Effectiveness of Three Bio-Rational Products and a Traditional Insecticide against Thrips spp . and Bemisia tabaci Attacking Tomato Fields in Kafr El-Sheik Governorate , Egypt

Destructive effects of conventional insecticides on environment have created a necessity to introduce bio-rational products in pest control programs. Effectiveness of bio-pesticide (Beauvaria bassiana), natural oil (anti-insect), a botanical extract (nimbecidine) and malathion insecticide was evaluated against Thrips spp. and Bemisia tabaci attacking tomato in Kafr El Sheik, Egypt. The trial was conducted during two successive seasons; 2017-18 in a total area of 4912 m cultivated with tomato cultivar zero 42. The experiment was set up in a randomized complete block design with five replications for each treatment. Yellow sticky traps were used to monitor population of both pests before and after spraying, in addition, their numbers on plants were counted. Results revealed that highest control rates of both pests were recorded after the fourth day of each spraying. Long inter-applications periods decreased effectiveness and the greatest control resulted when three consecutive sprayings were applied. Malathion achieved the highest suppression of both pests. Within the bio-rational pesticides, nimbecidine gave the greatest thrips control whereas products showed no significant difference for whiteflies. The study recommends those bio-rational compounds to join Integrated Pest Management programs of both pests in Egypt, taking into consideration spraying for 3 consecutive times with at least 5 days intervals.


Introduction
Tomato (Solanum lycopersicum) is a major world food crop; it is commercially grown in 159 countries.The top five tomato producers are China, India, USA, Turkey and Egypt, representing about 60% of the world production [1].Based on a comparison between 152 countries in 2013, Egypt was ranked the highest in tomato consumption per capita per year with 97.8 Kg.Therefore, the cultivated tomato area in Egypt considerably increased during the last two decades where it spread from the extreme North to the extreme South and approximately 223 thousand ha are cultivated with tomatoes.The majority of this area is concentrated in the Delta region [2] and total tomato production reached 7.94 million t in 2016 [3].
Tomato is subject to attack with scores of insect pests and diseases that affect its production [4].Thrips and whiteflies, belonging to the piercing sucking insects, cause severe damage to tomato crop by transmitting virus disease rather than direct feeding.The cultivation of tomato and availability of alternate hosts encourage the development of pest pressure round the year.The whitefly Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) is considered a major insect pest for tomato crop infesting all stages throughout cropping season [5].It is created by the over-use of pesticides that have killed off its natural enemies; for this reason the current study is investigating new and safe alternatives to control this pest.Whiteflies go round in hordes; suck plant sap resulting in a yellow mottling on the leaf surface, cause leaf loss, wilting and stunting.Not only do they feed on plants, but they also produce honey dews which spoil the plants' appearance, attract ants, which interfere with natural enemies activities that might control whiteflies [6].Yield losses due to direct and indirect damage caused by whiteflies were reported to the extent of 20% to 100% [7].
On the other hand, thrips is another annoying pest that attacks tomato and reduces their marketability [8] [9].While some species act as major vectors of viral plant diseases other damage tomatoes through their different feeding methods.Thrips feeding can stunt plant growth and causes damaged leaves to become papery and distorted, develop tiny pale spots and drop prematurely.Infested terminals may discolor and become rolled.They are difficult to control, therefore, it is recommended to follow an integrated program that combines the use of good cultural practices, natural enemies, and most selective least-toxic insecticides [10].
During the past three decades, efforts have been made to reduce the risk of human exposure to pesticides, especially insecticides.However, as a result of heavy selection pressures, caused by the extended, frequent and over-use of conventional insecticides, population of the piercing sucking insects has developed resistance worldwide [11].Although malathion (an organophosphorus insecticide used against those pests) has a significant importance in Egypt due to its wide distribution, persistence and extensive use, yet, it had caused several environmental problems in addition to severe tomato damage [12].Using an insecticide-only strategy faces major challenges, thus, there is a need to develop and introduce bio-rational insecticides that are highly selective, eco-toxicologically safe and have novel modes of action to be integrated in pest management programs [13].Bio-rational pesticides include several compounds such as soap, horticultural oil and neem.The neem-based pesticides are reported to control young nymphs of thrips; however, more information is needed to formulate an effective, low-cost and eco-friendly pest-management strategy that can be adopted sustainably in the existing agricultural framework [9].In addition, Beauvaria bassiana (Balsamo Crivelli) is a promising bio-control agent that can be integrated in the control strategy of piercing sucking pests [14].This fungus is safe to plants, humans and animals, as well as non-targeted insects and can kill thrips at all life-cycle stages [15] [16].
Consequently, a comparison between three bio-rational pesticides (a bio-pesticide, natural oil and a botanical extract) and malathion (as a conventional insecticide) was conducted against two important pests attacking tomato plantation in Egypt, i.e. whitefly and thrips, during 2017-18 seasons.The aim was to identify the most effective bio-rational pesticide for each target pest, the effective number of spraying times and post-treatment highest control days.The identified effective bio-products are recommended to join tomato Integrated Pest Management (IPM) programs under the Egyptian conditions hoping to reduce the severe effect of pesticides.
A field study was performed in a private farm in Qulien district, Kafr El Sheikh Governorate, Egypt, during Nili tomato plantation in two seasons, i.e. 2017-18 under a mean temperature and relative humidity of 28.11˚C ± 3.6˚C and 66.38% ± 0.82%, respectively, to compare between 3 bio-rational pesticides and one conventional insecticide on both thrips and whiteflies.A total area of 4912 m2 was cultivated with tomato cultivar zero 42 seedlings in mid-May of each season.

B 2.2. Bio and Conventional Pesticides
A bio-pesticide, natural oil, a botanical extract, in addition to a conventional chemical insecticide was used.

Experiment Design
The experimental area was divided into 5 plots each of 608 m 2 /treatment (16 × 38 m), laid in a randomized complete block design.Each plot was divided into 5 replicates.A distance of about half meter was left between plots and a distance of 30 cm was left between plants.Each plot was planted by about 715 tomato seedlings (=5000 plant/feddan where 1 feddan = 0.42 ha).All agronomic practices were maintained constantly when required.Each treatment was adjusted according to the plot size, calibrated and sprayed.A twenty liters volume sprayer was used and spraying was carried out three times during the season, i.e.June, 8 th and 24 th and July, 10 th .

Results' Recording
Numbers of both pests were recorded before and after spraying.Two methods were followed in results' recording: 1) Yellow sticky traps Yellow sticky traps measuring 16 × 17 cm were used for monitoring pests' population before and after treatments during the whole period of the study.Five traps were used in each plot including the untreated control plot (1 trap/replicate).Traps were hanged horizontally 30 cm above the top of the plants reversing wind direction and adjusted vertically whenever the crop attained additional growth.Numbers of insects caught on the sticky traps were counted one day before the first application and 4, 8, 12 and 16 days after each application.Upon the collection of the sticky traps, they were wrapped for protection, transferred to the laboratory for sorting, identifying, counting and meanwhile replaced with new ones after each inspection date.
2) Sampling For sampling, 10 plants were randomly selected and 10 leaves from each plant were investigated to detect the number of thrips and whiteflies.The sampling was done in five steps including one day before treatment, 4, 8, 12 and 16 days post treatment.

Statistical Analysis
Results were statistically analyzed using SPSS statistical package according to the analysis of variance (ANOVA).LSD was chosen to determine significant differences among various treatments at p < 0.05. the two seasons (2017-18) before spraying of nimbecidine, anti-insect, bio-power, malathion and in control plot were 90, 92, 94, 95.7 and 93.3, respectively.To determine the effectiveness of the products used in controlling thrips; sticky cards were monitored every 4 days and results were recorded for 4 inspection dates.This technique was also followed by Gill et al. [17].Results showed that there was a significant difference among the four inspection days in each of the 3 applications (Table 2).The least number of thrips (best control level) was recorded immediately after spraying, i.e. 4 days post treatment.First spraying mean numbers of thrips were 0.8 ± 0.8, 0, 3.6 ± 1.6 and 0 in nimbecidine, anti-insect, bio-power, and malathion treatments, respectively.Moreover, when spraying for the 2 nd time, results recorded on the 1 st inspection date were almost the same as those recorded in the first application, i.e. 0.8 ± 0.37, 0, 3.4 ± 1.3, and 0.4 ± 0.4, respectively.All mean numbers recorded after 4 days of the third spraying dropped to zero, except for the bio-power that recorded a mean number of 0.8 ± 0.37.ANOVA one analysis showed significant differences between the inspection dates for the different sprayed product in most cases (LSD for each product is calculated and listed in Table 2).All treatments were significantly superior over the untreated control as presented in the same table.
Repeating spraying resulted in raising products effect where each time the bio-rational pesticides and the malathion were applied, numbers of thrips stuck to the traps decreased till it reached the least records after the third application indicating more effectiveness, as shown in Figure 1 were, in general, much higher than those caught on the first season, but still, results of the second season confirmed the data obtained in the first season.Thrips recorded their lowest mean numbers on the yellow sticky traps on the fourth day post treatment in the 3 spraying times, as shown in Table 3.
Mean numbers of thrips decreased form one application to the next in all the experimental plots till it reached the lowest numbers on the third application as was found during the first season.The average mean numbers recorded within the bio-rational products after the 3 rd spraying were as follows: nimbecidine    2(a), a complete reduction occurred in the pest population after application, either for the three used bio-rational products or for malathion.Comparing the mean numbers of thrips stuck to traps before and after application, it was found that nimbecidine treatment decreased thrips mean numbers from 90 to 11.64 (7.7 times less), while the mean numbers caught in case of malathion dropped from 95.7 to 9.95 (about 9.6 times less).Each of the anti-insect and bio-power compounds caused 7.2 and 6 times reduction in pests' numbers, respectively.These results prove within the bio-rational products nimbecidine achieved the highest control level.
2) On tomato plants Investigation of thrips numbers on plants after the use of the tested products was also carried out during the two seasons to cover all pest stages that are not capable of reaching the traps and to confirm the results obtained from traps experiment.Figure 2(b) shows that all 4 treatments decreased thrips numbers on plant's leaves.Mean number of thrips before application were 35, 50, 61 and 44 for nimbecidine, anti-insect, bio-power and malathion, respectively.After spraying malathion gave the best thrips control followed by both nimbecidine and anti-insects as was found previously in traps test and mean numbers were; 2 ± 0.6, 6 ± 2.1 and 6 ± 2, respectively.There was a significant difference between malathion, on one hand, and both nimbecidine and anti-insect on the other hand (LSD 0.05 = 2.75).Moreover, no significant difference appeared between the bio-power and the control confirming again that bio-power is a weak product for thrips control.

Whiteflies' Population Pre-Application
The general mean numbers of B. tabaci on the yellow sticky traps before application, for the two seasons (2017-18), in the 5 treatments, i.e. nimbecidine, anti-insect, bio-power malathion and control treatments, were 17.1, 18.8, 16.8, 17.3 and 17.13, respectively.These numbers reflect adequate degree of uniformity in the whiteflies' population before applying any of the products.4).Whitefly's mean numbers increased slightly when the 3 rd spraying was carried out, except for the anti-insect product.These results indicate that the best control levels appear after 4 days of spraying followed by a fluctuation in pest numbers that differed from one treatment to another.B. tabaci numbers in control plot were always higher than all other treatments.
Repetition of spraying did not always cause reduction in B. tabaci population as shown in Figure 3  all plots (Table 5).Moreover, mean number of B. tabaci decreased from one application to the next in all the experimental plots till it reached its minimum number in the third application.In case of nimbecidine; mean number of the pest decreased from 13.45 ± 4.15 to 2.75 ± 0.92 and then to 2.25 ± 2.48 in the 3  As shown in Figure 4(a), there was a reduction in the general mean numbers of whitefly recorded before and after applications for all the used bio-rational products and the malathion pesticide.The mean numbers of B. tabaci caught in case of the malathion decreased from 17.3 to 2.96 (about 5.8 times less), while mean insects' numbers stuck to the traps in case of anti-insect and bio-power decreased from 18.8 to 4.01 (4.7 times less) and 16.8 to 4.19 (4 times less), respectively.Finally, nimbecidine caused the least reduction in whitefly's numbers, i.e. 17.1 to 5.13 (3.3 times less).These results highlighted that among the tested products malathion proved to be the best compound against B. tabaci where it caused the highest suppression in pest population, while, no significant differences appeared among the three bio-rational products in controlling this pest (LSD at 0.05 was 1.5).

2) On tomato plants
As shown in Figure 4(b), a complete reduction occurred after spraying where whitefly's numbers before application recorded 8, 13, 15 and 21, for nimbecidine, anti-insects, bio-power and malathion, respectively.Results after application of the products showed that malathion gave the best control level; whereas, no significant differences were recorded among the bio-rational products (LSD at 0.05 = 1.30).Malathion pesticide recorded the lowest mean number (1.08 ± 0.43 insects), whereas bio-power recorded a mean number of 1.83 ± 0.87 and each of the anti-insect and nimbecidine recorded a general mean number of 2.17 ± 1.47 and 2.67 ± 1.1, respectively.On the other hand, significant differences were recorded between the control treatments and all the tested products where control recorded a general mean number of 3.67 ± 1.

Discussion
Tomato crop is subjected to severe damage caused by the piercing sucking insects, which is considered of the most serious pest groups all over the world.
Yield losses due to direct and indirect damage caused by whiteflies, for example, can reach 100% [8].The current study aimed to find some alternatives to be used in controlling such pests.
Fluctuations in thrips numbers obtained during the different inspection dates, in some experimental plots within the two seasons, could be explained according to Gill et al. [17] who stated that thrips adults fly readily and can be carried on wind currents and move from sprayed to unsprayed areas as well.Concerning inter-application periods, our results did not correspond to what was found by Wagh et al. [18] who stated that spinosad, as one of the bio-rational natural compound, was very effective against whitefly and thrips on tomatoes during ten days after spray interval.However, our work coincided with a research carried out at Cornell University, stating that 5-day application intervals are more effective than 7-day intervals [17].In the current study the highest control of both thrips and whitefly was always obtained after the 4 th day of each application, and therefore, the idea of increasing the inter-application periods up to 16 days was not effective, as it was too long.Accordingly, we recommend that time between applications should not exceed 5 days to achieve better control levels.
In pest control, it is also important to decide how often a product should be used.The current results recommend that three consecutive spraying are necessary to achieve the best control.These findings highly corroborates the investigation of Emami [19] where he used four organically-farming insecticides, among which was the nimbecidine extract, and assured that applying the products for 3 times gave excellent control.Therefore, repeating applications may be necessary for better pest control [20].Moreover, Magsi et al. [21] supported our recommendation where they stated that applying different synthetic insecticides for 3 consecutive times against B. tabaci decreased pest population in all the tested insecticides.
According to our study malathion pesticide proved to be the best product among the tested chemicals where it achieved the highest control rates in both thrips and whitefly.However, although systemic insecticides may be highly effective, still they can have negative impacts on beneficial insects and pollinators [20].Not only that the pesticides kill natural enemies, but both thrips and whiteflies quickly build up resistance to them [12].On the other hand, Horowitz and Ishaaya [14] stated that bio-rational insecticides are good alternatives or supplemental forms of pest control and they are to be used in the IPM programs.
In addition, according to the US Environmental Protection Agency (EPA), bio-rational pesticides display minimal risk to the environment, break down H. Adel et al.
quickly, have minimal residues, safe to applier and relatively small amounts are needed for successful control [22] [23].In the current investigation, within the bio-rational pesticides, nimbecidine gave the highest control percentage in case of thrips, while in case of whitefly both bio-power (B.bassiana) and the anti-insect caused the highest control levels followed by nimbecidine.Difference in the effectiveness of used bio-rational products against the study pests could be attributed to their age specific toxicity, variant modes of action, the developmental stage of the pest and its location [24].

Conclusion
In conclusion, nimbecidine oil, bio-power and anti-insect are available promising products as alternatives or supplements to chemical insecticides in controlling thrips and whiteflies; one might choose two of them to alternate between.Therefore, it is recommended to integrate those three bio-rational compounds in the IPM programs of both piercing sucking insects in Egypt, provided that applications' numbers, period between sprayings and the suitable type of product, are taken into consideration.In addition, application's methodologies and concepts should be transformed to farmers to encourage their use and adoption.

B Acknowledgements
Thanks are due to our colleagues from the ARC, Egypt, Prof. Dr. Hashem Ibrahim for his assistance in the statistical analysis of this research, Prof. Dr. Maher Noman for revising and editing the final version of this manuscript and the authors also appreciate the administrative assistance provided by Miss Rehab El Sayed.

3 . 1 .
Thrips Spp. 1 5 B 3.1.1.Thrips Population Pre-Application Results showed an acceptable degree of uniformity in the thirps's population before application.Overall mean numbers of thrips on the yellow sticky traps for H. Adel et al.

Figure 1 .
Figure 1.Mean numbers of Thrips spp.caught on yellow sticky traps for the four treatments and the control during each of the three applications in season 1 (a) and season 2 (b).

Figure 2 .
Figure 2. General mean number of Thrips spp.caught before application (B.A) and after application (A.A) of the tested products on both the yellow sticky traps (a) and tomato plants (b) during the two seasons.
(a).The three consecutive applications of nimbecidine gave almost the same results with no significant difference among the applications, i.e. 4.25 ± 1, 4.40 ± 1.63, 4.40 ± 0.67, respectively.However, anti-insect and malathion treatments showed continuous reduction in B. tabaci numbers from one application to the other as presented in the same figure.

2 )
Second season (2018) Results of the second season (2018) confirmed the data obtained during the first season (2017), where the mean number of whitefly caught on the yellow sticky traps was the least on the fourth day post treatment and this was found in DOI: 10.4236/as.2018.9121081546 Agricultural Sciences H. Adel et al.

Figure 3 .
Figure 3. Mean numbers of B. tabaci caught on yellow sticky traps for the four treatments and the control during each of the three applications in season 1 (a) and season 2 (b).

Figure 4 .
Figure 4. General mean numbers of B. tabaci caught before application (B.A) and after application (A.A) of the tested products on both the yellow sticky traps (a) and tomato plants (b) during the two seasons.

Table 1 .
Table1presents the four products, their trade Pesticides used in the experiments and their information.

Table 2 .
Mean numbers of Thrips spp.caught on the yellow sticky traps in the different treatments during season 1 (2017).

Table 3 .
Mean number of Thrips spp.caught on the yellow sticky traps in the different treatments during season 2: (2018).

1.3. Combined Analysis of Thrips Results for Both Seasons before and after Spraying 1
) On yellow sticky traps As shown in Figure

1 9 B 3.2.2. Best Results Obtained and Effect of Repeating Spraying
0.24, 0.20 ± 0.2, 0.60 ± 0.6, and 0.40 ± 0.24 for the 4 products (A, B, C and D) respectively.It was also noticed that in the second application no significant differences appeared between the 4 th and 8 th days of spraying of all products, LSD at

Table 4 .
Mean numbers of Bemisia tabaci caught on the yellow traps in different treatments during season 1: (2017).
A: Nimbecidine; B: Anti-insect; C: Bio-power; D: Malathion; E: Control 0.05% for all treatments during the whole experiment periods are presented (Table

Table 5 .
Mean numbers of Bemisia tabaci caught on the yellow sticky traps in different treatments during season 2: (2018)., respectively, which differs from the first seasons where the mean numbers did not show significant differences among the 3 applications as discussed above.The three other products, i.e. anti-insect, bio-power and malathion caused high reduction in insect mean numbers recorded on the traps as by applications