Evaluation of the chinaberry extract against the tomato leafminer, Tuta absoluta (Merick) (Lepidoptera: Gelechiidae) in vitro

doi:10.21203/rs.3.rs-1962863/v1

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Evaluation of the chinaberry extract against the tomato leafminer, Tuta absoluta (Merick) (Lepidoptera: Gelechiidae) in vitro

https://doi.org/10.21203/rs.3.rs-1962863/v1

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The tomato leaf miner (TLM), Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is a important pest on tomato, potato and other Solanaceous with a huge economic importance. The discovery of active compounds that are less persistent will be beneficial to both the environment and agricultural product consumers. Management of the pest can be problematic, especially when the infestation pressure is high. In the current study, contact toxicity of the hexane extract from the chinaberry tree, Melia azedarach L. (MA) fresh fruit on the developmental stage of egg, the 2nd larval instars and pupae of T. absoluta were evaluated in the laboratory condition, 27 ± 2^oC, 65 ± 5% RH and 16L:8D hours photoperiods. Results indicated that with increasing the concentration of the extract, mortality of eggs, larvae and pupae also increased. Analysis of probit data showed that LC₅₀ for MA extract in egg, 2nd instar larvae and pupae were 948.93, 346.72 and 1.75 µl/ml, respectively. The results showed that this extract has a high potential for controlling T. absoluta in open and closed environments and is recommended to protect the environment and users' health.

contact toxicity

extract

Melia azedarach

Tuta absoluta

The tomato leaf miner (TLM), Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), a key pest of tomato and native to the western part of South America, invaded Brazil around 1980 (Souza and Reis 1992). It is now a devastating pest of tomato crops in South America, Europe, Africa and Asia (Tropea Garzia et al. 2012; Zappala` et al. 2013).

This pest is crossing borders and devastating tomato production in both protected and open fields (EPPO 2008, 2009; FERA 2009). In Iran, T. absoluta was first discovered in November 2010 to infest open-field tomato crops of the Uromiyeh Plant Protection Organization from Uromiyeh in Azerbaijan province in North West Iran region (Baniameri and Cheraghian 2012). In Iran, the insect has spread rapidly and it is currently considered a key insect pest on tomato crops, both in greenhouses and open-fields. Damage is caused by larval tunneling and they can penetrate young stems and fruits which finally result in the loss of over 80% of fruits (Desneux et al. 2011).

During the last decades, TLM controls were directed to the utilization of chemical insecticides. Environmental safety of insecticides is the first and foremost criterion for TLM control programs (Tropea Garzia et al. 2012). In most countries where T. absoluta occurs, the main control strategy includes frequent sprays with chemical insecticides because without control, T. absoluta causes about 100% yield losses and dramatically decreases the fruit quality in both field and greenhouse tomato crops (Gilardo´n et al. 2001; Tropea Garzia et al. 2012). Nevertheless, because of the development of resistance, chemical control has demonstrated limited efficacy even after the use of different types of pesticides and increasing the application frequencies (Lietti et al. 2005; Siqueira et al. 2000). This has led to the use of nonchemical control strategies, such as exploitation of the biocontrol provided by indigenous natural enemies (Zappalà et al. 2013) or the use of plant resistance with less environmental impact (Gilardo´n et al. 2001). The utilization of eco-friendly and easily biodegradable plant products with natural insecticidal activity has increased in recent years. To control pests without disturbing the environment, natural products have been screened for potential sources of insecticides. Plant materials with insecticidal properties have been employed to kill insects all over the world for generations. These materials are considered to be an alternative to conventional pesticides owing to their low toxicity to warm-blooded mammals, in addition to their high volatility. Botanical insecticides may be safer for the environment than synthetic insecticides, and they are usually easily processed and utilized by farmers and small industries (Belmain et al. 2001).

Interest in the plants’ essential oil and extract was renewed with emerging demonstration of their insecticidal properties. They act in several ways on various types of pests and can be applied to plants in the same way as other conventional insecticides (Benelli et al. 2012; Isman 2000). Most of the plant extracts are known to possess ovicidal, repellent, larvicidal activities and antifeedants against various insect species (Abbasipour et al. 2010, 2011a; Guedes et al. 2012; Isman 2000; Rosa et al. 2010; Sousa et al. 2013). Tuta absoluta integrated control programs may perhaps reduce control costs and environmental effects associated with the use of broad spectrum insecticides.

Melia azedarach L. (MA) also known as “chinaberry tree” is an ornamental species of the Meliaceae family considered to be native from Asia which grows from North to South America as well as Northern Australia, Africa and Southern Europe (Phua et al. 2008). It is a deciduous and evergreen 3–10 m tree with sweet-scented lilac flowers during autumn and spring, dark green leaves and a round-shaped fruit initially green and yellowish when mature (Botha and Penrith 2009). Trees are cultivated in countries with template to warm climates and in Argentina they are easily found in houses and parks as ornamental trees for protection against sunlight and winds.

Melia azedarach has demonstrated to have both pharmacological and toxicological properties. Fruits have been studied for their phytochemical composition which includes melianoninol, melianol, melianone, meliandiol, vanillin, and vanillic acid (Han et al. 1991). Toxic compounds are tetranortriterpens, known as meliatoxins, present in all the parts of the plants but specially concentrated in the ripe fruits (Botha and Penrith 2009). Aqueous and alcohol extracts prepared from different parts of MA have antibacterial (Sen and Batra 2012), antiparasitic (Szewczuk et al. 2006), antifungal (Carpinella et al. 2003), antiviral (Alche et al. 2003), and antioxidant properties (Marimuthu et al. 2013). MA has also been tested for insecticide activity. Vergara et al. (1997) and Carpinella et al. (2003) state that this capability is due to the anti-feeding effect of tri-terpenoids that inhibit food intake capacity, which has been demonstrated in phytophagous insects, thus leading to death and malformations in next generations. Plant extracts prepared from leaves or fruits have been tested on bean weevil (Mazzonetto and Vendramim 2003), mosquitoes (Pérez-Pacheco et al. 2004; Parra Henao et al. 2007) and moths (Rossetti et al. 2008). Some information exists regarding repellent and insecticidal properties on T. infestans (Valladares et al. 1999) but no up-to-date data are available.

Purpose of this work is to present the results of tests performed with hexane extract prepared from fruits of MA considering insecticidal capabilities on different evolutionary stages of Tuta absoluta for a possible economic and easy to implement complement of traditional pesticides used for integrated management of pest.

Plant material and extract preparation

Melia azedarach L. green fruits were collected from mature trees (> 15-yr-old) located in Shahed University Campus, College of Agriculture as described by Chiffelle et al. (2019). Fruits (3 kg) were dried by the dry shade method, and afterwards grinded in a mechanical grain mill to obtain powdered material. The ground powder was poured into Erlenmeyer 500 ml, the volume of the container was increased to 100 ml with hexane (Merck, Darmstadt, Germany) solvent. Then the solution was stirred with a magnetic stirrer (Heidolph, MR 3001K, Schwabach, Germany), at 37°C the first hour, and at room temperature to complete 24 h and then completely covered with foil and parafilm and placed in the refrigerator. After one day, the homogenized mixture was filtered through a Whatman Nº 1 filter paper and centrifuged for 15 min at 1500 rpm to obtain the supernatant (extract). After one hour, the remaining solution was filtered and was placed under the hood in Petri dish for 3–7 hours to complete removal of hexane, and finally pure extract was obtained.

To determine the concentrations and a preliminary test was carried out and first five initial concentrations (bracketing dose) were selected. These concentrations were selected as the upper and lower limit concentrations, which should lead to between 5 and 95% mortality. Then different concentrations of the extract were prepared using logarithmic intervals between the maximum and minimum concentrations and the main experiments was performed.

Insect rearing

Tomato leaves or leaf parts with larvae were collected from infested tomato greenhouses located in Karaj, Pakdasht and Varamin. Iran. After the emergence of adults, T. absoluta moths were collected by suction and released into a transparent polyester jar containing fresh, detached, composite tomato leaf with the cut end fixed in a vial (4 cm ×1 cm) filled with sterile water. The insects were reared in gross chamber at 27 ± 2^oC, 65 ± 5% RH and 16L:8D h photoperiods. The insects were provided with water and energy source (10% sucrose solution) and allowed to oviposit for 24–48 h. If an adequate number of eggs were observed, the infested leaves were placed in an insect-proof rearing cage to allow larval development to second instar. Above all, the infested tomato leaves were placed gently on a potted tomato plant to ensure adequate food availability. Second-larval instars, eggs and pupae were utilized for bioassay experiments.

Contact toxicity of extract on developmental stages of T. absoluta

The egg, the 2nd larval instars and pupa of T. absoluta were utilized to determine the contact toxicity of M. azedarach. To determine the LC₅₀ in the egg stage, five concentrations (60, 144, 524, 1000, 2000 µl/ml) and each concentration in three replications and in each replication of 20 eggs of 24-h old were used. Using the sampler, the required amount of the extract was poured on filter paper (Whatman 42), then the filter papers were dried in laboratory conditions and individually was placed into dishes (8 cm diameter) which their lid was blocked with the parafilm. Distilled water was used for the control treatment. The treated petri dishes were placed inside the germinator at 27 ± 2^oC, 65 ± 5% RH and 16L:8D hours photoperiods. The mortality and hatching of eggs after 24 hours and up to 5–7 days were examined using a light stereoscope microscope.

To determine LC₅₀ in the 2nd larval stages, six concentrations (60, 120, 250, 500, 1000, 2000 µl/ml) and each concentration in three replications and ten 2nd instar larvae in each replication were used. After preparing the desired concentration by means of a sampler by leaf-deep method in the extract was used to determine the toxicity of the extract on larvae. For this purpose, tomato leaf discs (8 cm diameter) were immersed in 50 µl of different concentrations of the extract for 10 seconds. The leaf disks were then dried in the laboratory and transferred individually to petri dishes lined with filter paper moistened with distilled water. Then 10 2nd instar larvae of the same age were placed on each leaf disc in the petri dish their lid was sealed with the parafilm to prevent the larvae from escaping. Distilled water was used for control treatment. The treated petri dishes were placed inside the germinator at 27 ± 2^oC, 65 ± 5% RH and 16L:8D hours photoperiods. Larval mortality was recorded at 24, 48 and 72 hours after treatment (Kim et al. 2002). Then, according to the number of insects killed, the percentage of losses for each concentration was obtained.

To determine LC₅₀ in pupa stage, the same age pupae were needed to do this experiment. To obtain pupae, the leaves containing the last instar larvae of pest were collected and placed in plastic containers with net lids to form pupae. The resulting pupae were immersed in a solution of different concentrations (60, 120, 250, 500, 1000, 2000 µl/ml) of extracts or distilled water (control) for 20 seconds. For each concentration between 15–20 pupae per replicate was considered. After drying, the pupae were transferred to a petri dish and kept until the insects hatched (Park et al. 2002). This experiment was performed in three replications for each concentration. The treated petri dishes were placed inside the germinator at 27 ± 2^oC, 65 ± 5% RH and 16L:8D hours photoperiods. Then, according to the number of lost pupae, the percentage of mortality for each concentration was obtained.

Statistical analysis

All experiments were assigned using completely randomized design. The data obtained from the experiments were analyzed by ANOVA analysis of variance using SAS software. After analyzing the variance of the data, if the data were significant, Tukey's test was used to compare the means. Values of LC₁₀, LC₂₅, LC₅₀ and LC₉₀ with 95% fiducial limits (FL) were calculated, using Probit analysis (SAS Institute 2004).

Contact toxicity of extract on developmental stages of T. absoluta

Egg stage

The results of the egg experiment showed that the application of M. azedarach extract significantly (P < 0.01) led to an increase in the number of killed eggs of T. absoluta (F = 97.69; df = 5; P < 0.01). Also, results showed that mean mortality of eggs was increased significantly compared to the control treatment (Fig. 1). Comparison of the mean by Tukey test showed that the control treatment with 3.3% had the lowest mortality of eggs (α = 0.05). However, in the two initial levels of concentrations (57.54 and 138.03 µl/ml), the mortality (6.8 and 10.3%, respectively) did not show a significant difference with the control (α = 0.05). The mortality of eggs by the extract in the fourth (238.84 µl/ml) and fifth (812.83 µl/ml) levels of the concentration increased significantly and reached 24.12 and 37.89%, respectively. Then, with a growth of 32%, the highest mortality (70.61%) was observed at the maximum concentration of the treatment, where the eggs were exposed to 1949.84 µl/ml of M. azedarach extract (Fig. 1). Analysis of the relationship between applied M. azedarach extract concentrations and mean mortality of eggs showed that a very significant linear correlation (P < 0.001) (Y = 12.67X − 18.83). The coefficient of explanation was equal to 0.87 (Fig. 1).

[Fig. 1]

Larval stage

The results of the 2nd larval instar experiment showed that the application of M. azedarach extract significantly (P < 0.01) led to an increase in the number of killed larvae of T. absoluta (F = 113.23; df = 5; P < 0.01). Also, results showed that mean mortality of larvae was increased significantly compared to the control treatment (Fig. 1). Comparison of the mean by Tukey test showed that in the three initial levels of concentration including control, 59 and 145 µl/ml with 1.23, 7.78 and 8.80%, respectively, the lowest mortality of larvae were observed (α = 0.05), and no significant difference was observed. The mortality by the extract increased significantly at the fourth (347 µl/ml) and fifth (832 µl/ml) levels of the concentration and reached 33.18 and 48.40%, respectively. Then, with a growth of 29%, the highest mortality of larvae (77.65%) was obtained at the maximum concentration of the treatment, where the 2nd instar larvae were exposed to 2041 µl/ml of M. azedarach extract (Fig. 1).

Analysis of the relationship between applied M. azedarach extract concentrations and mean mortality of 2nd instar larvae showed that a very significant linear correlation (P < 0.001) (Y = 14.721X − 22.019). The coefficient of explanation was equal to 0.87 (Fig. 1).

Also, at this stage, the effect of different times (24, 48 and 72 hours) on the effect of M. azedarach extract on the mean mortality rate of 2nd instar larvae of T. absoluta was evaluated. At 24 hours, 21.67%, at 48 hours 29.44%, and at 72 hours it reached 37.41% with a growth of 7.97% and significant difference between the three different time levels (F = 15.98; df = 2; P < 0.01). But the interactions of two factors, concentration and time was not significant (F = 1.09; df = 10; P > 0.05).

Pupal stage

The results of the pupa experiment showed that the application of M. azedarach extract significantly (P < 0.01) led to an increase in the number of killed pupae of T. absoluta (F = 39.32; df = 5; P < 0.01). Also, results showed that mean mortality of pupae was increased significantly compared to the control treatment (Fig. 1). Comparison of the mean by Tukey test showed that the control treatment with 13.33% and concentration of 1 µl/ml with 25% mortality were not significantly different. The mortality of pupae the second level (3.3 µl/ml) increased significantly and reached 57.5%. Then with a growth of 38% in the third (10.95 µl/ml), fourth (36.25 µl/ml), and fifth (119.99 µl/ml) levels with 95.5, 100 and 100%, respectively mortality was increased significantly with no significant difference between these three levels (Fig. 1).

Analysis of the relationship between applied M. azedarach extract concentrations and mean mortality of pupae showed that a very significant linear correlation (P < 0.001) (Y = 19.81X − 4.61). The coefficient of explanation was equal to 0.87 (Fig. 1).

Bioassay results of LC₁₀, LC₂₀, LC₅₀ and LC₉₀ of M. azedarach extract on stages

The insecticidal activity of hexane extract from M. azedarach was investigated. The extract had a remarkable insecticidal activity, and the results are shown in Table 1. The egg, larva and pupae mortality were observed against the TLM, T. absoluta. The ovicidal activity were LC₅₀ = 948.93µl/ml and LC₉₀ = 10353.60 µl/ml, the larvicidal activity were LC₅₀ = 346.72 µl/ml and LC₉₀ = 3581.91 µl/ml, and the pupicidial activity were LC₅₀ = 1.75 µl/ml and LC₉₀ = 8.8 µl/ml after 7 days, 72 hours and 7 days of exposure period, respectively. Also, the value of chi-square in the probit table shows the appropriate fit of the data. This difference in LC₅₀ of different stages shows the difference in susceptibility of different stages (Table 1).

Table 1

LC₁₀, LC₂₀, LC₅₀ and LC₉₀ values of *M. azedarach* hexane extract against different stages of the tomato leaf miner, *T. absoluta*
Stage	n	LC₁₀^* (µL/mL )	LC₂₀^* (µL/mL )	LC₅₀^* ( µL/mL )	LC₉₀^* ( µL/mL )	slope ± SE	df	χ²
Egg	300	86.97 (44.71–133.92)	197.54 (127.02–273.34)	948.93 (690.02–1452.09)	10353.6 (5156.7–32514.5)	0.54 ± 0.07	3	3.664^n.s.
2nd larval instars	180	6.616 (5.295–7.266)	6.616 (5.295–7.266)	7.876 (7.138–8.635)	10.271 (9.196–13.737)	2.891 ± 11.114	3	0.221 ^n.s.
Pupa	180	0.151 (0.002–0.220)	0.151 (0.002–0.220)	1.865 (1.566–2.165)	2.839 (2.394–4.160)	1.684 ± 7.028	3	0.412 ^n.s.
Note: n = number of insect; χ² = chi-square; df = degree of freedom; * = Fiducial limits; n.s.=non-significant

[Table 1]

The results showed that the effect of M. azedarach extract on pupae was more than the eggs and 2nd instar larvae. The LC₅₀ value of pupal stage with 1.75 µl/ml was much lower than egg stage with 948.93 µl/ml and 2nd instar larval stage with 346.72 µl/ml which indicated that this stage was more susceptible than the other two stages. The pupal stage, is covered with only one layer of pupal shell and is not able to move to escape the extract, so is more composed compare to the larvae where it is in contact with the extract, but the ability to select and escape from the extract. In the egg stage, the presence of chorion caused much less permeability than the other two stages. This extract had the highest percentage of mortality on the cabbage white butterfly, Pieris brassicae L. larvae compared to other extracts. The effect of 2.5% concentration of aqueous extract showed that this extract can cause up to 28.6% larval mortality after 24 hours (Sharma and Gupta 2009). In previous studies, the effect of M. azedarch aqueous extract on T. absoluta pupae extended the growth period and reduced the survival rate in compare to control. Also, it had a decreasing effect on the pupal weight of males compared to the control, but had no effect on the weight of the female pupae. Comparison between larval and pupal data showed very similar values, which is a rare result. According to Rodríguez and Vendramim (1998), the effect of insecticides on insect residues in the larval stage was more severe than in the pupal stage, because it is at this stage that the insect swallows chemicals (Brunherotto and Vendramin 2001).

Consistent with the results of this study, Abou-Fakhr Hammad et al. (2019) also pointed to the significant lethal effects of M. azedarch extract on T. absoluta. It has been suggested that the mortality of extract is due to the systemic action of this extract, which leads to penetration into the egg and lethality. Also in Abou-Fakhr Hammad et al. (2019) study, the lethal effects of M. azedarch extract on T. absoluta were evaluated similar to the effects of neem extract.

The results of the present study suggest that the M. azedarch extract can be used to protect crops against the extensive damage caused by T. absoluta larval feeding. Since the plant is easily grown and widespread, resource availability should not be an issue and the crude extract of M. azedarch can be used as a crop protectant for local use in Iran and many other regions of the world.

Our study demonstrates that the hexane extract of M. azedarch fruits was the most active toxicant to eggs, second instar larvae and pupae of T. absoluta. This organic extract have potential for development as botanical insecticide. However further studies are needed, especially to evaluate the cost/benefit ratio regarding its use in the integrated pest management schemes and its effects on non-target organisms.

Acknowledgements

This work was supported by the Shahed University of Iran and carried out in Department of Plant Protection, Faculty of Agricultural Sciences.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

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Evaluation of the chinaberry extract against the tomato leafminer, Tuta absoluta (Merick) (Lepidoptera: Gelechiidae) in vitro

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