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Role of photosensitizer in control of mealybug and scale insects (Homoptera: Margarodidae and Diaspididae), in comparison with conventional insecticide
Bulletin of the National Research Centre volume 48, Article number: 92 (2024)
Abstract
Background
Two photosensitizer agents were used: rose bengal and eosin alone and mixed with soap. Two other chemical compounds were used: active cable oil and soap. All these materials were compared with malathion as a conventional insecticide. The Egyptian mealybug Icerya aegyptiaca attacking ornamental–medicinal plants (acalypha and rose shrubs) and the black Parlatoria scale Parlatoria ziziphus attacking sour orange were evaluated against the tested materials.
Results
The results obtained suggest that soap, rose bengal mixed, eosin mixed, malathion and active cable oil revealed potency in reducing the population of I. aegyptiaca by 57.24, 87.25, 75.62, 98.71 and 59.91%, respectively, on rose; and by 54.91, 82.64, 62.48, 96.67 and 48.13%, respectively, on acalypha shrubs; their potency on insects showed a significant difference on infested rose than on infested acalypha. The tested compounds revealed lower potency in reducing the population of P. ziziphus than malathion. Reduction percentages were 35.43, 40.39, 34.25, 91.81 and 28.21%, respectively. The accumulation potency of the tested compounds on two insects collectively, without regard to insect species, stages or infested plant species, was assessed at 51.49, 66.18, 55.86, 94.37 and 44.69, respectively. The obtained results confirmed that malathion was the most effective agent against both tested insects, followed by rose bengal mixed with soap, eosin mixed with soap, soap alone and active cable oil.
Conclusions
The obtained results showed that rose bengal (as a photosensitizers) mixed with soap can be used as a promising agent against all tested insects.
Background
Egyptian mealybugs Icerya aegyptiaca (Douglas) and the armored scale (black Parlatoria scale) insect Parlatoria ziziphus (Lucas) are minute insects. It was difficult to detect an infestation with it at the beginning. They attack a wide range of ornamental and fruit plants, such as rose; acalypha shrubs and citrus trees, causing severe damage to these hosts (Liu and Shi 2020; Zhou et al. 2022). This damage grade comes from yellowing, drying leaves, loss in fruit yield and finally the drying of branches or drying of trees completely. This damage is a result of sucking sap by insects, injection of toxic enzymes into plant tissues, transmitting plant disease and/or secreting honeydew (Bragard et al. 2023).
Conventional scalicides used in controlling these insects repetitively and randomly in the last decades, produced insect resistance and environmental hazards, so they became harmful and useless (Dassanayake et al. 2021). At the current time, researchers are interested in finding alternative materials (Soaps, neem products, essential oils and light-activated molecules) for controlling scale insects and mealybugs (Yassin and Emam 2020; Mwanauta et al. 2021; Zhou et al. 2022). Soaps have been used in insect control for more than 200 years. Recently, demands to use soaps as insecticides have increased because of its efficiency on insects, easier use and safer on the environment than many of the current insecticides presented today. Aniwanou et al. (2021) demonstrated that soap and detergent sprays can be used effectively in reducing certain insect populations on ornamental plants for their favorable properties in comparison with synthetic organic insecticides. Curkovic (2016) mentioned that soaps and detergents are used in controlling insect pests belonging to families: Diaspididae, Coccidae, Pseudococcidae, Aleyrodidae, Aphididae, Thripidae and others. Reimer and Beardsely (1992) revealed that insecticidal soap spray against the green scale Coccus viridis (Green) (Coccidae) at 0.8% V/V caused a significant reduction in its population by ~ 50% at 4 weeks after spraying on coffee trees. The results found that the insect population level on treated trees increased gradually and returned to the same level that occurred before spraying (such as in control trees) after 106 days of treatment. Ashu et al. (2023) found that soap was used as a synergistic agents to increase the toxicity of some insecticides such as acetamiprid, clothianidin, imidacloprid, thiamethoxam, permethrin and deltamethrin against Anopheles mosquitoes. Porusia et al. (2019) found that soap was very effective against German cockroaches, Periplaneta americana at 2% concentration.
Light-activated molecules (photosensitizer dyes) such as rose bengal, eosin, methylene blue, phloxin and xanthene derivatives were examined as insecticides against larvae of Anopheles spp., Aedes spp and Musca domestica ( Diptera: Muscidae) and Hylemya antiqua (Meigen) ( Diptera: Anthomyidae) (Younis et al. 2021). Martins-Costa et al. (2022) consider a photopheresis system a “combination product” comprising two regulated components: a drug (photosensitizer) and a device (leukapheresis machine). Photosensitizers absorb all the UV in sunlight; and then become active and effective on insects even at very low doses, destroying several target molecules in the cell (Lima et al. 2018). Pieterse et al. (2023) used photosensitizer agents and oils against flower thrips (WFT), Frankliniella occidentalis. The results indicated that the photosensitizer decreased the WFT more than mineral oil applied alone. Ahmed et al. (1985) reported that eosin and methylene blue may be toxic to Spodoptera littoralis larvae, only larval death was observed (50%) when the high concentrations of these two compounds were used (483 and 884 μgm L−1), respectively. Many authors reported that photosensitizers must be used in a mixture (rose bengal and erythrosine), (eosin-methylene blue) and (hematoporphyrin and aluminum phthalocyanine) for more efficiency against Anopheles Aedes, S. littoralis and B. tabaci (EL-Bendary and El-Helaly 2022).
Malathion was able to reduce the population of Icerya aegyptiaca by a percent ranging between 99.5 and 100% (Salem et al. 2009), and this percentage was 85.04% in a population of Aulacaspis mangifera (Salem et al. 2011). Mohanny et al. (2022) found that malathion was very effective against I. purchasi under laboratory conditions. The LC50 was 0.24 ppm. Olabiyi et al. (2022) used malathion as a comparison agent against Hibiscus mealybugs, Nipaecoccus viridis.
This work aims to focus more light on the potency of soap alone; and soap mixed with rose bengal or eosin on both I. aegyptiaca and P. ziziphus in comparison with malathion and active cable-2.
Methods
Experimental sites and infested plants
This work was carried out at Qalyubia Governorate (situated north of Cairo in the Nile Delta region), Giza, Garden of Moltaqa El-Mobdeieen, Egypt. This area was about 15 feddan (fed. = 4200m2) of shrubs of Acalypha spp. and Rose spp. Which was planted in beds, each one had an area of about 5X9 m2 and was heavily infested with the Egyptian mealybug Icerya aegyptiaca. In Qalubeia, among the orchards of the Training Center for Management Development and Horticulture at Barrage district, the sour orange orchard, Citrus aurantium with an area of 2.5 fed., and is 55 years of age; trees are heavily infested with the armored scale insect (black Parlatoria scale), Parlatoria ziziphus (Figs. 1, 2 and 3). Six beds of both acalypha and rose shrubs, as well as 18 trees of sour orange were chosen to conduct six treatments by spraying tested compounds.
Tested compounds
1- Soap: consist of long-chain fatty acids (10–18 carbon atoms) was sprayed at a concentration of 7% (the recommended concentration according to Curkovic 2016).
2- Photosensitizer compounds.
A- Rose bengal mixed with soap (Rbm) (Rose bengal is an organic potassium salt that is the dipotassium salt of 2,3,4,5-tetrachloro-6-(2,4,5,7-tetraiodo-6-hydroxy-3-oxoxanthen-9-yl)benzoic acid. It has a role as a fluorochrome and a histological dye.
B. Eosin mixed with soap (Em).
Both rose bengal and eosin were obtained from Aldrich as commercial powder and imported by the International Center for Importation.
Soap was tested alone against the two tested insects and was tested by mixing with rose bengal and/or mixed with eosin Lima et al. (2018)
3. Mineral oil: Petroleum original compound “Active cable-2” was sprayed at a concentration 1%.
4. Conventional insecticide belonging to organophosphorus compounds “Malathion 57% EC” was sprayed at recommended concentration of 1.5%.
Treatments, sampling and inspecting
Heavily infested shrubs of Acalypha Spp. and Rose spp. with the mealybug I. aegyptiaca were sprayed with soap, rose bengal mixed with soap, eosin mixed with soap, malathion and active cable-2. Each one of the six treatments was replicated three times on three beds planted with each of the infested plants; each of the six beds had an area of about 5 × 9m2. Each replicate was performed on plants occupying a 5m2 area/bed. The same treatments were conducted on heavily infested 18 trees of sour orange with the armored scale insect P. ziziphus. Three applications were done, and one was weak interval.
Spraying was applied using an automatic sprayer motor “knapsack” (volume 12 L). A sample of 30 leaves was taken from each treatment/tested plant on the following dates: directly before spraying; and after spraying by one, two and three weeks. The sample size was 180 leaves from each one of the tested plants. Samples were transferred into the laboratory and inspected using a Binocular microscope. Assessment of the potency of tested compounds against mealybug and scale insects depends on counting the still-live individuals of females and nymphs of each insect.
Data analysis
The percentage of reduction in the live females and nymphs population was calculated using the Henderson and Tilton formula (1955). The average percent of reduction in each insect was calculated; the net potency/compound regardless of insect species or plant species was considered. Mean counts of mealybug and scale insect pre- and after spraying were subjected to ANOVA at a 5% level of significance using Aho (2019). Data on the sale insect were subjected to logarithm transformation before ANOVA; in case of significance calculated F value, the least significant difference (LSD) at P = 0.05 was calculated.
Results
The potency of tested compounds against mealybug insects during the first season of treatment
1- Against the females population
Data in Tables 1 and 2 show that females of Icerya aegyptiaca attacking rose shrubs responded to the potency of tested compounds such as soap, rose bengal mixed (Rbm), eosin mixed (Em), malathion (Mt) and active cable oil (Ac) during the two seasons. Table 1 shows that the percent of reduction in its population equals 58.88, 86.85, 72.3, 99.0 and 55.78%, respectively. Females population attack acalypha shrubs responded to the same compounds by revealing reductions equal to 48.35, 76.87, 55.46, 93.33 and 26.22%, respectively. This indicates that photosensitizer mixed with soap (rose bengal mixed) was more potent in reducing female population than eosin mixed. It reduced the population by (an average of 81.86%) for two shrub species (this average was calculated as follows: 86.85 + 76.87/2 = 81.86%), this average was higher than that caused by eosin mixed (63.88%) on both shrub species. Both of these compounds had more potency on females than soap alone or active cable oil, which reduced the population by averages of 53.62 and 41.0% on rose and acalypha together, respectively. But previously, percent and reduction averages were lower than those obtained by malathion 99.0 and 93.33% on rose, and acalypha, respectively (Table 1). Females counts only on acalypha shrubs had highly significant values where F values are 4.74** and 6.05** in pre-spraying and after spraying, respectively; only female counts after spraying had significant differences between treatments, referring to the potency of tested compounds in reducing the female population to significant levels.
2- Against the nymphs population
Data in Table 1 show that the nymphs population of I. aegyptiaca attacking rose shrubs responded to the potency of soap, rose bengal mixed, eosin mixed, malathion and active cable oil by reducing its population with 55.6, 87.64, 78.93, 98.47 and 64.03, respectively, and with 61.46, 88.4, 69.5, 100 and 70.03%, respectively, on acalypha shrubs. This indicates that rose bengal mixed was more potent in reducing nymph population (average 84.95%) than eosin mixed (average 69.05%) on both shrub species; both two compounds had more potency on nymphs than soap alone and active cable alone which reduced the population by averages 58.58 and 51.52% on both shrubs together.
But malathion revealed the highest potency on nymphs by reducing it by 98.47 and 100% on rose and acalypha, respectively (Table 1). Statically, nymphs count after spraying on rose shrubs between sprayed treatments and control. The numbers of nymphs after spraying of acalypha had a highly significant values F= 27.06 and a significant difference between treatments LSD= 7.06; this means that the tested compounds were able to reduce nymphs population to significant levels.
The potency of tested compounds against mealybug insect during the second season of treatment
Against the females population
As mentioned in Table 2 after the third application of Rose spp., the highest reduction percent on I. aegyptiaca population was caused by rose bengal mixed (rbm) (98.3%) followed by malathion (mt) (97.36%), eosin mixed (Em) (90.72%), soap (60.03%) and active cable (50.1%).
On the other hand, the efficacy of these compounds with Acalypha spp. varied. The highest reduction was carried out with malathion (90.96%) followed by rose bengal mixed (78.05%), eosin mixed (59.76%), soap (53.77%) and active cable (36.41%).
Against the nymphs population
The results in Table 2 showed that the tested compounds have a great influence on the nymph of I. aegyptiaca in both Rose spp. and Acalypha spp. After the third application of Rose spp. of the tested compound, the I. aegyptiaca population was reduced in different proportions. Malathion was the most effective followed by rose bengal mixed, eosin mixed, active cable and soap. The percent reduction were 94.75, 89.23, 75.33, 66.42 and 55.18%, respectively. The average of reductions showed that malathion was the most effective compared with the other tested compounds. The total reduction of I. aegyptiaca population on Rose spp. were 95.97, 93.78, 83.03, 58.26 and 57.61% for malathion, rose bengal mixed, eosin mixed, active cable and soap, respectively.
The corresponding results for Acalypha spp. were 97.89, 89.22, 70.59, 72.7 and 66.26%, respectively. The average reductions were 94.43, 83.64, 65.18, 60.02 and 54.56% for malathion, rose bengal mixed, eosin mixed, soap and active cable, respectively.
The potency of tested compounds on armored scale insects
Data in Tables 3 and 4 show that females and nymphs of Parlatoria ziziphus responded to the potency of tested compounds soap alone, rose bengal mixed, eosin mixed, malathion and active cable oil during the first season. The tested compounds were more effective against mealybugs as compared to the armored scale insects. These percentages were 20.49, 27.93, 19.46, 91.1 and 13.77% for females, respectively, and were 50.37, 52.84, 49.03, 92.52 and 42.65% for nymphs, respectively. This indicates that each compound revealed more potency in nymphs than in females. Statistical analysis revealed that the F value had highly significant values in both females and nymph populations pre- and after spraying; but the differences between treatments due to the potency of the tested compounds were not significant (Table 3). The average reductions were 91.81, 40.39, 35.43, 34.25 and 28.21% for malathion, rose bengal mixed, soap, eosin mixed and active cable, respectively.
Table 4 shows the efficacy of the tested compound against both females and nymphs of P. ziziphus during the second season.
1- Against the females population
The toxicity of malathion was compared with the other tested compounds (Table 4). The percent of female reduction with malathion treatment was 92.96% followed by soap (58.76%), rose bengal mixed (46.54%), eosin mixed (39.77%) and active cable (35.37%), respectively.
2- Against the nymphs population
The same results were obtained against the nymphs. The percentage population reduction of nymphs was 92.5, 55.0, 52.5, 52.2 and 44.9% for malathion, rose bengal mixed, soap, eosin mixed and active cable, respectively.
The average reduction in both females and nymphs was 92.7, 55.6, 50.8, 46.0 and 40.1, respectively (Table 4).
Cumulative effect of test compounds on insect pests
Data in Table 5 show the net potency of tested compounds on insects without regard to insect species, stages or plant species. On this basis, these compounds can be arranged descendingly as follows: malation < rose bengal mixed < eosin mixed < soap < active cable; their potency was assessed by reducing the insect population collectively with 94.37, 66.18, 55.86, 51.94 and 44.69%, respectively.
Discussion
The obtained results showed that soap alone had potency against the Egyptian mealybug, Icerya aegyptiaca. The potency was assessed by an average of reduction 57.24 and 54.91% in insect populations attacking rose and acalypha shrubs, respectively, in the first season (Table 1). The corresponding results in the second season were 57.61 and 60.02% (Table 2). As well as soap, it caused a reduction in the armored scale insect (black Parlatoria scale) Parlatoria ziziphus nymphs by percent 50.39% which was higher than that caused in females (20.47%) (Table 3). The corresponding results in the second season were 52.5 and 58.76% (Table 4). These were in agreement with the results of Williamson (2021). The author reported that soap was very effective, attractive to insects and safe against the scale insects compared with conventional insecticides. Gill et al. (2012) reported that spraying soaps against the citrus mealybug Planococcus citri (Pseudococcidae) caused significant control in the insect population. Curkovic (2016) showed that younger individuals (nymphs II) of the mealybug P. longispinus were significantly more susceptible to insecticidal soap than adult females. Blanco–Metzler and Zuniga (2013) revealed that a significant reduction in crawlers and females of the armored scale Aulacaspis yasumatsui was caused by soap on cica crops. Soap reduced the population of the green scale Coccus viridis (Green) by a significant value ̴ 50% on coffee trees at 0.8% concentration (Reimer and Beardsley 1992; Gardener 2021)). Cloyd (2018) used soap detergent to protect roses from scale insects. Akyazi et al. (2022) found that the soap mixed with garlic extract was very effective against Polyphagotarsonemus latus. The percentage of mortality was 100%. The obtained results cleared that both photosensitizers rose bengal and eosin mixed with soap had a potential to reduce mealybug populations more than soap alone, rose bengal mixed reduced insects by 87.25 and 82.64 on rose and acalypha shrubs, respectively, while eosin mixed recued it by 75.62 and 62.48%, respectively (Table 1). This agrees with the results of Younis et al. (2021). The authors used rose bengal against the larvae of Culex pipiens. The percent of mortality reached 100% after 6 h of treatment. El-Ghobary et al. (2018) evaluated rose bengal, eosin yellow lactone and methylene blue against the fourth larval instar of the cotton leaf worm as photosensitizer compounds. The results showed that rose bengal was the most effective compound compared with the other tested compounds. The potency of both Rbm and Em in reducing of P. ziziphus population did not exceed 40.39 and 34.25%, respectively, in the first season and 50.8 and 46.0% in the second season. This may be due to the nature of insects or to the compact canopy and shaded vegetative growth of the sour orange tree host. Meier and Hillyer (2024) found that rose bengal was effective against both Aedes aegypti and Anopheles gambiae.
The organophosphorus insecticide “malathion” had the highest efficacy against both two tested insects, it can reduce the mealybug population by 98.74 and 96.67%; 95.97 and 94.43% on rose and acalypha shrubs, respectively (Tables 1 and 2) in the first and second seasons; and reduces the armored scale insect by 91.81 and 92.7% in both seasons on citrus trees (Table 3 and 4). This is in agreement with the results of Salem et al. (2009) who found that malathion reduced I. aegyptiaca population by 99–100% and the population of armored scale insect A. mangifera by 85.04%. The commercial mineral oil “Active cable” revealed the lowest potency on tested insects; it reduced the mealybug population by 59.91 and 48.13% in the first season (Table 1); 58.26 and 54.56% in the second season; on rose and acalypha, respectively, and rescued scale insect populations by 28.21 and 40.1% in the first and second seasons, respectively, of citrus trees. In addition to this, another fact could be derived about the potency of mineral oil, its potency on insect nymphs was higher than on insect females (Tables 1 and 2). These results are in agreement with the results of Abd-Rabou et al. (2012) who revealed that the mineral oil “Super Misrona” reduced the population of soft scale insects Parasaissetia nigra and Pulvinaria floccifera to a satisfactory level. Avila et al. (2022) found that the essential oils were very effective against mealybugs. Mohanny et al. (2022) found that malathion was very effective against the nymphs of scale insects on citrus leaves. This difference in responsibility between mealybug and armored scale insects toward the potency of the same compounds may be attributed to the characteristics distinguish between both insects such as: movement, mealybug individuals are able to move from plant part to another, but scale insect settled on plant parts during all life stages unless crawlers: body cover secretions, mealybug secret wax layers and filaments cover their bodies but scale insects secrete a thick secured wax shell (scale) cover their bodies and live beneath this scale. These characteristics made the mealybug more suitable to expose or contaminate with spray solution and become more affected by the insecticidal effect of tested compounds. Also, this difference in the responsibility of insects toward the tested compounds may be due to the nature of their host plants, mealybugs infest rose and acalypha shrubs that have small vegetative sizes, all the plant parts can be exposed to sunlight and the sunlight, can penetrate all plant parts infested with mealybug and activated the photosensitizers to kill insect, but the armored scale infest old sour orange trees that has big vegetative growth and compact canopy which prevent partially the sunlight from penetrating plant parts; followed by nonactivating photosensitizer and not kill insect; Lima et al. (2018) concluded that 100% mortality in Aedes aegypti larvae was achieved when larvae were exposed to sunlight, while eosin-methylene blue was nontoxic to the larvae in the dark. As well as the obtained results, it was clear that rose bengal mixed revealed higher potency on each insect than eosin mixed, this agreed with the results of El-Ghobary et al. (2018) who explained that rose bengal had higher potency as a photoinsecticidal on M. domestica and Spodoptera littoralis than eosin mixed. This work indicated that photosensitizer compounds that had a greater number of halogen atoms in their constituents such as rose bengal (Fig. 2) which contain 4 chlorin atoms and 4 iodine atoms are able to perform more toxicity on insects than eosin which contains only 4 iodine atoms; so that the halogen atoms amplifying the reactions of toxicity. Pieterse et al. (2023) found that sodium magnesium chlorophyllin photosensitizer was very effective against western flower thrips (WFT), Frankliniella occidentalis, and was recommended as in an integrated pest management program. This also agreed with the results of (Attia 2016). Soap was able to reduce insect population by a percentage equal or higher than that obtained by the mineral oil active cable-2, these percents were 45.76 and 41.12%, respectively, this agreed with the results of Abdel-Aziz et al. (2022) revealed active cable oil reduced the population of the scale insect, Parlatoria ziziphi (Lucas) by up to 91.7%. This is agreed with the results of (Salem et al. 2011; Ahmed and Attia 2018) reported that malathion decreased the population of I. aegyptiaca by 99.5–100%; and the population of A. mangifera by 85.04%. Data in Table 5 and Fig. 4 show that mealybug I. aegyptiaca revealed more responsibility to tested compounds than armored scale insect P. ziziphus; mealybug responded by 57.45, 86.83, 71.58, 96.46 and 55.22% while scale insect responded by 45.53, 45.59, 40.13, 92.27 and 34.17% toward soap, rose bengal mixed, eosin mixed, malathion and active cable oil, respectively (Table 5). According to the net potency per compound against both tested insects (I. aegyptiaca and P. ziziphus) rose bengal mixed (66.18%) had higher potency in reducing insect populations than eosin mixed (55.86%), also the soap was able to reduce insect populations by a percent (51.49%) and “active cable” (44.69%). Bendary and El-Helaly (2022) found the same results against the cotton leaf worm, Spodoptera littoralis. The authors found that rose bengal was the most effective compound against the larvae of S. littoralis. The organophosphorus insecticide had the highest potency in reducing insect populations (94.37%) (Table 5 and Fig. 4). The I. aegyptiaca was more susceptible to all tested compounds than the I. aegyptiaca. Rose bengal mixed with soap can be a promising natural insecticides especially against I. aegyptiaca. Meier et al. (2023) found that rose bengal increased the pupal mortality of A. gambiae compared with methylene blue.
Conclusions
This work is a preliminary investigation to test the newest alternative methods, soap and soap mixed with two photosensitizer compounds, against mealybug I. aegyptiaca and armored scale insect, P. ziziphus. The results revealed that soap, alone; or mixed with rose bengal and or mixed with eosin had a potency in reducing the mealybug. This efficacy was determined by 57.24, 87.25 and 75.62% on rose shrubs; and assessed by 54.91, 82.64 and 62.48% on acalypha shrubs, respectively. These obtained percent can be compared with percent of 59.91, 48.13% and percent of 98.71% and 96.67% resulted in spraying mineral oil active cable and the organophosphorus insecticide malathion on the same insect infesting rose, acalypha shrubs, in arrangement. The potency of the same tested compounds in reducing the population of armored scale insect P. ziziphus was lower in comparison with their potency on the mealybug insect. In some cases, their potency was absent. Therefore, it can be concluded that soap, photosensitizer and mineral oil can be used successfully in controlling Egyptian mealybug, besides gathering the advantages of these compounds such as their safety on the environment, wildlife, domestic animals and human health.
Availability of data and materials
My manuscript has associated data in a data repository.https://wwwnrc.academia.edu/AlkazafySabry
Abbreviations
- ANOVA:
-
Analysis of variance
- LSD:
-
Least significant difference
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Salem, H.AN., Sabry, Ak.H. & El-den Aref, N.B. Role of photosensitizer in control of mealybug and scale insects (Homoptera: Margarodidae and Diaspididae), in comparison with conventional insecticide. Bull Natl Res Cent 48, 92 (2024). https://doi.org/10.1186/s42269-024-01246-7
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DOI: https://doi.org/10.1186/s42269-024-01246-7