HSD test: Effect of treatments on the weight loss of tomatoes fruits due to the infestation by Tuta absoluta (in mean %).

Means for groups in homogeneous subsets are displayed. Based on Type III Sum of Squares.

The error term is Mean Square (Error) = 154.222. a Uses Harmonic Mean Sample Size = 18.000. b Alpha = .05. 

Figure 9: Mean weight loss of tomatoes fruits due to the infestation by Tuta absoluta (in mean %) as affected by the different organic treatments.

Values marked with the same letter are not statistically different, according to the Tukey‘s HSD test (P≤.05).

The results obtained in tomato open-field cultivation reveal that it is possible to reduce the tomato leaf miner impact by applying Bacillus thuringiensis. The potential of Bacillus thuringiensis formulates in controlling Tuta absoluta was clearly demonstrated in laboratory tests [16-20]. Moreover, when compared to non-treated controls, a research undertaken in Spain to investigate the effect of Bacillus thuringiensis on Tuta absoluta revealed great effectiveness in minimizing the damage at high infestation levels. As indicated in the results above (Figure 7), where Bacillus thuringiensis reduced Tuta absoluta on leaves by 60%, while (Figure 8) revealed a 15% reduction in weight loss of tomatoes. In addition, it was the most effective treatment compared to others. Bacillus thuringiensis, also found to be quite effective in decreasing the damage caused by the first, second, and third Tuta absoluta larval instars [21]. Furthermore, another study found evidence that first instar larvae were the most susceptible to Bacillus thuringiensis and that it could keep Tuta absoluta below economic thresholds [22]. Moreover, a research evaluated the effectiveness of Bacillus thuringiensis against Tuta absoluta and found that it caused substantial mortality in all three larval instars [23]. The study’s findings support the larvicidal action of Bacillus thuringiensis var. Kurstaki suspension against Tuta absoluta and highlight it as a potentially safe tool for use in integrated pest control in agricultural settings [22]. In addition, the results of tomato open-field cultivation show that applying orange essential oil can also help in reducing the impact of tomato leaf miners. According to studies, with researchs experimented with the essential oils extracted from Citrus aurantium and Citrus limon peels against third instar larvae of both pest species. The analysis by gas chromatography showed that limonene was the principal constituent of Citrus aurantium essential oils (88.57%) and Citrus limon (70.46%). Fumigant toxicity tests showed that Citrus aurantium oil was more toxic (LC50 was 14.68 μl/l air than Citrus limon (LC50 was 24.33 μl/l air for Tuta absoluta). The mortality rate of Tuta absoluta increased with the increase in essential oils dose. Hence, the essential oils of the two Citrus were found to be toxic, this could be useful for the investigation of new natural insecticidal compounds [24]. The efficacy of essential oil extracted from Citrus limon (Rutaceae) peels against Tuta asboluta was investigated in this experiment. Limonene was found to be the most abundant ingredient in the gas chromatography analysis, accounting for 52.80% of the total. This study found that essential oil linked with nanoparticles cause the death of 12 % of eggs, 66 % and 52% of larvae for translaminar toxicity, and 30 % and 40 % of larvae for ingestion toxicity after 72 hours at a dosage of 40 mg/ml [25]. Studies revealed that plant extracts are potential larvicides of Tuta absoluta when prepared and applied appropriately. These findings were consistent with the data given in (Figure 8) above, where orange essential oil exhibited a 15% in weight loss and was the most effective among other treatments, in contrast to leaf infestation in (Figure 7), which had only 50% on the reduction of leave infestation. Finally, essential oils of orange have been tested as pesticides against a variety of pests. This interest could be due to their widespread availability at reasonable prices. Orange essential oil is frequently produced as a byproduct of the citrus juice industry, and the cold-pressing technique makes orange essential oil extraction less expensive than other methods. 

In this study, garlic and pepper extract mixed with organic olive soap extract showed relative moderate effect to control Tuta absoluta as shown by Figure 16, which this treatment resulted as 47% infection incidence on tomato leaves and 32% of weight loss due to infestation of Tuta absoluta (Figure 7). However, a similar study was conducted to determine if garlic (Allium sativum) and chili (Capsicum annum L) extracts may be used to control red spider mite in tomatoes. The results revealed that a combination of garlic and chilli was the most effective, followed by garlic and finally chilli [26]. On the other hand, a study carried out on tomatoes revealed that botanicals neem oil is effective in suppressing Tuta absoluta and has shown the greatest reduction in larval population [27]. 

According to this study, treating the Tuta absoluta with pepper and organic olive soap had little to no effect on it. This was consistent with (Figures 7 and 8), in which pepper experienced a 40% reduction in leaf infection and a 56% in weight loss due to Tuta absoluta infestation. However, studies included the effect of the water extract of Capsicum annuumers on some aspects of the life of the matrix Tuta absoluta, as a result of the destructive damage caused by this pest to the tomato crop in Iraq, three concentrations were used for the pepper extract (1%, 2%, and 4%), and studied the effect of these concentrations on egg hatching and the highest rate of hatching suppression 96.7% when using the pepper extract at a concentration of 4% and after 24 hours of laying eggs. Moreover, research evaluated the effect of Capsicum annuumers water extract on numerous aspects of the matrix Tuta absoluta's life. There were three concentrations of pepper extracts used: 1%, 2%, and 4%. As a consequence, the effect of various concentrations on egg hatching was investigated, with the highest rate of hatching suppression (96.7 %%t) when employing the pepper extract at a concentration of 4% and after 24 hours after egg laying [28]. The pepper Capsicum annuum L. aqueous fruit extracts were tested against the four larval stages of the tomato leafminer Tuta absoluta in a study. The results demonstrated that Capsicum annuum extracts were particularly efficient against Tuta absoluta larvae. The death rate was less than 25% after 24 hours, compared to more than 50% after 48 and 72 hours. Therefore, the extract used in this toxicological test was Capsicum annuum, which had a positive toxicological impact on Tuta absoluta larvae [29]. 

Garlic had no effect on the pest in this trial. Figures 6 and 7 indicated a 39% and 57% on leaf infestation, and in weight loss caused by the infestation, respectively. In accordance with Hussein et al. [30] discovered a significant drop in Tuta absoluta population after tomato plants were treated with garlic extract. Tuta absoluta was reduced moderately throughout this investigation due to the extraction procedure, which influences the presence of certain volatile oil that gives garlic its biological qualities. 

The findings of this study agreed with those of Ghanim and Abdel Ghani [31], who found that garlic had a little effect on Tuta absoluta second instar larvae in the laboratory but had a moderate effect in the greenhouse. Furthermore, a research was carried out on three natural plants, clove, parsley, and lavender, as well as three commercial monoterpenoils (eugenol, isoeugenol, and cincol), which were tested against Tuta absoluta. At 30 μl/l water concentration, clove, eugenol, and isoeugenol oils induced significant reductions in egg hatchability for both one- and four-day-old eggs. Furthermore, increased clove oil concentration triggered a histological impact on the body wall of the larvae [32]. A study was carried out to investigate the efficiency of aqueous extracts of Allium sativum (garlic), Allium cepa (onion), and Cloeme Arabica made by infusion on various pests that infect tomato plants by spraying them for biological control. The results revealed that all of these extracts had a toxic effect on the studied insects, equivalent to chemical pesticides. In contrast, the data revealed that the dosages and time flow had a noticeable influence on the death rate. The death rate was 100% for Tuta absoluta and Aphis gossypii when employing direct spraying [33]. Hussein et al. [30] obtained similar results with additional pests, reporting that a good aqueous solution of garlic will successfully control worms, beetles, and thrips in cowpea. 

The organic olive soap was highly affected by the infestation of Tuta absoluta. However, for almost 200 years, soap has been used to control insects. There has recently been a surge in interest in and use of these items. This shift is the result of a greater understanding of how to utilize soaps most effectively, as well as a desire to experiment with insecticides that are easier and safer to apply than many currently available options. It is still unclear how soaps and detergents kill insects. In most situations, control is achieved by disrupting the insect's cell membranes. Soaps and detergents may also remove the protective waxes that coat the insect, resulting in death due to excessive water loss [34]. Moreover, some studies had a positive effect in controlling other insects. A study suggests that native soap is an effective bio-pesticide against cowpea insect pests [35].

Tuta absoluta is one of the most harmful insect pests of several cultivated and non-cultivated host plants, particularly tomato plant Solanum lycopersicum L. Chemical insecticides are mainly used to manage the tomato leaf miner. However, their excessive use has led to several problems. Biological management remains an eco-friendly alternative for controlling of this pest. It relies on using bacteria, entomopathogenic fungi, animals, and plants. Plant extracts are easy to applicate and have low costs. Several species, plant parts and extracts forms are used. Biological effects of these extracts are due probably to their major components that affect vital physiological functions such as neurophysiology and respiration. This study is the assessment of the performance of organic treatments in Lebanon on Tuta absoluta. The results obtained here suggest that Bacillus thuringiensis treatment presented the lowest impact on tomato leaf infestation reduction and, was the most effective treatment in protecting the tomatoes plants, with at least reduction in weight loss of tomatoes fruits. The orange essential oil resulted as the second most effective treatment, followed by: (i) pepper and garlic extract mixed with organic olive oil soap, (ii) pepper extract mixed with organic olive oil soap, (iii) garlic extract mixed with organic olive oil soap, and (iv) organic olive oil soap used alone. As such, Bacillus thuringiensis and orange essential oils are relatively effective and economically viable to organically control Tuta absoluta.

Special thanks are due to Mr Marwan Haidar, Maison de l’Agriculture, Antélias, Beirut (Lebanon), for his valuable agricultural ex-tension services and promotions towards this research.

1. FAOSTAT (2020) FAOSTAT-Production quantities of Tomatoes by country.
2. Bhowmik D, Kumar KPS, Paswan S, Srivastava S (2012) Tomato-a natural medicine and Its health benefits. Journal of Pharmacognosy and Phytochemistry 1: 33-43.
3. Cherif A, Mansour R, Grissa LK (2013) Biological aspects of tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) in conditions of northeastern Tunisia: possible implications for pest management Sustainable management of the invasive pest Tuta absoluta in Tunisia. Environmental and Experimental Biology 11: 179-184.
4. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, et al. (2010) Biological invasion of european tomato crops by Tuta absoluta: Ecology, geographic expansion and prospects for biological control. Journal of Pest Science 83: 197-215.
5. El-Shafie HAF (2020) Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) An invasive insect pest threatening the world tomato production. Invasive species - Introduction pathways, economic impact, and possible management options. IntechOpen, UK.
6. Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and, management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annual Review of Entomology 63: 239-258.
7. Siqueira HÀA, Guedes RNC, Picanño MC (2000) Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agricultural and Forest Entomology 2: 147-153.
8. ElHajj AK, Rizk H, Gharib M, Houssein M, Talj V, et al. (2017) Management of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) using biopesticides on tomato crop under greenhouse conditions. Journal of Agricultural Science 9: 123.
9. Picanço M, Leite GLD, Guedes RNC, Silva EA (1998) Yield loss in trellised tomato affected by insecticidal sprays and plant spacing. Crop Protection 17: 447-452.
10. Frem M, Nigro F, Medawar S, Moujabber ME (2022) Biological approaches promise innovative and sustainable management of powdery mildew in Lebanese squash. Sustainability 14: 2811.
11. World Bank (2022) Lebanon climatology. climate change knowledge portal Lebanon.
12. Gesraha MA, Ebeid AR (2019) Impact of sulfur dust application on the abundance of two important coccinellid predators in marrow fields. Bulletin of the National Research Centre 43.
13. Zappalà L, Biondi A, Alma A, Jboory IJA, Arnò J, et al. (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. Journal of Pest Science 86: 635-647.
14. Frem M, El Hachem N, Zgheib M (2015) Evaluation of the efficacy of botanical extracts and bt on tuta absoluta in organic farming system. Lebanese Agricultural Research Institute, Lebanon 1.
15. Derbalah AS, Morsey SZ, El-Samahy M (2012) Some recent approaches to control Tuta absoluta in tomato under greenhouse conditions. African Entomology 20: 27-34.
16. Guillemaud T, Blin A, Goff IL, Desneux N, Reyes M, et al. (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Scientific Reports 5: 1-5.
17. Lietti MMM, Botto E, Alzogaray RA (2005) Resistência a Inseticidas em Populações Argentinas de Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology 34: 113-119.
18. Cônsoli FL, Parra JRP, Hassan SA (1998) Side-effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (, Gelechiidae). Journal of Applied Entomology 122: 43-47.
19. Lakhdari W, Dehliz A, Acheuk F, Mlik R, Hammi H et al. (2016) Biocontrol test against the leaf minerof tomato Gelechiidae by using entomopathogenic fungi in the Algerian Sahara. Journal Algérien des Régions Arides 13: 85-289.
20. Andrade NJP, Monteros AA, Bastidas CGT, Sørensen M (2020) Morphological, sensorial and chemical characterization of chili peppers (Capsicum spp.) from the catie genebank. Agronomy 10: 1732.
21. González CJ, Mollá O, Montón H, Urbaneja A (2011) Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). BioControl 56: 71-80.
22. Alsaedi G, Ashouri A, Talaei HR (2017) Evaluation of Bacillus thuringiensis to control Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under laboratory conditions. Agricultural Sciences 8: 591-599.
23. Tsoulnara D, Port G (2016) Efficacy of a Beauveria bassiana strain, Bacillus thuringiensis and their combination against the tomato leafminer Tuta absoluta. Entomologia hellenica 25: 23-30.
24. Khaoula Z, Ikbal C, Wafa T, Imed C, Asma L, et al. (2013) Bio-insecticidal potential of essential oils of two Citrus species against two greenhouse pests Tuta absoluta Meyrick and Spodoptora littoralis Boisduval. Microbiologie et Hygiène Alimentaire 25: 84-88.
25. Konan KAJ, Ouali NSWM, Fondio L (2021) Geographical distribution and host range status of Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in Côte d’Ivoire. International Journal of Tropical Insect Science 42.
26. Fatima K, Tembo L, Wisdom K (2015) Efficacy of Garlic (Allium sativum) and Red Chilli Pepper (Capsicum annum) Extracts in the Control of Red Spider Mite (Tetranychus urticae) in Tomatoes (Lycopersicon esculentum). Asian Journal of Applied Sciences 3: 2321-893.
27. Kona NEM, Taha AK, Mahmoud MEE (2014) Effects of botanical extracts of Neem (Azadirachta indica) and Jatropha (Jatropha curcus) on eggs and larvae of tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Persian Gulf Crop Protection 3: 41-46.
28. Mubasher AFMK, Abd AH, Ibraheem MK (2019) Effect of the water extract of the capsicum annuum and the insecticide (relddan) in some aspects of the life of the Tuta absoluta. Plant Archives 19: 1511-1514.
29. Chermiti B, Abbes K (2012) Comparison of pheromone lures used in mass trapping to control the tomato leafminer Tuta absoluta in industrial tomato crops in Kairouan (Tunisia). EPPO Bulletin 42: 241-248.
30. Hussein NM, Hussein MI, Gadel SHH, Shaalan HS, Hammad MA (2015) Effect of two plant extracts and four aromatic oils on tuta absoluta population and productivity of tomato cultivar gold stone. Journal of Plant Protection and Pathology 6: 969-985.
31. Ghanim NM, Abdel GSB (2014) Control of Tuta absoluta (Lepidoptera: Gelechiidae) and Aphis gossypii (Hemiptera: Aphididae) by some aqueous plant extracts. Egyptian Journal of Biological Pest Control 24: 45-52.
32. Moawad SS, Ebadah IMA, Mahmoud YA (2013) Biological and histological studies on the efficacy of some botanical and commercial oils on Tuta absoluta Meyrich (Lepidoptera:Gelechiidae). Egyptian Journal of Biological Pest Control 23: 301-308.
33. Daboub K, Ghraysa N (2017) Study of the effect of plant extracts of: garlic, onions and figs on some pests affecting tomato plants: Allium sativum Allium cepa Cleome arabica Lycopersicon esculentum. Université of Eloued Algiria.
34. Cranshaw WS (2008) Insect Control: Soaps and Detergents. Bioagricultural sciences and pest management 3.
35. Egho EO, Enujeke EC (2012) Effect of native soap on insect pests and grain yield of Cowpea (Vigna unguiculata (L) Walp) in Asaba and Abraka during the late cropping season in Delta State, Nigeria. Sustainable Agriculture Research 1: 275.