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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (3):896 - 905

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

Bionomics of the kirkaldyi (: Aleyrodidae) in Egypt as well as seasonal abundance of this and its on jasmine

EL-Amir, S. M. ; Abd El-Mageed, S. A. M. and Shaaban, Abd-Rabou Plant Protection Research Institute, Agricultural Research Center, Dokki, Giza, Egypt. ARTICLE INFO Abstract: Article History Jasmine is one of the oldest traditional flowers and it Received: 16/7/2020 is an important flowering group of plants which are Accepted: 21 /9/2020 commercially grown for their fragment flowers and oil ______production. The jasmine whitefly Dialeurodes kirkaldyi Keywords (Kotinsky) (Hemiptera: Aleyrodidae) is one of the most Bionomics, jasmine important pest of jasmine all over the world and Egypt. Larvae whitefly, Dialeurodes and adults of this pest suck the sap from the under surface of the kirkaldyi , seasonal leaves and infested leaves turn yellow. The aim of this work is abundance, to study the bionomics of D. kirkaldyi as well as seasonal Eretmocerus corni , abundance of this pest and its parasitoid on jasmine plant . The jasmine and Egypt. results indicated that D. kirkaldyi infested by 12 host plants

distributed in 9 Governorates and recorded associated with 4

in Egypt as well as studies of it was

provided.It also was found infesting jasmine plants at Gharbiya

Governorate, Egypt. To obtain basic ecological data for the

whitefly , D. kirkaldyi and its parasitoid Eretmocerus corni

Haldeman (Hymenoptera: Aphelinidae) every two weeks

intervals throughout two seasons (August to December 2018 and

2019). Seasonal fluctuations of alive total population, nymphs

and adults of D. kirkaldyi throughout the tested year. The

seasonal abundance for both and adult recorded one peak

on middle of October in two seasons. The effects of four

ecological factors (3 abiotic +1 biotic) on the population

dynamics of alive larvae and adult population were estimated.

The parasitoid E. corni showed highly significant correlation

with larvae of D. kirkaldyi by (r= 0.91 and 0.92) in two seasons.

Introduction Jasmine products are important and confectioneries. Even different natural raw materials in the perfume parts of the plants such as leaf, stem, industry. Jasmine flowers are used for bark, root and fruits are also used for making gariands for ceremonial medicinal purposes (Guledagudda et offering, for adoring hair by ladies and al.,1997) . Jasmine trade is estimated to for production of “attar” and concrete in pull in some $6.5 million annually for cosmetic industry. These flowers are Egypt, providing income to around also used in toiletries, food essences, 50,000 people, according to the chewing tobacco, dental preparations International Federation of Essential 896

EL-Amir et al., 2020

Oils and Aroma Trades (AFP, 2020). multitudes of pests Jasmine is infested by several constitutes the most important limiting and mite pests. The lepidopteran pests factor. To overcome these pests, the like bud borer, Hendecasis above mentioned IPM measures can be duplifascialis (Hampson) successfully imposed wherever (; ); bud applicable for the management of pests borer/gallery worm, Elasmopalpus in jasmine. The minimum yield loss jasminophagus (Hampson) caused by these pests can even be (Pyralidae: Lepidoptera), and leaf avoided (Rabeena et al., 2020). webworm, geometralis D. kirkaldyi has a history of (Guenee) (Crambidae; Lepidoptera) spreading internationally. It was first are of major importance. Sucking described in 1907 on Jasminum pests like eriophyid mite, Eryophes grandifolium from Hawaii (Kotinsky, spp (Acarina: Eriophyidae); tingid 1907), although the area of origin of the bug, Corythauma ayyari (Drake) is uncertain (Martin et al., (Hemiptera: ); whitefly, 2000). The nymphs and adults of Dialeurodes kirkaldyi (Kotinsky) whitefly suck the sap from lower (Hemiptera: Aleyrodidae) and flower surface of the leaves in large numbers , Isoneurothrips orientalis and cause yellowing. It invites sooty (Bagn.) (Thysanoptera: Thripidae) mould fungus thereby photosynthesis cause minor damage to the crop. will be affected and reduction in yield Dipteran pest like blossom midge, occurs (Rabeena et al., 2020). Contarinia maculipennis Fabricius It attacked by different host (Diptera: ) sometimes plant species in Egypt and the world by infests the crop (Pal and Abd-Rabou (1996 and 1997) , Evans Chakravarthy, 2020). The most (2007) and Sundararaj and Dubey important pests are , (2006). D. kirkaldyi is a widely specially in the Mediterranean region, distributed species that is found on so it is attacked by 16 species of (Russell , 1964; Sundararaj and David , whiteflies ; These are Aleuroclava 1992; Evans, 2007 and Chiun-Cheng et jasmini (Takahashi), al., 2010). Also is a mainly tropical and dispersus Russell , Aleurolobus sub-tropical oligophagous whitefly of bidentatus Singh, sp. , relatively little importance to UK Plant Aleurotrachelus trachoides (Back) , Health. Its main hosts are Jasminum giffardi (Kotinsky) , Bemisia species. It is already present in the EU jasminum David & Subramanian , (Portugal and Cyprus) (Mifsud et al., Bemisia tabaci (Genn.) , Dialeurodes 2010). citri (Ashmead), Dialeurodes kirkaldyi As a potential pest of , (Kotinsky) , Dialeurodes sp. , southern EU MS should be aware of Dialeurodes vulgaris Singh, this organism. It is likely to spread Minutaleyrodes minutus (Singh) , within the Mediterranean region. Citrus Singhiella citrifolii (Morgan), Singhius producing regions should monitor the hibisci (Kotinsky) and scientific literature for further vaporariorum (Westwood) . The information on this organism. The most dangerous pest of them is D. kirkaldyi favoured hosts, on which high numbers (Hemiptera: Aleyrodidae). The several of D. kirkaldyi can be found, are biotic and abiotic factors are Jasminum spp. and Morinda citrifolia responsible for low productivity and (Evans and Bennett, 1996 and Martin et quality deterioration of jasmine al., 2000). Also, it was found on production, but the damage caused by several species of host plants in Florida,

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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (3):896 - 905 including citrus, but high populations of The aim of this work is to study this whitefly are only known to occur the taxonomy, host plants , distribution on jasmine species (Nguyen et al., and parasitoids of D. kirkaldyi as well 1993). as seasonal abundance of this pest and However, immature stages and its parasitoid on jasmine plant . adults do cause damage by feeding on Materials and methods plant sap (Nguyen and Hamon, 1989). 1. Survey of host plants, distribution Larvae and adults of this pest suck the and parasitoids of the jasmine sap from the under surface of the leaves whitefly Dialeurodes kirkaldyi: and infested leaves turn yellow and is A survey of the jasmine associated with vectoring yellow ring whitefly D. kirkaldyi host plants , mosaic disease of jasminum distribution and parasitoids were carried (Mariappan and Ramanujam, 1975 and out in different locations in Egypt Mound, 1983). throughout two successive years. Nguyen et al. (1993) and Samples of infested leaves and Polaszek et al. (1999) recorded one branches with D. kirkaldyi . The parasitoid species, samples were packed in paper bags and protransvena Viggiani (Hymenoptera: transferred to the laboratory for Aphelinidae), has been reported from examination. The examined leaves were D. kirkaldyi. Evans and Bennett (1996) enclosed in plastic jars covered with recorded Eretmocerus rosei Evans and muslin held in position by a rubber Bennett for the first record of an band and kept under preferential Eretmocerus species that has been conditions for securing any emergence reared from this whitefly species, and of parasitoids. The parasitoids were only the second record of an collected, sorted into species and Eretmocerus species that attacks this preserved in vials contain 70 % ethyl whitefly genus. Denmark (1964) alcohol and glycerin, in addition to reported on the introduction of an slide mounting species for undetermined species of the genus identification. Eretmocerus into Florida as a natural 2. Seasonal abundance of the jasmine enemy of the citrus whitefly whitefly Dialeurodes kirkaldyi: Dialeurodes citri (Ashmead). It was carried out for 2 years, Eretmocerus corni Haldeman (August till December ,2018 and 2019) (Hymenoptera: Aphelinidae) is one of at Gharbiya Governorate, Egypt. A the most important parasitoids farm about one Fadden in area, associated with whitefly species and cultivated with jasmine and heavily first recorded in Egypt by Priesner and infested with D. kirkaldyi was chosen Hosny (1940). It is recorded associated for this study. The farm was not with 16 host whitefly and 14 countries exposed to any chemical treatment of the world and 3 whitefly species in 6 during three years prior to the present Governorates in Egypt (Abd-Rabou, study and during the investigation 1998c). The three whitefly hosts, B. period. Every15 day-intervals 30 leaves tabaci , phillyreae (Haliday) with different stages of the whitefly, D. and Trialeurodes ricini ( Misra ). In kirkaldyi were collected at random from 1998, Abd-Rabou and Abou-Setta the different directions of jasmine plant. recorded seven parasitoids attacking S. The leaves represented the different phillyreae one of them E. corni. Also, sides, peripheral, inner zones, lower and Abd-Rabou (1998 a,b,c and 2002) middle of the plant. These leaves were recorded this species associated with B. kept in a paper bag and transferred to tabaci and T. ricini. the laboratory for examination and

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EL-Amir et al., 2020 counting the whitefly . The 1.2.1.Synonyms : stages of whitefly insect considered in Aleyrodes (Dialeurodes) Cockerell counting process were larval and 1902: 283. Type species. Aleyrodes adults . citri Riley and Howard 1893, by 3. Seasonal abundance of the original designation, a synonym of A. parasitoid Eretmocerus corni citri Ashmead 1885. associated with the jasmine whitefly Dialeurodes Cockerell; full genus, Dialeurodes kirkaldyi: Quaintance and Baker 1914: 97. Jasmine leaves infested with Kanakarajiella David and Sundararaj larval instars of D. kirkaldyi were half 1993. Type species. Dialeurodes monthly ,(30 leaves /15 days ) from vulgaris Singh 1931, by original August till December ,2018 and 2019. designation; synonymy according to Each leaf was stored in well-ventilated Martin and Mound 2007: 28. glass emergence tube for its parasitoid Lankaleurodes David 1993: 23. Type emergence that its numbers were species. Dialeurodes radiipuncta recorded daily was calculated. Samples Quaintance and Baker 1917, by 30 leaves randomly selected whitefly original designation; synonymy were chosen. These samples according to Martin and Mound 2007: represented larval instars, . Each larval 28. whitefly was removed, transferred and Shanthiniae David 2000, in P.M.M. mulched on a slide in a water film. David 2000: 125. Type species - 4. Effect of biotic and abiotic factors Shanthiniae sheryli David 2000, by on the abundance the jasmine monotypy and original designation; whitefly Dialeurodes kirkaldyi: synonymy according to Martin and Weather factors as maximum, Mound 2007: 28. minimum temperature and relative Dialeurodes (Rabdostigma) humidity were considered from Central Quaintance and Baker 1917: 426, Laboratory for Agricultural Climate. Dialeurodes (Gigaleurodes) Quaintance The weekly maximum and minimum and Baker 1917: 426, and Dialeurodes temperatures as well as relative (Dialeuroplata) Quaintance and humidity were calculated and total Baker 1917: 435 number of parasitiods. Multiple Dialeuronomada Quaintance and regressions were conducted for weather Baker; full genus by Sundararaj and factors combined as well as plant age as David, 1991. described. The obtained determination 1.2.2. Diagnostic characters: factor (R2) of E.V. % was used to Pupal case dark brown or explain the effect of testing factors. yellowish, puparial outline not laterally Process Correlation and Regression indented abdominally ; puparial margin were used in SAS to analysis the smooth, or more coarsely crenulate. obtained date (SAS Institute, 1998). Thoracic and caudal tracheal openings Results and discussion at margin in form of distinct 1. Taxonomy of Dialeurodes invaginated pores which are smooth or kirkaldyi: finely crenate internally. Vasiform 1.1. Order: Hemiptera orifice relatively small, subcircular Suborder :‎‎ posterior margin often with small Superfamily: Aleyrodoidea median tubercle. Operculum usually Family : Aleyrodidae concealing lingula. Inner margins Genus : Dialeurodes toothed or smooth. Species: kirkaldyi 1.2.3. Key to Genus Dialeurodes 1.2. Genus Dialeurodes Cockerell members in Egypt: 899

Egypt. J. Plant Prot. Res. Inst. (2020), 3 (3):896 - 905 1. Subdorsal setae not extending : Jasminum grandiflorum, beyond margin of pupal case. Anterior Jasminum officinale, Jasminum rim short, length about one-eighth of sambac. Ranuculaceae: Ranuculus length of vasiform repens. Rubiaceae: Coffea sp., Coffea orifice…………………...Dialeurodes arabica. elbaensis Priesner & Hosny 2.2.In World: Apocynaceae: -Subdorsal setae different. Anterior rim Allamanda neriifolia, Beaumontia long…..………………………….….2 grandiflora, Plumeria acuminata, 2. 1st abdominal setae present. A brown Plumeria acutifolia, Tabernaemontana area, in the median area of the dorsum. sp., Trachelospermum jasminoides; The margin of vasiform orifice without Combretaceae: Terminalia sp.; median tubercle posteriorl..Dialeurodes Ebenaceae: Diospyros kaki, Ebenaceae: kirkaldyi (Kotinsky) Diospyros sp., Diospyros virginiana; -1stabdominal setae absent. No brown Geraniaceae: Pelargonium sp.; area in the median area of the dorsum. Jugandaceae: Juglans regia; Lauraceae: The margin of vasiform orifice with Persea americana; Loganiaceae: median tubercle posteriorlyDialeurodes Fagraea fragrans; Lythraceae: citri (Ashmead) Lagerstroemia indica; Malpighiaceae: 1.3. Dialeurodes kirkaldyi (Kotinsky) Hiptage benghalensis, Hiptage 1.3.1.Synonyms : madablota; Malvaceae: Malva Aleyrodes kirkaldyi Kotinsky 1907: 95- sylvestris; Oleaceae: Jasminum 96. Syntypes. USA: Hawaii, on amplexicaule, Jasminum arabica, unidentified trailing shrub. Jasminum auriculatum, Jasminum Beaumontia grandifolia, Morinda biflorum, Jasminum multiflorum, citrifolia and Jasminum grandiflorum, Jasminum nitidum, Jasminum USNM. officinale, Jasminum sambac, Dialeurodes kirkaldyi (Kotinsky); Jasminum volubile, Oleaceae: Quaintance and Baker 1914: 98. Jasminum frutiscens, Ligustrum Dialeurodes yercaudensis Jesudasan walkeri, Syringa sp.?; Rubiaceae: and David 1991: 307. Coffea arabica, Coffea sp., Gardenia 1.3.2. Dignostic characters: tahitiensis, Jasminum sambac, Morinda Median line of puparium often citrifolia, Morinda royoc; Rutaceae: pigmented brownish (examine several); Citrus sinensis, Citrus x paradisi; A brown area, in the median area of the Verbenaceae: Clerodendrum fragrans, dorsum; first abdominal setae present Premna integrifolia. but very small ; eighth abdominal setae 3. Distribution of Dialeurodes opposite, or posterior to, widest part of kirkaldyi : operculum . The margin of vasiform 3.1. In Egypt: Alexandria, Assiut, orifice without median tubercle Aswan, Cairo, Gharbiya, Giza, Ismailia, posteriorly, vasiform orifice toothed; Portsaid and Qalyubiya. pale species with median thoracic 3.2. In World: Australia, Azores, pigmentation. Submarginal setae Bahamas, Barbados, Burma, Caroline absent. Is., China, Cook Is., Costa Rica, Cuba, 2. Host plants of Dialeurodes Egypt, Fiji, Ghana, Greece, Guam, kirkaldyi: Guyana, Hawaii, Hong Kong, India, 2.1. In Egypt : Combretaceae: Iran, Israel, Jamaica, Japan, Lebanon, Terminalia sp., Terminalia chebula. Malaysia, Mexico, Pakistan, Covolvulaceae: Convolvulus arvensis. Philippines, Puerto Rico, Samoa, Sri Malvaceae: Malva rotundifolia, Malva Lanka, Syria, Tahiti, Taiwan, Thailand, silvestri. Myrtaceae: Pisdium guava. Trinidad, Turkey, UK, USA.

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EL-Amir et al., 2020 4.Parasitiods of Dialeurodes kirkaldy : E. corni showed highly significant 4.1. In Egypt: Aphelinidae: Encarsia correlation with larvae of D. kirkaldyi lutea (Masi) , Encarsia protransvena by (r= 0.91 and 0.92) in two seasons. Viggiani, Eretmocerus corni Haldeman 7. Effect of biotic and abiotic factors and Eretmocerus mundus (Mercet). on the abundance of Dialeurodes 4.2. In World: Aphelinidae: Encarsia kirkaldyi: abundantia Chou & Su, E. bothrocera We studied the effect of a biotic Huang and Polaszek, E. dialeurodis factor as parasitoid (Biotic) and abiotic Hayat, E. lahorensis (Howard) , E. factors maximum, minimum lutea (Masi), E.neoporteri Myartseva temperature and relative humidity. and Evans , E. nigricephala Dozier, E. Correlation, regression analysis and perflava Hayat, E. protransvena multi regression between biotic and Viggiani, Encarsia sp., E. strenua abiotic factors and population of D. (Silvestri) , E.strenua group, E. kirkaldyi was in liner degree, in two tabacivora Viggiani,, Eretmocerus years of study 2018 and 2019. portoricensis Dozier, Er. rosei Evans Statistically, the results represented in and Bennett, Eretmocerus sp. Table (3) showed the effect of the 5. Seasonal abundance of the weather factors (maximum, minimum jasmine whitefly Dialeurodes temperature and relative humidity) kirkaldyi: activity of D. kirkaldyi. With the Data presented in, (Tables 1 and respect to abiotic factors had significant 2) illustrated that larvae and adults effect on the population of the larval stages curves had one peak during the stage of D. kirkaldyi in two years of first year, (2018) and the second year study, while adult had significant effect (2019) on jasmine leaves. In the first on the population with maximum year, (2018) the peak of larvae recorded temperature in two years of study 2018 on (15th of October) with 1019 and 2019 (Tables 1 and 2). El- individuals (30 leaves ) and the peak of Borollosy et al. (1990) tested the effect adult recorded on (15th of October), of maximum and mean temperature as with 422 individuals (30 leaves ). While well as mean percentage of relative in the second year (2019) the peak of humidity on D. kirkaldyi abundance larvae also, recorded on (15th of they stated that these three factors had October) with 1028 individuals (30 influence on the population density of leaves ) and the peak of adult recorded this whitefly species, this influence on (15th of October), with 430 differed significantly from one individuals (30 leaves ). Helmi (2005) influence on the population density of D. kirkaldyi had three annual field this whitefly species, this influence generations which lasted 170, 90 and differed significantly from one weather 100 days, respectively. factor to another and from one season 6. Seasonal abundance of the to another. Later Helmi (2005) parasitoid Eretmocerus corni obtained results of statistical analysis associated with the jasmine whitefly for the effects of some ecological Dialeurodes kirkaldyi: factors on the population dynamics of The parasitoid E. corni is an D. kirkaldyi nymphs revealed that effective parasitoid which keeps maximum, minimum and mean populations of the D. kirkaldyi under temperature had high positive control in Egypt. In the first year (2018) significant effects on nymph seasonal. and the second (2019),the highest peak While mean percentage of relative was observed in 15th of October in two humidity had positive insignificant years (Tables 1 and 2). The parasitoid effects.

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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (3):896 - 905 Table (1) : Total population the jasmine whitefly Dialeurodes kirkaldyi and number of its parasitoid Eretmocerus corni on jasmine at Gharbiya Governorate during the first year 2018. Date Mean number of Dialeurodes Mean number of Climatic Factors kirkaldyi Eretmocerus corni

larvae Adults Max. Min. Mean Temp. ₒC Temp. ₒC RH.% 1 August 35.4 22.6 58.1 650 212 187 15-Aug 813 419 199 35.2 21.9 58.8 1 Sep. 939 390 243 33.8 21.3 61.5 15 Sep. 963 399 260 33.9 20.8 62.7 1 Oct. 995 412 322 31.4 19.7 62.1 15 Oct. 1019 422 436 30.2 18.8 63.1 1 Nov. 643 271 302 27.1 17.7 61.8 15 Nov. 635 268 232 26.1 16.4 57.3 1 Dec. 543 231 101 21.0 15.0 58.3 15 Dec. 553 235 15 18.3 14.1 57.0 Table (2): Total population the jasmine whitefly Dialeurodes kirkaldyi and number of its parasitoid Eretmocerus corni on jasmine at Gharbiya Governorate during the second year 2019. Date Mean number of Dialeurodes Mean number of Climatic Factors kirkaldyi Eretmocerus corni

Larvae Adults Max. Min. Mean Temp. ₒC Temp. ₒC R.H.%

1 August 701 190 175 35.8 20.7 59.7

15-Aug 822 428 207 35.7 22.7 59.6

1 Sep. 948 398 251 35.4 21.1 60.5

15 Sep. 971 408 269 33.7 20.7 61.7

1 Oct. 1004 421 330 34.1 19.9 62.7

15 Oct. 1028 430 444 31.6 18.9 63.9

1 Nov. 651 280 310 28.6 17.5 62.1

15 Nov. 644 277 240 27.4 16.2 58.5

1 Dec. 551 240 109 26.1 15.1 59.1

15 Dec. 561 244 20 20.4 14.6 60.6

Table (3) : The simple correlation and regression coefficients and multiple regressions between the different stages of Dialeurodes kirkaldyi , climatic factors and Eretmocerus corni in 2018 and 2019 years. 902 EL-Amir et al., 2020

Factors Simple correlation and regression Multiple regression

R P B E.V % 2018 2019 2018 2019 2018 2019 2018 2019 Max. Temp. ₒC 0.67 0.71 0.036 0.022 21.2 26.1 79.58 80.77

Min. Temp. ₒC 0.60 0.71 0.068 0.021 38.6 48.4

Mean R.H.% 0.82 0.66 0.003 0.038 66.0 72.3

ae Eretmocerus corni 0.75 0.75 0.012 0.012 1.2 1.2 v

All above 80.05 82.12 lar Max. Temp. ₒC 0.59 0.53 0.072 0.112 8.8 9.7 63.78 59.23 Min. Temp. ₒC 0.52 0.61 0.126 0.059 15.6 20.8

0.72 0.55 0.020 0.101 26.8 29.8 s Mean R.H.% t Eretmocerus corni 0.65 0.65 0.043 0.043 0.5 0.5

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