Egypt. J. Plant Prot. Res. Inst. (2020), 3 (4): 1067-1074

Egyptian Journal of Plant Protection Research Institute www.ejppri.eg.net

Ecological studies on two mealybug species () and their predator on navel orange trees at Qalubiya Governorate, Egypt Hanan, F. El-Sobky Plant Protection Research Institute, Agricultural Research Center, Dokki, Giza, Egypt.

ARTICLE INFO Abstract: Article History Citrus mealybug Planococcus citri (Risso) (Hemiptera: Received: 4 /11 /2020 Pseudococcidae) and Egyptian fluted mealybug, Icerya aegyptiaca Accepted: 16 / 12 /2020 (Douglus) (Hemiptera: Monophlebidea) are serious pests, attack the navel orange trees and cause a severely considerable Keywords damage. The present study aimed to determine mealybug generations under the studied conditions and the proper time for Mealybugs, their control. Field studies were carried out on P. citri and I. Planococcus citri, Icerya aegyptiaca on 100 navel orange leaves and 25 twigs in half aegyptiaca , Rodolia monthly samples, at a private farm in Qalubiya Governorate, cardinalis , predator and Egypt throughout two years 2018 and 2019. The obtained results navel orange . showed that P. citri population had three peaks of infestation in the first year (2018) in June 1st, July 2nd and August 2nd. In the second year (2019) two peaks were recorded on 1st week of July and 2nd week of September. The Egyptian mealybug I. aegyptiaca had one peak in both years occurred in the second week of September in first year and in second week of October the second year. Two peaks of abundance during the first year 2018 recorded for the associated predator, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae), in June 2nd and in the October 1st. During the second year of study, it had two peaks in June 1st and October 1st. There was simultaneous occurrence of the total population of P. citri and I. aegyptiaca and its associated predator R. cardinalis. Positive correlation between Max., Min. temperatures and the total population of P. citri and I. aegyptiaca was determined. On the other side there were negative correlation of relative humidity and total population during the two years of study.

Introduction These are sucking pest of plant Citrus is the most important sap and secret large amount of the fruit in Egypt as far as its acreage, honey dew which encourage the growth production and exportation potentials of sooty mold fungi, that consequently are concerned (El-Kassas, 1984). reduce the photosynthesis and Mealybugs are serious insect pests, respiration of plant leaves. Usually, attack the citrus trees and cause a occurrence of the sever infestation lead severely considerable damage under the to the death of the whole trees (Radwan, prevailing agroecosystems in Egypt. 2003).

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The citrus mealybug, Planococcus citri was considered as a replicate and 20 (Risso) (Hemiptera: Pseudococcidae) is leaves and five twigs were taken an important pest attacking several randomly from each tree representing crops. Biotic and abiotic factors, as well the four cardinal directions). Samples as the substrate they feed on influence were collected half monthly from early its population (Correa et al., 2005). The January till the end of December during citrus mealy bug infested 65 plant the two successive years 2018 and species belonging to 56 genera in 36 2019. The collected samples were families and distributed in 20 transferred to the laboratory in paper Governorates. P. citri prefers citrus bags for examination by the aid of a followed by guava and grape (Ahmed binocular stereomicroscope, and Abd-Rabou, 2010). Identification of mealybug species and The genus Icerya includes about their insect predator was done by 35 species in the world that are specialists at the Department commonly known as fluted scales of Scale Insects and Mealy bugs, Plant because of the fluted appearance of the Protection Research Institute, Dokki, ovisac. The Egyptian fluted mealybug, Egypt. The mealybug species and their Icerya aegyptiaca (Douglus) associated insect predators for each (Hemiptera: Monophlebidea) has the sample were identified and counted. most distributed in the world and with The upper and lower surfaces of the numerous host plants. It is commonly leaves were carefully examined. The known as Egyptian Icerya, because of it rate of increase/decrease in population is original description from Egypt. This densities was calculated by dividing the monophlebid scale causes considerable mean number of insects found in the damage on Mangifera indica and sample over that found in preceding one tropical fruit trees in Chahbahar as described by (Bodenheimer, 1951). (Moghaddam et al., 2015). Statistical analysis for the data were Therefore, the present study analyzed by using one-way ANOVA by aimed to shedding light on two species Costat software program (2004). of mealybugs infesting navel orange trees and their associated predatory Results and discussion insect as well as their seasonal 1. The population abundance of two abundances in Qalubiya Governorate, mealybug species and their Egypt. And to determine its predator: generations under the studied 1.1. Population density of conditions and the proper time for their Planococcus citri: control. The obtained results in Figure Materials and methods (1) showed that the estimated The present studies were fluctuating densities of the P. citri conducted at a private farm in Qalubiya population indicated three peaks of Governorate, Egypt. All the agricultural infestation in the first year (2018). practice was carried out except the These peaks occurred in June 1st, July insecticide's applications. To evaluate 2nd and August 2nd with values of 320, the seasonal abundance of the 512 and 685 individuals, respectively. mealybug species and their associated In the second year (2019), two peaks predators, 100 navel orange leaves and were recorded on 1st week of July (362 25 twigs were taken from five navel individuals) and 2nd week of September orange trees of the same age and same (457 individuals) as shown in Figure size as half monthly samples (each tree (2).

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800 POPULATION DENSITIES OF P. CITRI ON ORANGE TREES DURING 2018 700

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Figure (1): Population density of Planococcus citri on navel orange trees in 2018.

POPULATION DENSITIES OF P. CITRI ON ORANGE TREES DURING 2019 500

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Figure (2): Population density of Planococcus citri on navel orange trees in 2019. 1.2. Population density of Icerya (Moustafa, 2012) on citrus trees in aegyptiaca: Behira showed that the insect The Egyptian mealybug I. population of P. citri reached maximum aegyptiaca had one peak in the first during May in first and second years, year, occurred in the second week of respectively, also results indicated that September (148 individuals) as shown citus mealybug, P. citri has two peaks in Figure (3). In the second year (2019) on citrus trees in Cairo. Mesbah (2008) one peak was recorded in the second in Egypt recorded P. citri and I. week of October (112 individuals) as aegyptiaca infesting pomegranate and shown in Figure (4). These results are occurred with high numbers during the similar to those of (Ghanim et al., 2013) two seasons 2005 and 2006. Our results who studied the population density of of P. citri disagree with those of mealybug species attacking mandarin (Awadalla, 2017) who recorded two trees. They found that, the highest peak peaks of citrus mealybug P. citri on of P. citri on October while, I. pomegranate trees in Mansoura, and seychellarum and I. aegyptiaca were agreed with those recorded for I. recorded in September during the two aegyptiaca (One peak of abundance years of study. Another study by during 2014 and 2015).

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160 POPULATION DENSITIES OF I. EGYPTIACA ON ORANGE TREES DURING 2018

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Figure (3): Population density of Icerya aegyptiaca on navel orange trees in 2018.

120 POPULATION DENSITIES OF I. EGYPTIACA ON ORANGE TREES DURING 2019

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Figure (4): Population density of Icerya aegyptiaca on navel orange trees in 2019. 1.3. Population density of associated cardinalis had two peaks in June 1st and predator Rodolia cardinalis: October 1st, and represented by 21 and Data illustrated in Figure (5) 35 individuals, respectively as revealed that, R. cardinalis had two illustrated in Figure (5). (Ghanim et al., peaks of abundance during the first year 2013) recorded that this predator 2018, the first one was recorded in the associated with the mealybug species June 2nd (25 individuals) and the second and had three peaks in Mandarin trees peak in the October 1st (32 individuals). at Mansoura district. During the second year of study, R.

POPULATION DENSITIES OF R. CARDINALIS ON ORANGE TREES DURING 2018 and 2019 40 35 30 25 20 15 10 5 0 01-Jan 01-Feb 01-Mar 01-Apr 01-May 01-Jun 01-Jul 01-Aug 01-Sep 01-Oct 01-Nov 01-Dec

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Figure (5): Population density of Rodolia cardinalis on navel orange trees in 2018 and 2019.

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2. Number of annual generations: density of P. citri clearly show that the The mealybug P.citri has three favorable periods for its development annual generations throughout the first and population increase were at April, year of study (2018), and two annual June and September where (MVR) generations throughout the second values averaged 2.1, 2.9 and 1.9, year of study (2019) of the insect respectively as shown in Figure (6). In population under field condition at the second year the highest values of Qalubiya Governorate. During the first (MVR) were in February (1.5), July year of investigation, the percentage of (2.4), and September (1.9) as shown in nymphal population of P.citri recorded Figure (6). Monthly variation rate 84%, 74% and 72.7 % of total (MVR) of population density of I. population through June 1st, July 2nd aegyptiaca illustrated in Figure (7) and August 2nd, respectively. In the 2nd shows that the favorable periods for its year (2019), two annual generations development and population increase existed, in July 1st (79 %) and were at February, July and August September 2nd (74%). The mealybug I. where (MVR) values averaged 1.8, 2.4 aegyptiaca has one annual generation, and 1.6, respectively. In the second year and these results were ensured the highest values of (MVR) were in throughout the two years of study of the February (1.6), March (2.6), and June insect population under field condition (2.1) as shown in Figure (7). These at Qalubiya Governorate. The results are in harmony with (Khalil et percentage of nymph population of I. al., 2011) who found three annual aegyptiaca recorded 67.5% of total generations of the purple scale population in September 2nd and 64.3% Lepidosaphes beckii Newm. of total population in October 2nd in first (Hemiptera: Diaspididae) on navel and second years of study, respectively. orange throughout the two years of Results concerning the Monthly study of the insect population under variation rate (MVR) of population field condition at El-Behaira.

MVR O F P. C I T RI ON ORANGE TREES DURING 2018 A ND 2019

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Figure (6): Monthly variation rate (MVR) of population density of Planococcus citri on navel orange trees in 2018 and 2019.

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MVR O F I. EGYPTIACA ON ORANGE TREES DURING 2018 A N D 2019

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Figure (7): Monthly variation rate (MVR) of population density of Icerya aegyptiaca on navel orange trees in 2018 and 2019. 3. The relationship between ). The results indicate Planococcus citri and Icerya that R. cardinalis is well adapted to I. aegyptiaca and their associated insect aegyptiaca in Egypt (Ragab, 1991). predator Rodolia cardinalis: This work agrees with the findings The obtained results showed recorded by Hamid and Hassanian that there was simultaneous occurrence (1991) who recorded the predator R. of the total population of P. citri and I. cardinals associated with monophlebid, aegyptiaca and its associated predator Icerya spp. R. cardinalis. 4. Effect of prevailing hygro-thermic The obtained results are in agreement condition on the population density with the finding of (Mesbah, 2008) in of Planococcus citri and Icerya Egypt, suggested that, the relationship aegyptiaca: between the predator R. cardinalis and The effect of Max., Min. I. aegyptiaca showed a significant temperatures and relative humidity on difference during the two season 2005 the total population of P. citri and I. and 2006. Also, (Mani and aegyptiaca during the two studied years Krishnamoorthy, 2000) in India, determined positive correlation recorded that, the natural enemies between Max., Min. temperatures and parasitiods and predators effectively the total population (r = 0.51 and 0.53) reduced the population density of P. in the two years of study respectively, citri. Developmental stages of R. while the higher temperatures, the cardinalis have been found to be higher population. On the other side associated with populations of I. there were week negative correlation of aegyptiaca on Ficus nitida trees in the relative humidity and total population Mansoura district of Egypt. The value (r) was -.243 and -0.314 during development of R. cardinalis larvae the two years of study in Qalubiya when reared in culture on Governorate respectively. Ahmed and Icerya aegyptiaca (Douglas) Abd-Rabou (2010) observed that the (Hemiptera: Coccoidea: host plants and temperature greatly Monophlebidae) was significantly influenced on the development of P. faster than that fed on citri and the lowering of temperature Maskell (Hemiptera: Coccoidea: increase the dimension of the mealybug

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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (4): 1067-1074 and lengthen the developmental period. El-Kassas, S.E. (1984): Effect of iron These results agreed with (Zaki et al., nutrition on the growth, yield, (2013) mentioned that there were fruit quality, and leaf significant effects of temperatures on I. composition of seeded balady seychellarum total population during lime trees grown on sandy 2011 and there were insignificant calcareous soils. J. Plant effects of relative humidity during the Nutrition, 7:301-311. two years of study in Qalyubyia and Ghanim, A. A.; Abdel-Salam, A. H.; Giza Governorates. Also, (Moustafa, Elkady, H. A.; El-Nagar, M. 2012) reported that there were E. and Awadalla, H. S. positively high significant correlations (2013): Ecological studies on between I. seychellarum population and some mealybug species both of mean temperature and relative attacking mandarin trees and humidity at Demyaata Governorate. their predatory insects at References Mansoura district. J. Plant Prot. Ahmed, N. H. and Abd-Rabou, S. M. And Path., Mansoura Univ., 4 (2010): Host plants, (3); 303 – 315. geographical distribution, Hamed, A. R. and Hassanien, F. A. natural enemies and biological (1991): Survey of parasitoids studies of the citrus mealybug, and predators of important scale Planococcus citri (Risso) insects, mealybugs and (Hemiptera: Pseudococcidae). whiteflies in Egypt. Egypt, J. Egyptian Acad. J. Bio.l.Sci., 3: Biol. Pest Control, 1 (2): 147- 39- 47. 152. Awadalla, H. S. S. (2017): The Khalil, A. A. D.; EL-Saadany, G. B. ; Population Abundance of the Mansour, M. A.; Hashem, A. Mealybug Species Infesting G. and Darwish, A. A. E. Pomegranate Trees and their (2011): Ecological studies on Associated Insect Predators in the purple , Mansoura Region Egypt. J. Lepidosaphes Beckii Plant Prot. and Path., Mansoura (hemiptera: diaspididae) on Univ., Vol.8 (1), 15– 19. navel orange trees at El-behaira Bodenheimer, F.S. (1951): Additions Governorate, Egypt in 2009 and to the Coccidae of Iran, with 2010 seasons. J.Agric. and descriptions of two new Env.Sci.Dam.Univ.,Egypt , 10 species. Bull. Ent. Soc. D' (1). Egypte, 28:81-84. Mani, M. and Krishnamoorthy, A. Correa, L. R. B.; Souza, B. and (2000): Seasonal incidence of Santa-Cecilia, L. V. C. (2005): major sucking pests of Development of the citrus pomegranate and their relation mealybug Planococcus citri with weather parameters in (Risso, 1813) (Hemiptera: India. Acta Horticulturae, Pseudococcidae) on different 890:589-596. fruit-bearing plants. Arquivos- Mesbah, A. H. (2008): Biological do-Instituto-Biologico-Sao- suppression of mealybugs Paulo, 75(2): 239-242. Planococcus citri Risso and Costat software program (2004): Planococcus lilacinus (Ckll.) on Costat. www.cohort.com pomegranate in India. Indian J. Montery, California, USA. Plant Protection, 28(2):187- 189.

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Moghaddam, M.; Esfandiari, M. and Ragab, M.E. (1991): Adaptation of Khosravi, M. (2015): First Rodolia cardinalis (Mulsant) recorded of I. aegyptiaca (Col., Coccinellidae) to Icerya (Homoptra: Coccoidea: aegyptiaca (Douglas) (Hom., Monophlebidae) from Iran first Margrodidae) as compared with Iranian international Congress Icerya purchasi Mask., Journal of Entomology, 29-31 . of Applied Entomology, 119 (1‐ Moustafa, M. (2012): Scale insects 5): 621-623. (Coccoidae: Hemiptera) Zaki, D.N.; Amin, A. H.; Abdallah, Y. infested citrus trees and their E. Y. and Hassan, N. A., natural enemies, with a key of (2013): Certain ecological these pests in Egypt. Egypt. aspects for Icerya seychellarum Acad. J. biolog. Sci., 5(1): 1- 23 (Westwood) on coffee plants . coffea arabica in Egypt. J. Plant Radwan, S. (2003): Toxicological Prot. and Path., Mansoura studies on some scale insects Univ., 4 (3): 265 – 277. infested mango and guava trees. Ph. D. Thesis, Fac. Agric., Cairo University.

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