Effect of some insecticides and their side effects in controlling the California red scale, Aonidiella aurantii (Maskell)

INTRODUCTION

The scale insects (Hemiptera: Coccomorpha: Coccoidea) are one of the most important insect group in agricultural crops. The Coccoidea is divided into two major groups, the neococcoids and the archaeococcoids. The three largest families of neococcoids are the Pseudococcidae (mealybugs), Coccidae (soft scales), Diaspididae (armored scales). Family Diaspididae encompassing a number of important scale insects (2650 species in 400 genera) (Alford, 2002, 2007 and García et al., 2016) occur on a wide variety of host plants includes more than 1380 plant genera in 182 plant families (Miller and Davidson, 2005). The California red scale, Aonidiella aurantii (Maskell) (one of the species of family Diaspididae) is a highly polyphagus insect pest with a high preference for citrus species (Sorribas et al., 2010; El-Otmani, et al., 2011; Tena, and Garcia-Marí, 2011; Mohammed, 2020).  A. aurantii attacks all the above-ground parts of the tree including fruits, leaves, branches and twigs and sucking the sap of the plant tissue with their long, piercing-sucking mouthparts causing significant production losses (Beardsley Jr and Gonzalez 1975). Branches and twigs substrate are less preferred for the California red scale while the fruit is the preferred plant part, followed by leaves (Hare, et al., 1990). A. aurantii infests foliage and fruits and is of serious concern to citrus production. Its feeding on leaves may cause them to yellow and the heavy infestations can cause stems and branches to dieback. The presence of the scales on fruit (particularly if infestations occur when fruit are developing) may cause them to be blemished or distorted considerably reduces their market value (Flint et al., 1991; Vacas, 2010). The survey studies are very vital for update and population dynamics data documentation (Jendoubi, 2018). Keeping in view the above mentioned information, it is necessary to test several insecticides with different mode of action against red scale insects because of its rapid ability to develop resistance. Therefore the aim of the present work was to estimate the population dynamic, numbers of generation, infestations percentages, horizontal and vertical distribution, parasitism rates and effect of of the main climatic factors on the population density of A. aurantii, as well as for well understanding and establishing IPM strategies against this pest. Also, the current experiments aimed to study the efficiency of five insecticides (Pyriproxyphen 10% EC, Acetamiprid 20% SP; sulfoxaflor 24%, SC, Azadirachtin 0.03% EC and Kz oil 95% EC) against A. aurantii in different dates according to the life stage composition.

MATERIALS AND METHODS

The present study was planned to determine the changes in the relative abundance of A. aurantii population. The experiments were carried out between the beginning of January 2020 and the end of December 2021 at a sweet orange private farm in Nubaria district, Beheira Governorate, Egypt. Samples of seventy five leaves of 5 sweet orange trees were weekly picked throughout the two years. The selected trees were in the same age (twelve years old), size, height and vegetative growth. The leave samples were kept in 15 labeled poly ethylene bags; each bag represents a particular direction or a specific layer of the experimental trees. Each bag contains five leaves. The samples transferred to the laboratory and carefully inspected using a stereomicroscope. Among each inspection, the individuals of A. aurantii in the sample leaves (on upper and lower surfaces) were divided into pre-adult (immature) and adult stages. All the different stages of A. aurantii were precisely counted and recorded. The infestation percentage of leaves also was recorded by dividing number of infested leaves by the total number of leaves in each investigation date. The weekly counts of the total population of were accumulated along the whole year, arranged and illustrated graphically on semigassian paper (scale gausses) to estimate the number and duration of generations of A. aurantii (Audemard and Milaire, 1975 and Iacob, 1977).

Population dynamic and rate of parasitism of A. aurantii parasitoids:

This work was planned to study the parasitism rates and population dynamic of the parasite Aphytis spduring two successive years (beginning of January 2020 and the end of December 2021). Weekly specimens of 8 sweet orange leaves infested with A. aurantii were collected from sweet orange trees and transferred to the laboratory. The leave samples put in 4 glass jars after removing all the other scale insects except A. aurantii. The jars were 15 cm diameter and 25 cm height and covered with muslin held by a rubber band and kept under laboratory conditions for securing any emerging parasitoids. Numbers of emerging parasites were daily recorded and the rate of parasitism was calculated by dividing the number of emerging parasitoid by the number of existing scales.

Efficiency of different insecticides in two different dates on the California red scale

Five insecticides were evaluated against A. aurantii populations on sweet orange trees in two different spraying dates. In each spraying date, twenty four trees (plots) in the same age, size, height and vegetative growth were used. Every 4 trees (plots) were considered for each applied treatment in addition to the 4 trees for control plots. Application of the five treatments was in March 1^st and April 8^th in the two years. Five leaves from each trees were examined and the number of alive individuals of A. aurantii were counted before treatment and after 1, 2, 4 and 6 weeks of the treatment. The spraying dates were determined based on the life stage composition. One of them was in the nymph abundance time and the other was in the time of adult abundance. The percentages of population reduction were calculated according the equation of Henderson and Tilton (1955) as following:

Ta x Cb

 % Reduction = 100 x 1- ـــــــــــــــــــــــــ

 Tb x Ca

Where:

Cb = mean of population density in control plots before application

Ta = mean of population density in treatment plots after application

Ca = mean of population density in control plots after application

Tb = mean of population density in treatment plots before application

The tested insecticides were

Mineral oil (Star oil) 95% EC provided by International Company for Chemical Industries (GINTRA Egypt), 15 Cm³ L^-1

Pyriproxyphen (Admiral) 10% ECprovided by Sumitomo Chemical Australia Pty Ltd, 0.5 ml/L^-1

Azadirachtin (Nimbecidine) 0.03% EC provided by T. Stanes and Company Limited, 5 Cm³l^-1

Acetamiprid (Mospilan) 20% SP provided by Nippon Soda Ltd, 25 mg L^-1.

Sulfoxaflor (Closer) 24%, SC provided by DowAgro Sciences Co., Ltd, 0.5L^-1

Data analysis: Statistically significant mean values (P <0.05) were calculated as mean ± SD (standard deviation) using analysis of variance (ANOVA) and separated by least significant differences (LSD) test (SAS Statistical software, 1999).

RESULTS AND DISCUSSION

The population dynamic of California red scale, A. aurantii:

The results represented in Tables (1 & 2) show the weekly average numbers of different stages as well as the fluctuations in the total population of the California red scale insect, A. aurantii on sweet orange trees during the first (2020) and second (2021) years in Nubaria district, Beheira Governorate. During the course of this study, the total population of A. aurantii had four peaks of abundance in the first year. The first peak occurred in April 8^th (24.04 individuals/ leaf), the second in July 8^th (22.77 individuals/leaf), the third one appeared in September 15^th (31.04) and the fourth was recorded in November 15^th (35.31). In respect to the 2^nd year, 2021 the total number of A. aurantii scales also showed four peaks of abundance recorded in April 22^nd (25.2), July 1^st (19.67), September 1^st (40.43) and  November 1^st (47.09). Also, the results presented in Fig 1&2 illustrated that the California red scale had four overlapping generations. The 1^st generation extended from the mid-Feb to May 22^nd, the 2^nd extended from Jun 1^st to Jul 22^nd, the 3^rd extended from Aug 1^st to Oct 8^th and the 4^th extended from mid-Oct to mod-Dec. In 2021, the 1^st generation extended from mid-Feb to Jun 8^th, the 2^nd extended from mid-Jun to Aug 1^st, the 3^rd extended from Aug 8^th to Oct 1^st and the 4^th extended from Oct 8^th to Dec 22^nd. The current results are in agreement with the results of Selim (2014) at Giza governorate, Egypt who found that the population of A. aurantii had three annual generations (peaks) on Balady orange and four generations (peaks) on Succari orange during the two successive seasons. In slightly different results Farghaly et al . in 2016 (in Middle Egypt) and Balboul and Helmy, 2019 (in Giza Governorate) recorded three overlapping generations per year for the California red scale during two years of study. On another hand the results of Nabil and Shahein in 2014 in Ismailia Governorate revealed that A. aurantii had only two to three annual generations on navel orange trees. Abd-Elghaffar et al. 2017at Sharkia Governorate showed that the sweet orange appeared to be the most susceptible citrus tree hosts to infestation by A. aurantia

 followed by navel orange and mandarin. They found that the population density of A. aurantii had three generation on the three citrus tree hosts during the two study years (2013 and 2014).

Table (1): The population dynamic and the infestation percentages of the California red scale, A. aurantii on sweet orange trees at Beheira Governorate during the 1^st year, 2020

Table (2): The population dynamic and the infestation percentages of the California red scale, A. aurantii on sweet orange trees at Beheira Governorate during the 2^nd year, 2021

Fig. 1. The number of generation and generation duration of the California red scale, A. aurantii on sweet orange trees at Beheira Governorate during 2020 and 2021 years:

The horizontal and vertical distribution of A. aurantii:

Concerning the horizontal distribution of the California red scale, the results of analysis of variance showed that there were significant differences between the different cardinal directions of the sweet orange trees during the two years of study. As shown in Figs. 3&4, the seasonal average of A. aurantii population was higher for the eastern direction (21.73±9.33 and 26.8± 13.23 individuals per leaf), followed by southern direction (14.71± 6.41 and 19.72± 10.14 individuals per leaf). In contrast, the leaves in the tree core were the least infested leaves with A. aurantii (13.17 ± 5.79 and 15.33 ± 9.38 individuals per leaf). The leaves in west (14.72± 6.41 and 19.72± 10.14) and north directions (14.35±6.36 and 21.22±10.82) were moderately infested with the insect. On the other hand, the results of analysis of variance clearly indicated that there were significant differences in the population means of the California red scale among the three strata of sweet orange tree for each season. The leaves in middle stratum was the most preferred by the California red scale, A. aurantii with a general average of 22.58 ±10.76 and 27.51 ± 13.81 individuals per leaf per year during the 1^st and 2^nd years, respectively, followed by the leaves in top stratum (17.07 ± 7.13 and 20.59 ±10.65 individuals / leaf / year ), while the leaves in bottom stratum was the least infested by the insect with a general mean of 9.04 ± 3.43 and 16.7 ±8.18 of scale per leaf, during the two tested years 2020 and 2021, respectively.

We may therefore conclude that A. aurantii prefer to concentrate on the eastsouthern side and the middle stratum of the sweet orange tree. The results of the horizontal and vertical distribution of the California red scale insect must be taken into consideration when planning for the integrated pest management programs particularly the chemical control for this insect. The present results were agreement with the results of Darwish, 2016 who found that the black parlatoria, Parlatoria ziziphi prefer to the existing leaves on the southern and eastern branches of mandarin tree. Nabil and Shahein, 2014 found that the population of A. aurantii on navel orange trees were occurred in north western direction in the 1^st season (2011-2012), while during the 2^nd season (2012-2013) the population was concentrated in the north eastern side of the trees.

Fig.2 General means of the insdividuals of the California red scale, A. aurantii on the cardinal direction of the sweet orange trees throughout 2020 and 2021 years

Means followed by the same letter(s) are not significantly different (p≤0.05)

Fig. 3. General means of the insdividuals of the California red scale, A. aurantii on the different strata at the sweet orange trees throughout 2020 and 2021 years

Means followed by the same letter(s) are not significantly different (p≤0.05)

Regarding preferable leaf surface of A. aurantii, data illustrated in Fig. (-) indicated that in the first and second years of the study, the total population of A. aurantii was higher on the upper leaf surface than the lower one with values of 9.701 individuals on the upper surface and 6.53 individuals on the lower surface during the 1^st season, 2020 and 14.59 individuals on the upper leaf surface and 7.01 on the lower surface in the 2^nd season, 2021. The current results also are in agreement with the results of Darwish, 2020 who found that the scale insect, Lepidosaphes beckii prefer the upper surface of Valencia orange leaves than the lower surface.

Fig. 4. General means of the insdividuals of the California red scale, A. aurantii per a sweet orange leaf throughout 2020 and 2021 years on upper and lower leaf surfaces. Means followed by the same letter(s) are not significantly different (p≤0.05)

The higher infestation percentages of sweet orange leaves with A. aurantii were 48, 33.33, 65.33 and 66.67 % in April 8^th, July 8^th, September 15^th and November 15^th, respectively during the 1^st season in synchronized with the account peaks of the population dynamic. These percentages reach 54.67, 61.33, 76 and 78.67 in April 22^nd, July 1^st, September 1^st and November 1^st, respectively in the 2^nd year, 2021.

Parasitization rates

During the 1^st season, 2020, the parasitization level ranged from 4.62% (on mid-January) to 19% (on mid-June) (Fig. 4). During the 2^nd year 2021 (Fig. 5), the parasitization rates ranged between 6.36% (on January 1^st, 2021) and 25.71% (on June 8^th, 2021). As a general the percentage of parasitism reached its maximum level during the third generation of the California red scale (at the summer generation of the insect). During the first year of study 2020, the activity of parasitism had five peaks five representing overlapping generations per year. In the second year, 2021 (as illustrated in Fig. 5), six peaks had been observed. At probability level 0.05 the simple correlation values were positive and highly significant in the two years of study. The correlation coefficient values were 0.674** and 0.805** for 2020 and 2021 years, respectively.

Fig. 5. Parasitism percentages of Aonidiella aurantii parasitoid (Aphytis sp) on sweet orange trees during the 1^st year, 2020

Fig. 6. Parasitism percentages of Aonidiella aurantii parasitoid (Aphytis sp) on sweet orange trees during the 2^nd year, 2021

The efficiency of five insecticides against A. aurantii

The 1^st date, when the crawlers were the target:

As shown in Table (3 a&b), among the tested insecticides, the insecticide Sulfoxaflor was the most effective insecticide with a general mean of reduction percentage of 88.63±13.02 followed by Pyriproxyfen, Azadirachtin, Acetamiprid and Kz oil with reduction percentages of 80.93±11.64, 72.33±17.21, 67.05±22.66 and 58.91±26.08, respectively in the 1^st season, 2020. During the 2^nd season, 2021 these percentages recorded 84.41±13.74, 75.98±9.31, 69.42±11.42, 63.64±17.66 and 56.92±19.78 for Sulfoxaflor, Pyriproxyfen, Azadirachtin, Acetamiprid and Kz oil, respectively.

The 2^nd date, when the adults were the target:

Data presented in Tables (4 b) refer to the insecticide Sulfoxaflor was the most effective insecticide with a reduction percentage of 84.41±13.74 followed by Kz oil (80.12±9.41), Azadirachtin (73.33±11.37), Pyriproxyfen (71.57±8.08) and Acetamiprid (66.98±13.93). During the 2^nd season 2021, these results were repeated with a slightly different whereas the Kz oil was the most effective insecticide followed by Sulfoxaflor, Azadirachtin, Pyriproxyfen and Acetamiprid with reduction percentages of 79.48±8.78, 78.8±7.37, 73.02±9.3, 71.53±5.43 and 67.96±13.23.

Finally, it could be concluded that the most effective insecticide for controlling the California scale insect, A. aurantii depend on the time of the control. In the times when the crawlers are prevalent and abundant, use of the insecticide Sulfoxaflor is preferred while the insecticide Kz oil is preferred when the adult is prevalent. Rezk, et al., 2021 testedpyriproxyphen, imidacloprid, spirotetramat, sulfoxaflor and a mineral oil against A. aurantii on navel orange trees. They found that among the tested insecticides, Kz oil was the most effective in reducing the treated population.