567-576 Issn 2077-4613

Middle East Journal of Applied Volume : 08 | Issue :02 |April-June| 2018 Sciences Pages: 567-576 ISSN 2077-4613

Seasonal Abundance and Host Preference of Most Insect Pests and Predators Associated With Certain Citrus Trees

Asmaa M. Abd-Elghaffar, Gamila Sh. Selem, I.M. Kelany and Shadia M. Omara

Plant Prot. Dept., Fac. Agric., Zagazig Univ., Egypt Received: 14 Feb. 2018 / Accepted: 30 April 2018/ Publication date: 20 May 2018

ABSTRACT This investigation was carried out in order to study the seasonal abundance and host preference of the most insect pests and predators existing on the three citrus tree hosts (sweet orange, navel orange and mandarin) and intercropping plants among them in different citrus orchards at Minia Alkamh district, Sharkia Governorate, Egypt during two successive years extended from December 2012 to November 2014. Host preference through the effect of epidermal cell thickness of the three studied citrus tree host leaves on the seasonal abundance of Aonidiella aurantii (Maskell), Chrysomphalus aonidum (L.) and Phyllocnistis citrella Stainton was investigated. The results showed that 9 insect pests belong to 6 families and 3 orders and 3 predaceous species belong to 2 families and 2 orders were recorded. The highest population of all pests and predators was exhibited in the second year (9403 and 217individual/ sample) than the first one (7823and 114 individual/ sample), respectively. P. citrella Stainton, A. aurantii (Maskell) and C. aonidum (L.) were the dominant species on citrus tree hosts which collected by plant sample technique. Empoasca decipiens (Paoli) was the most common insect pest and Chrysoperla carnea (Stephens) was the most common predators collected by sweep net on intercropping eggplant and mallow plants among the three citrus tree hosts. Seasonal abundance of the two scale insects had negative relationship with citrus leaf epidermal cell thickness where showed that sweet orange was the attractive host to infestation with the main scale insects.

Key words: Seasonal abundance, host preference, pests, predators, citrus tree hosts.

Introduction Citrus is one of the most important members of the family Rutaceae and ranked first among fruit crops in Egypt as farasitsacreage, production and exportation potentials are concerned (El-Kassas, 1984). Citrus trees subjected for injuries by many insect pests were studied in Egypt by many authors (Morsi, 1999; Tawfeek, 2007; Tawfeek and Abu-Shall, 2010; Moustafa, 2012; Tawfeek, 2012; Mogahed et al., 2013; Abo-Alnor et al., 2016 and El-Maghraby et al., 2016). A large number of pests are found on citrus (Uygunet al., 1992). Diaspididae family, which has the maximum species number with approximately 2,400 species, cause important damage by feeding on plants (Miller and Davidson, 2005). Further studies are needed to assess the relation between leaf epidermal cell thickness of citrus tree hosts and the population density of scale insects and the citrus leaf miner. Therefore the present study was contributed towards a better knowledge of the following: 1-Seasonal abundance of the main insect pests infested the three citrus tree hosts and intercropping plants among them and associated insect predators. 2-Host preference through the effect of epidermal cell thickness of the three studied citrus tree host leaves on the seasonal abundance of the main insect pests.

Materials and Methods These investigations were carried out at Minia Alkamh district, Sharkia Governorate, Egypt during the two successive years, 2012/2013 and 2013/2014 in citrus orchards of area about 20 feddans (more than 12 years old). This farm cultivated with the three citrus trees hosts (sweet orange, Citrus

Corresponding Author: Gamila Sh. Selem, Plant Prot. Dept., Fac. Agric., Zagazig Univ., Egypt E-mail:[email protected] 567 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613 sinensis, navel orange, Citrus sinensis and mandarin, Citrus reticulate that belong to family Rutaceae and order Geraniales). One feddan was selected for each citrus tree host to collect the samples. Eggplant, Solanum melongena (Solanales: Solanaceae) and mallow, Corochorus olitorius (Malvales: Tiliaceae) were intercropped among these citrus trees.

Seasonal population of the dominant insect pests by using plant sample technique:

Three citrus trees in each tested host which nearly similar in size and vegetation were selected per feddan. The plant sample technique (25 leaves/ tree) was used for collecting the insect species on leaves of sweet orange, navel orange and mandarin trees from main directions (north, south, east and west) and inner at early morning at weekly intervals during the period from December 2012 to November 2014. Weekly samples were kept in tightly closed paper bags and transferred to the laboratory in the same day for examination and counting the total number of the insect pests by the aid of stereoscopic microscope.

Seasonal population of the main insect pests and associated insect predators by using insect sweep net:

Sweep net technique were used to carried out in order to study the seasonal population of the main insect pests on intercropping plants (eggplant and mallow) among citrus tree hosts and associated insect predators. The used sweep net was 30 cm diameter and 60 cm deep. Each sample consisted of 50 double strokes was taken randomly at early morning during weekly intervals from both diagonal directions of the experimental area (about 100 m2). Each sample was kept in a tight closed paper bag and transferred to the laboratory for inspection by stereoscopic microscope. The insect pests and associated insect predators in the collected samples were classified and counted.

Host preference of insect pests infested certain citrus trees:

The anatomical studies carried out during 2013 - 2014 in the laboratory of Botany Department, Faculty of Agriculture, Zagazig University to study the effect of leaf epidermal cell thickness on the infestation of the main insect pests (A. aurantii, C. aonidum and P. citrella) according to Johanson, (1940); Corgan and Widmoyer, (1970) ; Saeed, (1992).

Results and Discussion

Seasonal population of dominant insect pests and associated insect predators on the three citrus tree hosts and intercropping plants:

The obtained data compiled in Table 1 revealed that there were 12 insect species belong to 8 families and 5 orders associated with the three citrus tree hosts and intercropping plants during the two years of the study. Insect pests were represented by 9 species belong to 6 families and 3 orders and predaceous insects composed of 3 species belong to 2 families and 2 orders. The homopterous insect pests were Aonidiella aurantii (Maskell), Chrysomphalus aonidum (L.), Empoasca decipiens (Paoli), Empoasca decedens (Paoli), Cicadulina chinai Ghauri and Toxoptera aurantii (Boyer de Fonscolombe) belong to three families. Order Lepidoptera included two insect pest species; Phyllocnistis citrella Stainton and Vanessa cardui Linnaeus belong to 2 families, Gracillariidae and Nymphalidae, respectively. Order Hemiptera composed one insect pest species, Nezara viridula (L.) belong to family Pentatomidae. The citrus leaf miner, P. citrella was the dominant insect pest species which ranked the first pest on the three citrus tree hosts constituting dominance of46.19% of the total number of all insect pests, followed by A. aurantii (43.66%), C. aonidum (5.09), E. decipiens (1.46%), T. aurantii (1.06%), C. chinai (0.88%), E. decedens (0.80%), V. cardui (0.53%) and the at least was N. viridula (0.33%). Similar trends were found by Kamel (2010) who recorded that thirteen insect pest species belong to 8 families: Aphididae, Coccidae, Margarodidae, Diaspididae, Anthomyidae, Aleyrodidae, Thripidae and Drosophilidae attacking citrus trees (balady and navel orange) at Qalyubiyah Governorate, Egypt.

568 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613

Moustafa (2012) and Tawfeek (2012) recorded that the most serious scale insects infested citrus trees were the red scale and the black scale. Knapp et al. (1995), Elkady (2005) and Latif et al. (2013) mentioned that Phyllocnistis citrella infested different hosts of citrus trees. Abo-Alnor et al. (2016) added that leafhopper insect species included Empoasca decipiens, E. decedens, Cicadulina chinai infesting navel orange, mandarin trees in Diarb-Nigm District, Sharkia Govemorate, Egypt.

Table 1: List of the main insect pests and associated predators with the three citrus tree hosts and intercropping plants at Minia Alkamh district, Sharkia Governorate from December 2012 to November 2014. Feeding Sample Order Family Species Host plant Grand Dom. behaviour technique total %

Navel orange, Plant A. aurantii Phytophagous sweet orange & 7521 43.66 sample mandarin Diaspididae Navel orange, Plant C. aonidum Phytophagous sweet orange & 877 5.09 sample mandarin

Eggplant & Sweep E. decipiens Phytophagous 251 1.46 mallow plants net Homoptera

Eggplant & Sweep Cicadellidae C. chinai Phytophagous 152 0.88 mallow plants net

Eggplant& Sweep E. decedens Phytophagous 138 0.80 mallow plants net T. aurantii Eggplant & Sweep Aphididae Phytophagous 183 1.06 mallow plants net Navel orange, Plant Gracillariidae P. citrella Phytophagous sweet orange & 7957 46.19 sample Lepidoptera mandarin V. cardui Eggplant& Sweep Nymphalidae Phytophagous 91 0.53 mallow plants net Eggplant& Sweep Hemiptera Pentatomidae N. viridula Phytophagous 56 0.33 mallow plants net

Grand total 17226 100.00 Eggplant& Sweep Neuroptera Chrysopidae C. carnea Predator 237 71.60 mallow plants net

Eggplant& Sweep C.undecimpunctata Predator 53 16.02 mallow plants net Coleoptera Coccinellidae Eggplant& Sweep S. interruptus Predator 41 12.38 mallow plants net Grand total 331 100.00 Dom. %= Dominance %

Regarding the predators that surveyed by using sweep net, the present data showed that the neuropterous predators were one species, Chrysoperla carnea (Stephens) belong to family Chrysopidae. The coleopterous predators were the least all orders in number during the two years and included two species Coccinella undecimpunctata (Linnaus) and Scymnus interruptus (Goeze) belong to one family (Coccinillidae). Such findings are in agreement with that of Abd Allah (1988) who recorded that coleopterous predators, Coccinella undecimpunctata & Scymnus interruptus and neuropetrous predator, Chrysoperla carnea fed on scale insects infesting citrus in Mansoura region. Hamed and Hassanein ( 1991) reported nine predators belong to Coccinellidae and Chrysopidae. Chrysoperla carnea larvae were very common and polyphagous predator feeding on many scale insects. El-Agamy et al. ( 1994)

569 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613 mentioned that Chrysoperla carnea was associated with different species of many scale insects in Kafr El-Sheikh. Michaud and Browning (1999) added that coccinellids and chrysopids were recorded as predators on brown citrus aphid in Puerto Rico. Moreover, Mohamed (2002) found that predatory coccinellid species were associated with Aonidiella aurantii.

Seasonal population of the main insect pests in tested citrus orchards by using plant sample:

Obtained results in Table 2 showed the population dynamic of insect species that surveyed on the three citrus tree hosts by using plant sample during two years of 2012 / 2013 and 2013 / 2014. It is clear that the most dominant species were arranged descendingly according to their relative densities as follows: P. citrella, A. aurantii and C. aonidum. The citrus leaf miner, P. citrella was the most insect pest species which ranked the first pest on the three citrus tree hosts constituting dominance of 48.62% and 48.67% in the two studied years, consecutively by general dominance of 48.65% of the total number of the three insect pests during the two years. The obtained results agree with that of Kamel (2010) who reported that significant numbers of scale insects and leaf miners were found on the citrus trees (balady and navel orange) at Qalyubiyah governorate, Egypt. El-Maghraby et al. (2016) showed that significant differences in infestation rates with citrus leaf miner P. citrella, where navel orange recorded the highest followed by valencia orange, mandarin, sweet orange, balady orange and sour orange at Ismailia and Sharkia governorates, Egypt. The california red scale insect, A. aurantii ranked the second pest constituting dominance of 46.16 % and 45.84%in 2012/2013 &2013/2014, respectively by general dominance of 45.99%. These results partially agree with that of El- Rahman et al. (1979) who found that the hosts of the red scale insect A. aurantii could be arranged as follows: lemon, sour orange, navel orange and mandarin. The black scale insect, C. aonidum ranked the third pest representing by 5.22% and 5.48% in the two years, respectively by general dominance of 5.36%. The results agree with that of Moustafa (2012) who recorded that the most serious scale insects infesting certain citrus trees were the california red scale, the citrus wax scale and the black scale. Data also, appeared that sweet orange was the most attractive citrus tree hosts to infestation by these studied pests, whereas the occurrence percentages were 49.61% and 48.67% on sweet orange followed by 32.74% and 32.22% on navel orange and at the least 17.65% and 19.11% on mandarin in the two years of the study, respectively. These results are in accordance with that of Elkady (2005) who stated that balady mandarin was the least infestation and navel orange was moderately infested host.

Seasonal population of the main insect pests and associated predators intested citrus orchards by using sweep net:

Data in Table 3 appeared the population dynamic of insect species and associated predators that surveyed on intercropping plants among the three citrus tree hosts by using sweep net during two years, 2012 / 2013 and 2013 / 2014. These results showed that the highest dominant insect pest was E. decipiens (30.77% and 26.41) followed by T. aurantii (28.48% and 11.79%), C. chinai (20.58% and 13.59%), E. decedens (9.56% and 23.59%), V. cardui (4.78% and 17.44%) and N. viridula (5.82% and 7.18%) was the lowest one. Results also, showed that navel orange was the most attractive citrus tree hosts to infestation by the studied pests, whereas the occurrence percentages were 46.99% and 42.05%on navel orange followed by 33.68% and 32.05% on sweet orange and at the least 19.33% and 25.90% on mandarin in the two years of the study, respectively.The results are harmony with those recorded by some authors such as Herakly(1970); Abd-Elsamad (1999) and Malik et al., (2010) who stated that the sweep net proved to be the best technique to collect the leafhopper insects on navel orange and mandarin. Hegab et al. (2014) added that collected leafhopper species were arranged descendingly according to their abundance as follows: Empoasca decipiens, E. decedens, E. lybica (De Berg) Balclutha hortensis (Lindb) and Cicadulina chinai. The results in Table 3 also showed that the most dominant associated predators were arranged descendingly according to their abundance as follows: C. carnea, C. undecimpunctata and S. interruptus. These predators were existed by dominance of 57.02% & 79.26%, 25.44% &11.05% and

570 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613

Table 2: Total number and dominance percentage of the insect pests on the three citrus tree hosts by using plant sample at Minia Alkamh district, Sharkia Governorate during 2012/2013 and 2013/ 2014. 2012 / 2013 2013 / 2014 General Host plant Host plant Insect pest Total Dom. Total Total Sweet Sweet Navel Dom. (%) Dom. (%) Navel orange Mandarin No. (%) Mandarin No. No. orange orange orange P. citrella 848 1789 933 3570 48.62 1026 2131 1230 4387 48.67 7957 48.65 A. aurantii 2550 514 325 3389 46.16 3070 646 416 4132 45.84 7521 45.99 C. aonidum 244 101 38 383 5.22 291 127 76 494 5.48 877 5.36 Grand total 3642 2404 1296 7342 100.00 4387 2904 1722 9013 100.00 16355 100.00 Occ.% 49.61 32.74 17.65 100.00 48.67 32.22 19.11 100.00 Dom. %= Dominance % Occ.% = Occurrence%

Table 3: Total number and dominance percentage of the insect pests and associated predators on intercropping plants by using sweep net at Minia Alkamh district, Sharkia Governorate during 2012/2013 and 2013/ 2014. 2012 / 2013 2013 / 2014 General Intercropping plant among: intercropping plant among: Insect pest Total Total Total Navel Dom. (%) Navel Dom. (%) Dom. (%) Sweet orange Mandarin No. Sweet orange Mandarin No. No. orange orange E. decipiens 34 90 24 148 30.77 34 48 21 103 26.41 251 28.82 T. aurantii 23 86 28 137 28.48 19 15 12 46 11.79 183 21.01 C. chinai 65 20 14 99 20.58 11 28 14 53 13.59 152 17.45 E. decedens 19 15 12 46 9.56 18 41 33 92 23.59 138 15.84 V. cardui 10 7 6 23 4.78 34 20 14 68 17.44 91 10.45 N. viridula 11 8 9 28 5.82 9 12 7 28 7.18 56 6.43 Grand total 162 226 93 481 100.00 125 164 101 390 100.00 871 100.00 Occ.% 33.68 46.99 19.33 100.0 32.05 42.05 25.90 100.0 Predator C. carnea 23 16 26 65 57.02 63 34 75 172 79.26 237 71.60 C. undecimpunctata 8 11 10 29 25.44 6 10 8 24 11.05 53 16.01 S. interruptus 6 9 5 20 17.54 5 8 8 21 9.67 41 12.38 Grand total 37 36 41 114 100 74 52 91 217 100 331 100.00 Occ.% 32.46 31.58 35.96 100.00 34.10 23.96 41.94 100.0

571 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613

17.54% & 9.67% in both years of the study, respectively. Also, the obtained results showed that C. carnea was the most dominant predator on citrus trees by general dominance of 71.60% followed by C. undecimpunctata by 16.01% and S. interruptus by 12.38%. The highest occurrence percentages of these predators were recorded on mandarin by 35.96% and 41.94% followed by 32.46% and 34.10% on sweet orange and finally by 31.58% and 23.96% on navel orange in the two years of the study, respectively.The present results partially agree with that of Yoldas et al. (2011) who found that Chrysoperla carnea and Coccinella septempunctata were predators associated with Toxoptera aurantii in four Satsumamand arinorchards in İzmir, Turkey. Abd- Rabou et al. (2012) recorded many insect species as predators of scale insects in Egypt, of them Coccinella undecimpunctata, Chrysoperla carnae and Scymnus interruptus. It could be concluded that there were negative relationship between the populations of each the main pests and the associated predators on intercropping plants among the three citrus tree hosts by using sweep net technique, where the decreasing in the population density of main pests may be due to the increasing in the population density of associated predators.

Seasonal population of the two scale insects infesting the three citrus tree hosts during the four seasons of the year:

The highest general dominance percentages of each of the two scale insects, A. aurantii and C. aonidum on the three citrus hosts were recorded in winter and the lowest one was represented in summer during the two years of the study (Table 4). The highest general percentages of the two scale insects in the four seasons during 2012/2013 and 2013/2014 were38.65% in winter followed by19.65% in spring, 16.75% in summer and 24.95% in autumn. The highest general percentage of the two scale insects was found on sweet orange by73.98% and 72.65% followed by16.31% and 16.71% on navel orange and 9.71% & 10.64%on mandarin in the two years of the study, respectively. These results disagreed with that of Abul- Nasr and Swailem (1975) who reported that the highest level of population density of A. aurantii on citrus tree stook place during April in Qaluobea & during September in Menofia and Giza, and during May, June in Gharbeia and Sharkia. The population reached the minimum levels in most of the regions of study in winter. Rizk et al. (1978) recorded that all stages of A. aurantii on citrus were presented throughout the year. Swailem et al. (1980) found that the populations of the scale insect increased during late summer and autumn and were smallest during winter.

Host preference of insect pests infested certain citrus trees:

The anatomical studies carried out to study the effect of leaf epidermal cell thickness (upper and lower surface) on the infestation of the main insect pests (A. aurantii, C. aonidum and P. citrella) during 2013 / 2014.

A. aurantii (Maskell):

Results given in Table 5 showed that the highest annual total number of the california red scale insect, A. aurantii infesting sweet orange was 3070 insects/ sample influenced by the lowest mean of upper surface of leaf epidermal cell thickness of 14.79µm and lower surface of 9.23µm. When the mean of upper surface of leaf the epidermal cell thickness increased to 17.95µm and lower one to 12.36µm, the annual total number of A. aurantii decreased to 646 insects/ sample on navel orange. Mandarin had the highest means of upper (19.40µm) and lower (13.04µm) leaf epidermal cell thickness and the lowest annual total number of A. aurantii (416 insects/ sample).

C. aonidum (L.):

Data represented in Table 5 showed that the same trend of the relationship between the thickness of epidermal cells and the annual total number of A. aurantii was observed for C. aonidum. The highest annual total number of C. aonidum infesting sweet orange (291 insects/ sample) influenced

572 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613

Table 4: Population density of A. aurantii and C. aoniduminfesting the three citrus tree hosts during the four seasons from December 2012 to November 2014 by using plant sample at Minia Alkamh district, Sharkia Governorate.

Total number of scale insects on: 2012/ 2013 2013/ 2014 General Date Sweet orange Navel orange Mandarin Total no. % Total no. % Total no. % season (month) 2012/ 2013/ 2012/ 2013/ 2012/ 2013/ 2013 2014 2013 2014 2013 2014 Winter Dec. 177 172 35 34 28 39 Jan. 405 455 63 89 52 77 1535 40.72 1710 36.96 3245 38.65 Feb. 616 661 104 119 55 64 Total number 1198 1288 202 242 135 180 Spring Mar. 324 371 55 86 12 52 Apr. 162 267 18 37 7 15 619 16.42 1031 22.29 1650 19.65 May 16 127 16 46 9 30 Total number 502 765 89 169 28 97 Summer June 146 159 63 83 22 20 July 102 146 33 43 25 24 629 16.68 777 16.80 1406 16.75 Aug. 176 224 30 43 32 35 Total number 424 529 126 169 79 79 Autumn Sept. 285 305 98 79 40 50 Oct. 222 344 59 88 62 73 987 26.18 1108 23.95 2095 24.95 Nov. 158 130 41 26 22 13 Total number 665 779 198 193 124 136 Grand total 2789 3361 615 773 366 492 3770 4626 8396 100.00 General % 73.98 72.65 16.31 16.71 9.71 10.64 100.00 100.00

573 Middle East J. Appl. Sci., 8(2): 567-576, 2018 ISSN 2077-4613 by the lowest mean thickness of the upper and lower surfaces of leaf epidermal cells (14.79 and 9.23µm). When the thickness of upper and lower leaf surfaces of the epidermal cells increased to 17.95 and 12.36µm, respectively, the annual total number of C. aonidum decreased to 127 insects/ sample on navel orange. The lowest annual total number of C. aonidum (76 insects/ sample) was represented on mandarin when the mean thickness of upper and lower leaf surfaces of the epidermal cells were the highest (19.40µm and 13.04µm, respectively).

Table 5: Effect of leaf epidermal cell thickness of the citrus tree hosts on the population densities of the two scale insects and the citrus leaf miner at Minia Alkamh district, Sharkia Governorate during the second year 2013/2014. Thickness of leaf epidermal Annual total number Citrus tree host cell (µm) Upper surface Lower surface A. aurantii C. aonidum P. citrella Sweet orange 14.79 9.23 3070 291 1026 Navel orange 17.95 12.36 646 127 2131 Mandarin 19.40 13.04 416 76 1230

Generally, it could be mentioned that there was negative relationship between the thickness of leaf epidermal cells and the infestation level of the two scale insects. According to the obtained data, it could be concluded that sweet orange was the most attractive host but mandarin was the least attractive citrus tree hosts to infestation by the two scale insects.

P. citrella Stainton:

Results summarized in Table 5 indicated that no clear relation was found between thickness of epidermal cell and the infestation by P. citrella, which may be due to larvae mouth parts which is chewing type not piercing and sucking mouth parts such as in scale insects. The obtained result are in agreement with those of Hegab (2001); El-Gindy (2002); Hashem (2005); Abd-Elsamad (2006) and Abo- Alnoret al. (2016) who mentioned that the population density of the piercing-sucking insects were affected with the epidermal cell and sub epidermis cells wall.

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