Population Dynamics and Chemical Control of Two Diaspid Scales Infesting Mango Trees

INTRODUCTION

Mango, Mangifera indica (L.), fam. Anacardiaceae, is considered to be one of the most important fruit trees in the world, including Egypt. The total cultivated area in Egypt is about 187730 Fed.  with a total annual production of 850114 metric tons (Food and Agriculture Organization of the United Nation, 2020). As many tropical and subtropical crops, many species of insects and mites have been reported to infest mango trees such as the scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Worldwide, the scale insects are key pests on ornamental plants and fruit trees. The three most important families of the scale insects, according to the economic damage and number of genera, are Coccidae (soft scales) with 170 genera, Pseudococcidae (mealybugs) with 272 genera and Diaspididae (armored scales) with 419 genera (García Morales, et al., 2016). Diaspid scales can cause economic damage directly with its piercing and sucking mouth parts; through sucking the sap from the leaves, twigs and fruits; the transmission of viruses; and the injection of toxins into the plants, which weaken the plant and lower the fruit yield and quality (Waite, 2002; Sathe, et al. 2014; Hassan, et al., 2012; Ouvrard, et al., 2013; Darwish, 2015 and Darwish, 2020). The mango white scale, Aulacaspis tubercularis (Newstead) is one of the most dominant armored scale insects in mango orchards (El–Metwally, et al., 2011; Reda, et al., 2011; Abo-Shanab, et al., 2012; Ayalew, 2015; Hamdy, 2016; Pino, 2020 and Lo Verde, et al., 2020). The first record of A. tubercularis as a new pest of mango trees in Egypt was in Minia governorate (Morsi et al., 2002). Thereafter, the insect has been distributed allover the governorates of Egypt. If no control measures were performed, the mango white scale can cause yield losses up to ninety percent in mango groves (Pino, et al., 2020). The olive scale, Parlatoria oleae (Colvée) is another important scale insect infesting mango trees (Bakry, et al., 2019 and Bakry, et al., 2020). Both the nymphs and the adults of P. oleae are the damaging stages. Heavy infestations with P. oleae on leaves and branches of the fruit trees cause extensive die-back and yield losses. The injection of toxins into the plants by the stages of P. oleae causes dark-red spots on fruits, branches and leaves of its hosts. It was emphasized that the first step towards the progress of the integrated pest management program of any insect pest is the extensive ecological study of this pest (Hassan and Radwan, 2008). Therefore, to select and schedule appropriate control strategies, growers should use the information gathered from the field monitoring/scouting of the insect pests. We also have to take into account the fact that the updated survey of the scale insect pests is very required because most scale insects are sensitive to the changes in the meteorological factors, the host preference and the agriculture practices. Chemical control has been considered to be the most important tool employed for the management of scale insects, particularly when the other control measures are not sufficient to prevent plant injury. Keeping in view the above-mentioned facts, the present work was designed to study some ecological aspects and chemical control of two diaspid scales infesting mango trees during two successive years (2019 and 2020) in Behiera governorate.

MATERIALS AND METHODS

Some ecological aspects of A. tubercularis and P. oleae on mango trees

The present experiments were conducted at a private mango farm in Nobaria district, Beheira governorate, Egypt. Twelve years old Ewais mango trees were used in this study. The trees were grown in sandy soil under drip irrigation system, spaced at 6 X 4 m apart. The study period extended from the beginning of 2019 until the end of 2020, ie, two consecutive years. Ten mango trees homogenous in size and age were chosen and marked for sampling purposes. The selected trees were infested by some diaspids scale insects including A. tubercularis and P. oleae. Regular weekly samples represented the four cardinal directions (south, north, west, and east) as well as the tree core and the three tree strata. The sample consisted of seventy five leaves (15 leaves/ tree) of five mango trees, from the selected trees. The different stages of the two scale insects on the different mango leaf surfaces were accurately counted and recorded. The picked leaves were kept in 15 polyethylene bags; each bag represents a specific direction or a particular layer of the tree. Samples were transported to the laboratory, and inspected carefully with the aid of a stereomicroscope. Throughout the study period, except the application of any insecticides, all recommended agriculture practices were performed as usual. The monthly variation rate (MVR) in population density was calculated by dividing the average count given in a month by the average count given in the precedingone (Abdel-Fattah et al, 1978).

Fruit samples

Twenty five fruits on mango trees, or those dropping on the soil, were collected within 8 weeks' time during the fruit ripping period to study the relative fruit susceptibility to infestation with the two scale insects, A. tubercularis and P. oleae.

Effect of four different insecticides on the population density of A. tubercularis and P. oleae

Field experiments were carried out to evaluate the effect of four insecticides on the population density of A. tubercularis and P. oleae.  Five treatments, four insecticides and control, were applied using a randomized complete block design (CRBD). The treatments were replicated five times with one tree per replicate making a total of 25 mango trees homogenous in size, age, height, and vigor. Before the start of the experiment, the experimental units, ie, trees, were not treated with any insecticide. The tested compounds were sprayed on April 25^th in both seasons at their label recommended rates with complete coverage of all parts of the treated trees. A Knapsack sprayer, CP3 was used for spraying the different insecticides. The control plots were sprayed only with water. Randomly, five mango leaves of each tree (25 leaves from each treatment) were picked and kept in paper bags for the further examination in the laboratory. The total population of A. tubercularis and P. oleae were recorded just before spraying with insecticides and after one, two, three and four weeks. The reduction percentages of A. tubercularis and P. oleae were calculated according to the Henderson and Tilton (1955) equation as follows:

Corrected % = (1 –((ncb*nta)/(nca*ntb)))*100

Where:

nta = mean numbers of scale insects in treatment after application

ncb = mean number of scale insects in control before application

ntb = mean number of scale insects in treatment before application

nca = mean number of scale insects in control after application

The tested insecticides and their usage doses

Admiral^® (Pyriproxyfen 10% EC): formulated by Sumitomo Chemical Co. Ltd., used at the rate of 50 ml / 100 L water

Nimbecidine^® (Azadirachtin 0.03% EC): formulated by T. Stanes and Company Limited, used at the rate of 500 Cm³ / 100 L water

K.Z oil^®: In Miscible type formulated by Kafr El-Zayat Co., used at the rate of 1.5 L / 100 L water.

Mospilan^® (Acetamiprid 20% SP): formulated by Nisso Co., used at the rate of 30 g/100 L water

RESULTS AND DISCUSSION

The white mango scale, A. tubercularis

Seasonal fluctuation of different developmental stages of the white mango scale, A. tubercularis

The seasonal fluctuation of A. tubercularis which represented by weekly mean numbers of immature and adult stages throughout two successive years are graphically illustrated in Figs. 1 and 2. The results showed that the population density of A. tubercularis was higher during the 2^nd year, 2020, than in the 1^st year, 2019. Three population peaks occurred in January 15^th, March 12^th and September 17^th throughout the first year, 2019, with average values of 46.93, 54.4 and 91.47 individuals/ leaf, respectively. In the consecutive growing year, 2020, such three peaks were recorded on January 21^st (89.87 individuals/ leaf), March 31^st (88 individuals/ leaf) and September 22^nd (108.53 individuals/ leaf). The results also showed that the population density of the adult stage was less than that of the immature stages. From the current results, it's obvious that the white mango scale has three peaks per year ie, three overlapping generations. The present results are slightly different from the results of Kawiz, 2009, Hamdy, 2016 and Amer et al., 2017 in Qaliobiya governorate and Lo Verde, et al., 2020 in Southern Spain who recorded four peaks for this insect. On the other hand, Attia, et al., 2020 in Sharkia governorate found that the total alive stages population of A. tubercularis had two activity peaks during two successive years of study.

Fig (1): Seasonal fluctuations of immature and adult stages of the white mango scale, Aulacaspis tubercularis represented by weekly means/leaf, on mango trees during 2019 year.

Fig (2): Seasonal fluctuations of immature and adult stages of the white mango scale, Aulacaspis tubercularis represented by weekly means/leaf, on mango trees during 2020 year.

The vertical distribution of A. tubercularis

Data in Fig. 3 revealed that the distribution pattern of A. tubercularis significantly varies according to the levels of mango trees. During the 1^st season, the middle stratum of mango trees always harbored the highest population density of the adult stage, with a general mean of 19.12 adults/ leaf. The lowest population density, with a general mean of 15.23 adult /leaf, was recorded in the upper

stratum. The results also showed that the middle level of mango trees always harbored the highest population density of immature stage of A. tubercularis, 33 individuals /leaf, followed by the lower level, 26.54 individuals /leaf, and the upper level, 24.21 individuals /leaf. As shown in Fig. 3, the results obtained in the 2^nd season, 2020, revealed that the upper stratum of the mango trees was the least preferable stratum for both adults and immature stages of A. tubercularis followed by the lower and the middle stratums. The present results support the results of Bakry and Eman, 2019 who found that the white mango scale prefers the middle stratum of the mango trees in Esna District, Luxor governorate, Egypt. On the contrary, Nabil et al. (2012) reported that the infestation with the same insect, A. tubercularis, at the bottom stratum of the mango trees was higher than that at the top one in Sharkia governorate, Egypt.

Fig. 3. Seasonal mean numbers of A. tubercularis, adults and immature stages, in the different strata of mango trees through two successive years (2019 and 2020)

The horizontal distribution of A. tubercularis

Data shown in Fig. 4 emphasize that population distribution pattern of A. tubercularis considerably differs from one direction to another. The mango leaves at eastern direction harbored the maximum average numbers of A. tubercularis immature, 36.85 and 48.75 individuals/leaf in 2019 and 2020, respectively; and adult stages,19.98 and 28.46 adults/leaf in 2019 and 2020, respectively. South direction ranked the second with a seasonal mean of 29.58 and 41.66 immature individuals/leaf, and 18.98 and 23.86 adult individuals / leaf throughout the 1^st and 2^nd seasons, respectively followed by tree core, 28.25 and 37.26 immature individuals/ leaf, and 16.36 and 22.92 adults/leaf in 2019 and 2020, respectively. The lowest average numbers were recorded in the western direction,21.59 and 26.1 immature individuals/ leaf, and 17.78 and 19.14 adult/leaf in 2019 and 2020, respectively. The current results are in agreement with the results of Nabil et al. (2012) who mentioned that the white mango scale are concentrated in the eastern direction than the other directions. In close results, El-Metwally et al. (2011) found that the southern direction was the most preferable direction for A. tubercularis followed by the eastern direction.

Fig. 4. The horizontal distribution of A. tubercularis (adults and immature stages) in the main cardinal directions and mango tree core through two successive years (2019 and 2020). The bars followed by the same letter(s) in the column are not significantly different (P< 0.05)

.

Distribution of A. tubercularis on different leaf surfaces

Results depicted in Fig. 5 clearly indicated that the adult and immature stages of A. tubercularis prefer the upper surface of the mango leaves to the lower surface. The seasonal mean numbers of the immature stage of the white mango scale per leaf on the lower surface were 5.55 ± 2.37 and 12.56 ± 6.7 for the two years of study, 2019 and 2020, respectively. These means on the upper surface were 22.36±11.83 and 24.92 ±10.91 individuals/leaf, in 2019 and 2020, respectively. Regarding the distribution of adults of this insect on the upper and the lower surfaces of mango leaves, the results showed that high population densities of adults of A. tubercularis were recorded in the upper surface 9.23±3.9 and 13.82±5.73 in 2019 and 2020, than the lower surface, 8.16±2.94 and 8.95±2.35 in 2019 and 2020.

The current results are in agreement with the results of Bakr et al. (2009), Nabil et al. (2012), Sanad (2017) and Bakry and Eman, 2019 who found that the white mango scale prefers the upper surface of mango leaves to the lower one. Other results were obtained by El-Metwally et al., 2011 who found that the white mango scale prefers the upper surface in winter months, whereas in the summer months they prefer the lower surface. The statistical difference between the population density in the upper and the lower surfaces was more pronounced for immature stage (t= 12.349 for 1^st year, 2019; t= 18.658 for the 2^nd year, 2020) than it's in the case of adult stage (t= 3.086 for 1^st year, 2019; t= 8.795 for the 2^nd year, 2020)

Fig. 5. Seasonal mean numbers of A. tubercularis (adults and immature stages) in the different surfaces of mango leaves through two successive years (2019 and 2020)

The Olive Parlatoria, Parlatoria Olea (Colvée)

Seasonal fluctuation of different developmental stages of the olive parlatoria, P. Olea

During the 1^st season, 2019, as shown in Fig. 6, the population density of  P. oleae started with relatively low numbers and then increased gradually till reaching the first abundance peak on March 26^th,13.6 individuals/leaf. The 2^nd peak, the highest peak, was recorded on the May 21^st, 14 individuals/ leaf. Afterwards, the population decreased and fluctuated throughout the period from May to September. Then it increased again to reach the 3^rd peak on October 8^th, 12.53 individuals/leaf. During the 2^nd season, 2020, a similar trend was obtained (Fig. 7), whereas the 1^st

peak, the highest peak, was recorded on March 17^th, 21.87 individuals/leaf. The 2^nd and the 3^rd peaks were recorded on June 19^th and September 29^th with a mean of 19.73 and 17.07 individuals/leaf, respectively. Similar results were obtained by Moursi, et al., 2013 who found that the population of olive parlatoria scale reached the maximum density during April, November and January in 2010, but in 2011 the insect had four peaks during March, August, November and January on plum trees in Burg El-Arab area, Egypt.

Fig (6): Seasonal fluctuations of immature and adult stages of the olive parlatoria, Parlatoria oleae represented by weekly means/leaf, on mango trees during 2019 year.

Fig (7): Seasonal fluctuations of immature and adult stages of the olive parlatoria, Parlatoria oleae represented by weekly means/leaf, on mango trees during 2020 year.

The Vertical distribution of P. Oleae

The data obtained in Fig. 8 showed that the highest population density of P. oleae was found on leaves at the bottom level of mango trees, followed dissentingly by the population density on leaves at middle and top levels of the tree. The seasonal mean of immature population densities at the bottom level recorded 6.71± 2.38 and 11.91 ± 3.36 per leaf during the 1^st and the 2^nd seasons, respectively. While the population densities of adult stages were 3.08 ± 1.11 and 5.39 ± 1.52 adults per leaf through the two successive years 2019 and 2020, respectively. Regarding the tree middle level, the seasonal means of adults and immature stages were 2.91 ± 0.75 and 6.3±2.61 during the 1^st season and 4.46±1.59 and 8.36 ± 2.88 during the 2^nd season, respectively. The leaves of the lower stratum of mango tree had the lowest population density of P. oleae, whereas the adults and immature densities were 1.77±0.53 and 4.01±1.5 in the 1^st season and 2.89±0.98 and 6.37±2.19 individual/leaf during the 2^nd season. The present results are in harmony with the results of Bakry, et al., 2019 who found significant differences between the mean population densities of P. oleae on different levels of mango trees.

Fig. 8. Seasonal mean numbers of A. tubercularis (adults and immature stages) in the different strata of mango trees through two successive years (2019 and 2020)

The Horizontal distribution of P. oleae

As illustrated in Fig. 9, the leaves at mango tree core harbored the maximum population of P. oleae immature, 23.23 and 31.73 individuals/leaf in 2019 and 2020, respectively, and adult stages,9.64 and 15.02 adults/leaf in 2019 and 2020, respectively. South direction ranked the second with a seasonal mean of 18.6 and 29.52 immature individuals/leaf and 7.81 and 13.71 adult individuals /leaf throughout the 1^st and the 2^nd seasons, respectively followed by the east direction, 17.02 and 26.4 immature individuals/leaf and 8.52 and 13.08 adults/leaf in 2019 and 2020, respectively. The lowest average numbers were recorded in the northern direction, 12.77 and 21.08 immature individuals/leaf and 7.08 and 11.98 adult/leaf in 2019 and 2020, respectively.

Fig. 9. The horizontal distribution of P. oleae (adults and immature stages) in the main cardinal directions and mango trees core through two successive years (2019 and 2020). The bars followed by the same letter(s) in the column are not significantly different (P< 0.05).

Distribution of P. oleae on different leaf surfaces

The data illustrated in Fig. 10 showed that the adult and immature stages of P. oleae prefer the upper surface of the mango leaves to the lower surface. The general means of the immature stage on the lower surface were 2.22 ± 0.89 and 3.65 ± 1.24/ leaf for 2019 and 2020, respectively, whereas the general immature means on the upper surface were 3.46 ±1.24 and 5.23 ±1.65/leaf, in 2019 and 2020, respectively. The population density of P. oleae adults on the upper and lower surfaces of mango leaves recorded 1.33 ± 0.43 and 1.25 ± 0.41 during 2019 season, whereas these values in the 2nd season, 2020 were 2.41 ±0.71 and 1.84 ±0.7 on the upper and the lower surfaces, respectively. The present results support the results of Bakry, et al., 2019 who found that the total population of P. oleae was more abundant on the upper surface than on the lower one.

Fig. 5. Seasonal mean numbers of P. oleae (adults and immature stages) in the different surfaces of mango leaves through two successive years (2019 and 2020)

The relative susceptibility of mango fruits to infestation with both of P. olea and A. tubercularis

Despite the obvious increase in the population density of the white mango scale compared with the parlatoria scale as shown in Figs. (1, 2, 6 and 7), the study of the population density of the two scales on mango fruits shows that the olive parlartoria scale is present more abundantly than white mango scale. This result suggests that the parlatoria scale might be more dangerous than the white mango scale.

Fig. 10. The relative susceptibility of mango fruits to infestation with P. oleae and A. tubercularis (adults and immature stages) through two successive years (2019 and 2020)

The Monthly variation rate (MVR) of population density of A. tubercularis and P. oleae

The monthly counts of the total population of A. tubercularis and P. oleae through the two successive years of investigation are tabulated in Table 1. Data concerning the monthly variation rate (MVR) of population density of A. tubercularis clearly show that the favorable periods for its development and population

increase were in March and September 2019, with MVR values of 1.49 and 1.71, respectively (Table 1). In the second year, 2020, the highest values of MVR were 1.309, 1.698 and 1.71 in January, July and September, respectively. On the other hand,

the highest monthly variation rates (MVR) of population density of P. oleae were 1.46, 1.48 and 1.374 in February, March and September in the 1^st year, 2019, and 1.539, 1.463 and 1.378 in February, March and June in the 2^nd year, 2020, respectively

Table (1): The monthly variation rate (MVR) of population density of A. tubercularis and P. oleae during two successive seasons, 2019 and 2020

Effect of four insecticides on A. tubercularis and P. oleae

Based on data presented in Tables (2&3), it is evident that during the 1^st season, 2019, acetamiprid was the highly effective insecticide against A. tubercularis, with a general mean of 87.87% reduction percentage, followed by pyriproxyfen 84.56 %, azadirachtin 78.01 % and KZ oil 69.1 % with significant difference between the efficacy of the tested insecticides on the total population of A. tubercularis. The same results were obtained during the 2^nd season, whereas the descending order of the tested insecticides was acetamiprid 90.37 %, pyriproxyfen 84.55 %, azadirachtin 81.25 % and K.Z oil 67.26 %. The two tested insecticides acetamiprid and pyriproxyfen,during the 1^st season, and pyriproxyfenand azadirachtin, during the 2^nd season, had insignificant differences between each one of them with the other where L.S.D. was 6.2106 and 5.4696 during the two consecutive seasons 2019 and 2020, respectively. Regarding the susceptibility of P. olea to the tested insecticides (Tables 4 and 5), it's obvious that the olive scale was more resistant to the tested insecticides than the white mango scale. The insecticide pyriproxyfen was the highly effective insecticide against the insect with general means of 76.77 % and 77.57 % in 2019 and 2020 seasons, respectively. The insecticide, acetamiprid ranked the second with general means of 75.19 % and 69.97 %, followed by azadirachtin with general means of 66.59 % and 62.85 %, and finally K Z oil with general means of 65.08 and 61.97 in 2019 and 2020 seasons, respectively.

The current results revealed that the tested insecticides were more effective than the K.Z oil in disagreement with the results of Dewer, et al., 2012 who studied the effect of five insecticides, i.e., azadirachtin, pyriproxyfen, acetamiprid, emamectin benzoate and summer mineral oil and their mixtures for controlling Lepidosaphes beckii. They found that the use of summer mineral oil gave the highest reduction percentages. In agreements with Baker, et al., 2012 the reduction percentages of the insecticide pyriproxyfen (IGRS) still to increase and gave high effect till the end of the experiment. Mohamed, 2002 found that the red scale insect, A. aurantii was affected by pyriproxyfen than K.Z oil. Mohamed (2002) tested fenitrothion, pyriproxyfen, mineral oil 94% E C on P. oleae in Ismailia; he found that oil alone or mixed with other compounds held superior category allover the experiment time.

Table (2): Reduction percentages of the white mango scale, A. tubercularisinduced by application of four insecticides on mango trees during the 1^st season, 2019

The reduction percentages followed by the same letter(s) in the column are not significantly different (P< 0.05).

Table (3): Reduction percentages of the white mango scale, A. tubercularisinduced by application of four insecticides on mango trees during the 2^nd season, 2020

The reduction percentages followed by the same letter(s) in the column are not significantly different (P< 0.05).