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Host and natural enemies of Bemisia tabaci (: Aleyrodidae) in

ARTICLE in SCIENCE · JANUARY 2011 Impact Factor: 2.14 · DOI: 10.1111/j.1744-7917.2010.01395.x

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ORIGINAL ARTICLE Host plants and natural enemies of Bemisia tabaci (Hemiptera: Aleyrodidae) in China

Shao-Jian Li1,XiaXue1, Muhammad Z. Ahmed1, Shun-Xiang Ren1, Yu-Zhou Du2, Jian-Hui Wu1, Andrew G. S. Cuthbertson3 and Bao-Li Qiu1 1Department of Entomology, South China Agricultural University, Guangzhou, 2School of Horticulture and Protection, Yangzhou University, Yangzhou, Jiangsu Province, China, 3The Food and Environment Research Agency, Sand Hutton, York, UK

Abstract The sweetpotato , Bemisia tabaci, has been a destructive pest in China for over the past two decades. It is an extremely polyphagous insect, being recorded feeding on hundreds of host plants around the world. Potential host plants and natural enemies of B. tabaci in the south, southeast, middle, north and northwest of China were investigated during the last decade. In total 361 plant species from 89 families were recorded in our surveys. Plants in the families Compositae, Cruciferae, Cucurbitaceae, Solanaceae and Leguminosae were the preferred host species for B. tabaci, which therefore suffered much damage from this devastating pest due to their high populations. In total, 56 species of parasitoids, 54 species of predators and seven species of entomopathogenic fungi were recorded in our surveys. Aphelinid parasitoids from and Eretmocerus genera, lady and lacewings in Coleoptera and Neuroptera were found to be the dominant arthropod predators of B. tabaci in China. The varieties of host plant, their distribution and the dominant species of natural enemies of B. tabaci in different regions of China are discussed. Key words Bemisia tabaci, China, host plant, natural enemy, survey

Introduction and their products is considered as one of the key reasons for this pests’ global invasion (Dalton, 2006; Qiu et al., Invasive insect pests can greatly affect the community 2007a). structure of native and cause substantial damage in Bemisia tabaci was first recorded in China in the late agricultural and forest ecosystems (Pimentel et al., 2000). 1940s (Chou, 1949), but it was not considered a seri- Among these invasive pests, the sweetpotato whitefly, ous pest until outbreaks were recorded in the mid-1990s, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), which were due to the invasion of the B biotype (Wu et al., has been found globally distributed except in Antarctica 2003; Qiu et al., 2007a). Previous investigations have re- (De Barro, 1995; De Barro et al., 2000; De Barro et al., ported that this pest can damage a wide range of host 2005). B. tabaci remains a serious pest of many agri- plants, including vegetables, economic crops and orna- cultural and ornamental crops worldwide, being recorded mental plants; for example, Avidov and Harpaz (1969) re- on a large range of host plant species (Nomikou et al., ported 52 host plants in Israel, Azab et al. (1971) reported 2001; Cuthbertson et al., 2007). Furthermore, the in- 172 plant species in Egypt and Gameel (1972) recorded creasing international trade and transportation of plants 115 plants of B. tabaci in Sudan. On a global basis Mound and Halsey (1978) reported 420 host plant species in 74 families and Greathead (1986) recorded more than 500 Correspondence: Bao-Li Qiu, Department of Entomology, host plant species worldwide. Recently, Gelman et al. South China Agricultural University, Guangzhou 510640, (2005) reported that B. tabaci can attack more than China. Tel: +86 20 85283717; fax: +86 20 85280316; email: 600 species of host plants in both field and greenhouse [email protected] settings, including food, fiber and ornamentals.

C 2011 The Authors 101 Journal compilation C Institute of Zoology, Chinese Academy of Sciences 102 S. J. Li et al.

In China, the earliest report concerning host plants of B. southeast (Fujian, Jiangsu, Zhejiang), north (Beijing), tabaci was by Chang (1969) who recorded 87 host plant northwest (Xinjiang) and the middle of China () species in Taiwan. Afterwards, Luo et al. (2000) reported from 1999 to 2009. The investigated plants included veg- 74 species (including variants) in 24 families in Beijing. etables, ornamentals, economic crops and trees, as Qiu et al. (2001) recorded 176 plant species in 46 families well as weeds on farmland, roadsides and hills. in the Guangzhou area. In the investigations of Zhou et al. Host plants with whitefly adults, eggs and nymphs si- (2003) and He et al. (2003), 101 species in 31 families multaneously present on the same plant or with “pupae” and 62 species in 17 families were recorded in Jiangsu (a short term of pharate adult) were recorded. During the and Fujian Provinces, respectively. Moreover, 103 species surveys, 15 (five from the top, middle and bottom, of B. tabaci host plants were reported by Zhang et al. respectively) of one plant were removed and taken back to (2005) in Shanxi Province. Although there are several the laboratory where the B. tabaci nymphs and pupae on published investigations concerning the host plants of B. the leaves were examined under a binocular microscope. tabaci in China (Luo et al., 2000; Qiu et al., 2001; He The plant species were identified by Dr. Tong-Xing Sun et al., 2003; Zhou et al., 2003; Zhang et al., 2005; Xu (Qingdao Agricultural University, China). The whitefly et al., 2007a; Xu et al., 2007b), providing essential and species were identified either according to the morphol- important information in the development of biological ogy of the pupa stage or by comparing their mitochondrial and integrated management strategies for the pest, all of cytochrome oxidase I (mtCOI) sequencing with B. tabaci them were in very localized regions or at the most limited (Qiu et al., 2009b). to one or two provinces. To date, no survey has been reported concerning the host ranges of B. tabaci nation- Natural enemies investigation wide in China. Bemisia tabaci continues to show an increasing level During the investigation of natural enemies, the leaves of resistance to a range of chemical insecticides, includ- with parasitized whitefly nymphs or pupae were put into ing imidacloprid, pyrethroid, acetamiprid and nitenpyram Petri dishes and taken back to the laboratory. Predatory (Morin et al., 2002; Horowitz et al., 2008; Byrne et al., lady beetles, lacewings and bugs were captured by remov- 2010; Feng et al., 2010; Schuster et al., 2010). Several ing the plant leaves gently and placing the living insects recent studies in China have shown that most of the rou- either into Petri dishes or directly into 95% ethanol. The tine pesticides available have lost their effectiveness in B. emerged parasitoids were identified by Dr. Jian Huang tabaci control (He et al., 2009; Qiu et al., 2009a; Wang (Fujian Agriculture and Forestry University, China) and et al., 2009). Therefore, there is an urgent need for the the predatory natural enemies were identified by Dr. development of alternative means of control. Biological Shun-Xiang Ren in the Department of Entomology, South control agents and associated technologies have now be- China Agricultural University (SCAU). Collected ento- come the main areas of research in B. tabaci management mopathogenic fungi were incubated, isolated and identi- studies over the last two decades (Huang & Polaszek, fied by Dr. Qiong-Bo Hu in SCAU and Prof. Zong-Qi 1998; Gerling et al., 2001; Ren et al., 2001; Huang, 2002; Liang in Guizhou University, China. All the specimens of Cuthbertson & Walters, 2005; Qiu et al., 2007b, 2008; natural enemies collected were kept in SCAU. Cuthbertson et al., 2008, 2010; Stansly & Naranjo, 2010). Some references about host plants and natural enemies In this study, we list the results of two systematic surveys of B. tabaci were also cited in current surveys. outlining the host plant species and natural enemies of B. tabaci recorded throughout China. The latter survey in- cludes both insect natural enemies and entomopathogenic Data analysis fungi. This report will provide a clear understanding of the current status of both the host plant species and natural The infestation rate of host plants by B. tabaci was enemies of B. tabaci in China. evaluated according to the average population level of B. tabaci nymphs and pupae on the leaves. To make the sample size uniform, the whitefly nymphs and pupae pop- Materials and methods ulations per were converted to numbers in 10 cm2/leaf area, irrespective of the size and type of leaves of differ- Host plants investigation ent plant species (Attique et al., 2003). The infestation rates of host plants were categorized as four grades; they The host plants and natural enemies of B. tabaci were were recorded as 4th grade when the average number investigated in south (, , ), of B. tabaci nymphs and pupae were more than 50 in

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 Plants and natural enemies of Bemisia tabaci 103 the 10 cm2/leaf area; recorded as 3rd grade when the species Amitus longicornis and A. hesperidum. Among nymphs and pupae were between 31–50 individuals in the the aphelinid parasitoids, one species of Ablerus genus 10 cm2/leaf area; recorded as 2nd and 1st grades when was recorded along with 41 and 12 species of Encarsia the nymphs and pupae were between 11–30 or ≤ 10 in- and Eretmocerus parasitoids, respectively. dividuals in the 10 cm2/leaf area, respectively (Qiu et al., 2001). The predatory of B. tabaci in China

Results In total, 54 species of predatory arthropods were recorded as natural enemies of B. tabaci in China, in- Host plants of B. tabaci in China cluding 23 species of lady beetles, 16 species of spiders, seven species of lacewings, six species of predatory bugs The results of our field surveys showed that the host in the Anthocoridae, one species in the Nitidulidae and plants of B. tabaci in China are abundant. In total, 361 one species in the Staphylinidae, among which, lady bee- plant species (including variants) belonging to 89 families tles were the dominant populations in the field surveys were recorded during these surveys (Table 1). The 89 fam- (Table 4). The predators were sampled across the en- ilies included nine families in which the host plant species tire geographical area of China, but overall the species were more than 10 species and four families with more diversity and richness was most abundant in the south, than 20 plant species. The largest number of plant species southeast and middle of China. was found in the family Compositae with 44 species, followed by 26 species in the family Leguminosae, 23 species in the family Cruciferae and 22 species in the Entomopathogenic fungi for control of B. tabaci in China family Solanaceae. Nineteen species were found in the family Cucurbitaceae (Table 2). During the surveys, seven species of entomopathogenic As for the types of host plants, 153 of the 361 species fungi that can infest B. tabaci were collected and identi- were ornamentals and , 80 species were vegeta- fied. Among them, five species belonged to Hyphomyc- bles, and 63, 43 and 22 species were weeds, economic erales, including Beauveria bassiana, Paecilomyces crops and , respectively. According to the num- aleyrodis, Paecilomyces farinosus, Paecilomyces fu- bers of B. tabaci nymphs and pupae, 28 species were mosaroseus, Lecanicillium muscarium and two species recorded in the 3rd grade of infestation rates; among belonged to Sphaeropsidales, Aschersonia aleyrodis and them were eight species in the Cruciferae, six in the Aschersonia placenta. All the seven species of ento- Cucurbitaceae, four in the Compositae, three in the mopathogenic fungi were widely distributed in the south, Solanaceae, two in the Leguminosae and Euphorbiaceae, southeast, middle, north and northwest of China. and one species in the Malvaceae and Polygonaceae (al- though not included in the top 10 families in Table 2). Discussion Eleven species were recorded in the 4th grade of in- festation rates; among them were four species in the A full understanding of both the range of host plants and Solanaceae, three in the Cucurbitaceae and one each in the natural enemy status of B. tabaci through a systematic Cruciferae, Euphorbiaceae, Leguminosae and Malvaceae sampling process is the basis for developing B. tabaci (Table 2). Results from the surveys indicated that host integrated pest management strategies. Much work has plants in the families Compositae, Cruciferae, Cucur- been done in this area in different regions of the world bitaceae, Solanaceae, as well as Leguminosae were the (Avidov & Harpaz, 1969; Chang, 1969; Azab et al., 1971; most preferred hosts for B. tabaci and as a result suffered Gameel, 1972; Mound & Halsey, 1978; Greathead, 1986; the most damage. Luo et al., 2000; Qiu et al., 2001; Attique et al., 2003; He et al., 2003; Zhou et al., 2003; Gelman et al., 2005; Zhang Parasitoids of B. tabaci in China et al., 2005). In the current investigations, 361 species of host plants were recorded, among which 242 species The results of natural enemy surveys indicated that there were found in south China, followed by 213 species and were 56 parasitoid species that can parasitize B. tabaci in 165 species in southeast and middle China. The larger China. All of them are hymenopteran wasps (Table 3). abundance of host plants in south China maybe due to the The recorded parasitoids belong to two families, Aphe- higher temperature in this area which can lead to a greater linidae and Platygasteridae, but the latter only has two richness of plant biodiversity.

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 104 S. J. Li et al.

Table 1 The host plants of Bemisia tabaci in China.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

1 Acanthaceae Adhatoda vasica b,g OM,N 1 2 Barleria cristata c WS 1 3 Pachystachys lutea h OSE 1 4 Sunchegia nolilis b,g OM,N 1 5 Aceraceae Acer buergerianum c,g OS,M 1 6 Acer palmatum b,c,g O S,M,N 1 7 Agavaceae Agave americana b,c O S,N,NW 1 8 Aizoaceae Mollugo pentaphylla c,g ES,M 1 9 Amaranthacea Achyranthes aspera c WS 1 10 Alternanthera philoxeroides a,e W SE 2 11 Amaranthus caudatus g OM 1 12 Amaranthus mangostanus a,c,d,g,,h VS,SE,M 1 13 Amaranthus retroflexus c,g WS,M 1 14 Amaranthus spinosus a,c,g WS,SE,M 1 15 Amaranthus tricolor c,g VS,M 2 16 Amaranthus viridis a,c,g WS,SE,M 1 17 Celosia argentea c WS 1 18 Celosia argentea L.CV. phunosa b,c,f OS,SE,N 1 19 Celosia cristata c,e,f,g OS,SE,M 1 20 Gomphrena globosa b.c O S,N,NW 1 21 Amaryllidaceae Hippeastrum vittatum b ON,NW 1 22 Lycorisradiate b ON 1 23 Apocynaceae Allamanda cathartica c OS 1 24 Catharanthus roseus b,c,f OS,SE,N 1 25 Nerium indicum b,c,g O S,M,N 1 26 Plumeria rubra b,g OM,N 1 27 Vinca major b,c,g,f O S,M,N,SE 1 28 Vinca major ‘Variegata’ b,c,g,f O S,M,N,SE 1 29 Aquifoliaceae Llex latifolia b ON 1 30 Araceae Alocasia macrorrhiza b,c OS,N 1 31 Caladium bicolor b ON 1 32 Colocasia esculenta c,d,e,h VS,SE 1 33 Philodendron selloum h FSE 1 34 Scindapsus aureus h OSE 1 35 Spathiphyllum palls h OSE 1 36 Syngonium barry b ON 1 37 Araliaceae Fatsia japonica f OSE 1 38 Hedera helix c,f,h WS,SE 1 39 Polyscias carolorum b ON 1 40 Asclepiadaceae Dischidia nummularia c OS 1 41 Telosma cordarum b,f,g O M,N,SE,NW 1 42 Averrhoaceae Averrhoa carambola c FS 1 43 Balsaminaceae Impatiens balsamina b,c,e,f,g O S, SE, M, N 1 44 Basellaceae Basella rubra f,h VSE 2 45 Begoniaceae Begonia ravenii b,g OM,N 1 46 Begonia simperflorens h OSE 1 47 Berberidaceae Berberis thunbergii b,g OM,N 1

to be continued

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 Plants and natural enemies of Bemisia tabaci 105

Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

48 Nandina domestica f ESE 1 49 Bignoniaceae Campsis grandiflora c,f,g O S,M,SE 1 50 Bombacacceae Ceiba pentandra c OS 1 51 Pachira macrocarpa c,e,g,h OS,SE,N 1 52 Boraginaceae Ehretia microphylla c OS 2 53 Buxaceae Buxus harlandii c,f OS,SE 1 54 Buxus megistophylla c,f,g OS,SE,M 1 55 Buxus sinica c,f FS,SE 1 56 Caesalpiniaceae Cassia suffruticosa b,c,g O S,M,N 1 57 Cassia surattensis c OS 1 58 Campanulaceae Campanula rapunculus b,g EM,N 1 59 Cannabinaceae Humulus scandens a,b,c,e,g,h W S, SE, M, N 2 60 Capparidaceae Cleome spinosa b,g OM,N 1 61 Caprifoliaceae Lonicera japonica b,c,g ES,SW,M,N1 62 Lonicera sempervirens b,g OM,N 1 63 Caricaceae Carica papayac FS 1 64 Celastraceae Euonymus bungeanus b,f ESE,N 1 65 Chenopdiaceae Chenopodium album c,g WS,M 1 66 Chenopodium ambrosioides c WS 1 67 Spinacia oleracea a,b,c,d,e,f V S, SE, M, N 1 68 Combretaceae Quisqualis indica b EN 1 69 Commelinaceae Setcreasea purpurea f,h OSE 1 70 Zebrina pendula b,g OSE,N 1 71 Compositae Ageratum conyzoides a,c WS,SE 1 72 Bellis perennis b,g OM,N 1 73 Bidena bipinnata c WS 1 74 Bidens pilosa a ESE 1 75 Calendula officinalis c,f,g OS,SE,M 2 76 Cerbera jamesonii c,e,f,h OS,SE 3 77 Chrysanthemum cornarium a,b,c,d,f,g,h V S, SE, M, N 1 78 Chrysanthemum morifolium c,f,h OS,SE 3 79 Chrysanthemum nankingensis e,h VSE 1 80 Cichorium intybus b,g WM,N 1 81 Cirsium japonicum c,e,f,g WS,SE,M 2 82 Cirsium setosum b,g WM,N 1 83 Conyza bonarinsisc WS 2 84 Cosmos sulphureus c,f OS,SE 2 85 Dahlia pinnate c,f,g,h OS,SE,M 2 86 Dendranthema chanetii c,g OS,M 2 87 Dendranthema indicum b,c,g,f W S, SE, M, N 2 88 Eclipta prostrate a,c,h WS,SE 2 89 Emilia sonchifolia c WS 1 90 Erigeron breviscapus f ENW 1 91 Erigeron canadensis a,c,e WS,SE 1 92 Gynura crepidioides c,g WS,M 1 93 Helianthus annuus b,c,e,g E S, SE, M, N 2 94 Helianthus tuberosus f,h OSE 1

to be continued

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Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

95 Lactuca brevirostris c WS 1 96 Lactuca sativa var. angustana b,g V SE, M, N 2 97 Lactuca sativa var. asparagina c,d,h VS,SE 1 98 Lactuca sativa var. capitata c VS 1 99 Lactuca sativa var. crispa b,c,d,g V S, SE, M, N 2 100 Lactuca sativa var. longifolia b,c,d,g,h V S, SE, M, N 2 101 Melampodium ‘Lemon Delight’ c,f,g OS,SE,N,NW 2 102 Osteospermum ecklonis c,f,g O S, SE, M, 2 103 Siegesbeckia glabrescens c WS 1 104 Siegesbeckia orientalis a,c WS,SE 1 105 Sonchus arvensis b,c,g,h W S, SE, M, N 2 106 Sonchus oleraceus b,c,g VS,M,N 3 107 Synedrella nodiflora c WS 1 108 Tagetes erecta b,c,e,f,g,h O S, SE, M, N 3 109 Tagetes patula b,c OS,N 2 110 Taraxacum mongolicum c,e,g WS,SE,M 1 111 Wedelia chinensis a,c WS,SE 1 112 Xanthium sibiricum a,c,e,h WS,SE 1 113 Youngia japonica c WS 1 114 Zinnia elegans f,h WSE 1 115 Convovulaceae Calystegia hederacwa b,g WM,N 1 116 Dichondra repens c,g WS,M 1 117 Ipomoea aquatica a,c,d,f,h VS,SE 1 118 Ipomoea batatas a,c,e,f,g,h ES,SE,M 2 119 Pentas lanceolata h OSE 1 120 Pharbitis nil e,f,h WSE 1 121 Quamolit coccinea c,f,g OS,SE,M 1 122 Quamolit pennata b,g OM,N 1 123 Cornaceae Aucuba japonica c,f OS,SE 3 124 Crassulaceae Crassula arborescens c,g OS,M 1 125 Hylotelephium erythrostictum b WN,NW 1 126 Kalanchoe blossfeldiana f,h OSE 1 127 Sedum adolphii b,f OSE,N 1 128 Cruciferae alboglabra a,c,e,g VS,SE,M 4 129 Brassica campestris ssp. chinensis var. communis a,b,c,d,e,f,g,h V S, SE, M, N 3 130 Brassica campestris ssp. chinensis var. utilis c VS 2 131 Brassica campestris ssp. var. pekinensis a,b,c,d,e,f,g,h VS,SE,M 3 132 Brassica campestris b,c,f,g V S, SE, M, N 2 133 Brassica chinensis a,c,f VS,SE 1 134 Brassica juncea var. capitata a,c,d,e,g,h VS,SE,M 3 135 Brassica juncea var. foliosa a,b,c,d,e,f,g,h V S, SE, M, N 1 136 Brassica juncea var. megarrhiza c VS 1 137 Brassica juncea var. multiceps d,f,g,h VSE,M 3 138 Brassica juncea var. tumida VNW 1 139 Brassica oleracea var. acephala b,d,e,g,h V SE, M, N 3 140 Brassica oleracea var. botrytis a,b,c,d,e,f,g V S, SE, M, N 3 141 Brassica oleracea var. capitata a,b,c,d,e,g,h, V S, SE, M, N 1

to be continued

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Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

142 Brassica oleracea var. caulorapa b,c,f,g V S, SE, M, N 3 143 Brassica oleracea var. italica b,c,e,g V S, SE, M, N 2 144 Capsella bursapastoris c,d,e,h VS,SE 2 145 Daucus carota d,f VSE 1 146 Nasturtium officinale c VS 1 147 Raphanus sativus var. longipinnatus a,b,c,d,e,f,g,h, V S, SE, M, N 3 148 Rorippa dubia c WS 2 149 Rorippa indica h WSE 1 150 Youngia japonica c VS 2 151 Cucurbitaceae Benincasa hispida var. chiehqua c VS 2 152 Benincasa hispida a,b,c,d,e,f,g VS,SE,M 2 153 Citrullus lanatus a,b,c,d,e,f,g FS,SE,M 2 154 Cucumis melo var. conomon c VS 4 155 Cucumis melo var. flexuosus c,d,e,g,h VS,SE,M 3 156 Cucumis melo b,c,d,e,g,h V S, SE, M, N 3 157 Cucumis sativus b,c,f,g V S, SE, M, N 3 158 Cucurbita moschata a,b,c,e,f,g V S, SE, M, N 2 159 Cucurbita moschata var. meloformis h VSE 4 160 Cucurbita moschata var. toonas h VSE 4 161 Cucurbita pepo a,b,c,d,g,h V S, SE, M, N 3 162 Lagenaria cylindrica c VS 2 163 Lagenaria siceraria c,g VS,M 3 164 Lagenaria siceraria var. hispida a,d,f,h VSE 1 165 Luffa acutangulac VS 2 166 Luffa cylindrica a,b,d,e,g,h V SE, M, N 2 167 Momordica charantia a,b,c,e,g V S, SE, M, N 3 168 Sechium edule a,c,f VS,SE 2 169 Trichosanthes anguina b,g VM,N 1 170 Cuscutaceae Cuscuta chinensis a WSE 171 Dioscoreaceae Dioscorea opposite c,e VS,SE 1 172 Ebenaceae Diospyras discdot b,g OM,N 1 173 Diospyros kaki c,e,f,g FS,SE,M 1 174 Ericaceae Rhododendron simsii c,e,f OS,SE 2 175 Euphorbiaceae Acalypha australis c,f,h WS,SE 1 176 Acalypha wilkesiana b,c,g OS,M,N 2 177 Alchornea trewioides c OS 1 178 Codiaeum variegatumc,h OS,SE 3 179 Euphorbia heterophylla c OS 1 180 Euphorbia hirta a WSE 2 181 Euphorbia humifusa h OSE 2 182 Euphorbia milii c,h WS,SE 1 183 Euphorbia pulcherrima b,c,e,g,h O S, SE, M, N 4 184 Jatropha podagrica b ON 1 185 Manihot esculenta c ES 2 186 Ricinus communis c,e,f,g,h ES,SE,M 1 187 Sauropus macranthus c OS 3

to be continued

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Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

188 Geraniaceae Geranium wilfordii c WS 1 189 Pelargonium hortorum f,h OSE 2 190 Pelargonium odoratissimumf ONW 1 191 Gesneriaceae Columnea gloriosa b,g OM,N 1 192 Hamamelidaceae Lorpetalum chinense var. rubrum b ON,NW 1 193 Iridaceae Iris tectorum b,c,g O S,M,N 1 194 Labiatae Coleus blumei h WSE 1 195 Leonurus artemisia c ES 1 196 Mentha haplocalyx b,c,e,g,h E S, SE, M, N 1 197 Perilla frutescens c,e ES,SE 1 198 Salvia splendens b,c,e,f,g,h O S, SE, M, N 1 199 Scutellaria baicalensis b,g OM,N 1 200 Scutellaria barbata c,f,g O S,M,NW 1 201 Lardizabalaceae Sargentodoxa cuneata c ES 1 202 Leguminosae Albizzia julibrissin c,f,g OS,SE,M 2 203 Arachis hypogaea a,c,e,h ES,SE 2 204 Astragalus sinicus b,g EM,N 1 205 Cassia surattensis g OM 1 206 Cassia tora c,f OS,SE 1 207 Cercis chinensis b,f,g,h O SE, M, N 1 208 Glycine max a,c,d,e,f,g,h VS,SE,M 3 209 Glycine soja c,h VS,SE 1 210 Lablab purpureus c,d,e,g,h VS,SE,M 2 211 Medicago sativa b,g EM,N 2 212 Millettia reticulata c ES 1 213 Mimosa pudica b,c,f,g O S, SE, M, N 1 214 Pachyrrhizus erosus c VS 1 215 Phaseolus angularis d,h ESE 1 216 Phaseolus aureus a,c,d,e,g VS,SE,M 3 217 Phaseolus vulgaris a,c,d,g,h VS,SE,M 4 218 Pisum sativum a,c,d,e,f,g VS,SE,M 1 219 Psophocarpus tetragonolobus a VSE 2 220 Pueraria lobata c,e,h ES,SE 2 221 Pueraria thomsonii c,h VS,SE 2 222 Robinia pseudoacacia c,f OS,SE 1 223 Sophora japonica f. pendula b,c,g O S,M,N 1 224 Sophora japonicum b,c,g O S,M,N 1 225 Trifolium repens b,c,f OS,SE,N,NW1 226 Vigna radiata c,e,g VS,SE,M 2 227 Vigna unguiculata a,b,c,d,e,g,h V S, SE, M, N 2 228 Liliaceae Asparagus officinalis c,f VS,SE 1 229 Asparagus setaceus c OS 1 230 Dracaena fragrans var. victoria c,g,h OS,SE,M 1 231 Liriope palatyphylla b,g WM,N 1 232 Ophiopogon japonicus b,g EM,N 1 233 Lythraceae Cuphea lanceolata c WS 1 234 Lagerstroemia indica b,c,g O S,M,N 1

to be continued

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 Plants and natural enemies of Bemisia tabaci 109

Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

235 Woodfordia fruticosa c OS 1 236 Magnoliaceae Chlorophytum comosum c,f,g OS,SE,M 1 237 Hosta plantaginea b,c,f,g O S, SE, M, N 1 238 Hosta ventricosa c,g OS,M 1 239 Liriodendron chinense c,f,g FS,SE,M 1 240 Magnolia denudate c OS 1 241 Magnolia grandiflora c,f,g OS,SE,M 1 242 Michelia maudiae c,g OS,SE 1 243 Malvaceae Abelmoschus moschatus c OS 1 244 Abutilon theophrasti b,g EM,N 3 245 Gossypium hirsutum b,c,g,h E S, SE, M, N 2 246 Hibiscus mutabilis c OS,SE 2 247 Hibiscus esculentus a,c,h VS,SE 2 248 Hibiscus rosa-sinensis b,c,e,g,h O S, SE, M, N 4 249 Hibiscus rosa-sinensis var. cooperi b,g OM,N 2 250 Hibiscus syriacus f O1 251 Leonurus artemisia b,g EM,N 1 252 Malva crispa b,g EM,N 2 253 Sida rhombifolia c OS 2 254 Urena lobata a WSE 1 255 Meliaceae Melia azedarach c,f ES,SE 1 256 Toona sinensis b,c,e,f V SE, M, N 2 257 Moraceae Broussonetia papyrifera b,c,g OS,M,N 1 258 Ficus carica c,e,f,g FS,SE,M 1 259 Ficus hispida c OS 1 260 Ficus religiosa b,g OM,N 1 261 Morus alba c,f,g,h ES,SE,M 1 262 Musaceae Musa acuminata c FS 1 263 Myrtaceae Eucalyptus urophylla c ES 1 264 Psidium guajava c FS 1 265 Nepenthaceae mirabilis c OS 1 266 Fraxinus szaboana c,f ES,SE 1 267 Jasminum mesnyi b,c,g OS,M,N 1 268 Jasminum nudiflorum b,c,f OS,SE,N 2 269 Jasminum sambac c,f,h ES,SE 1 270 Ligustrum lucidum c,f OS,SE 1 271 Ligustrum quihoui c,f OS,SE 1 272 Ligustrum vicaryi c,g OS,M 1 273 Osmanthus fragrans b,c,f,g O S, SE, M, N 1 274 Onagraceae Jussiaea linifolia a WSE 1 275 Ludwigia prostrate a WSE 1 276 Orichidaceae Chlorophytum comosum f,h OSE 1 277 Oxalidaceae Oxalis corniculata c,e,f WS,SE 1 278 Paeoniaceae Paeonia lactiflora b,c,f,g O S, SE, M, N 1 279 Palmae Rhapis excelsa c,f OS,SE 1 280 Passifloraceae Passiflora edulis c OS 1 281 Pedaliaceae Sesamum indicum g,h ESE,M 1

to be continued

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Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

282 Phytolaccacea Phytolacca americana f OSE 1 283 Platanaceae Platanus acerifolia b,f OSE,N 1 284 Polygalaceae Polyala chinensis c ES 1 285 Polygonaceae Polygonum chinensisc ES 1 286 Polygonum orientale f,g OSE,M 1 287 Polygonum perfoliatum a,e WSE 3 288 Rheum palmatum c,f ES,SE 1 289 Portulaceae Portulaca grandiflora b,c,f OS,SE,N 1 290 Portulaca oleracea f,h WSE 1 291 Punicaceae Punica granatum c,e,f,g FS,SE,M 1 292 Ranunculaceae Ranunculus asiaticus c OS 1 293 theezans b,g OM,N 1 294 Ziziphus zizyphusb,f,g F SE, M, N, NW 1 295 Rosaceae Amygdalus persica f,h FSE 1 296 Amygdalus triloba b ON 1 297 Cerasus pseudocerasus c,f,g FS,SE,M 1 298 Eriobotrya japonica c FS 1 299 grandiflora c,e,f,h FS,SE 1 300 Kerria japonicaf,g OSE,M 1 301 Malus halliana e,f OSE 1 302 Malus pumila b,f,g F SE, M, N 1 303 Pyracantha fortuneana c,f OS,SE 1 304 Pyrus bretschneideri b,f,g F SE, M, N 1 305 Rosa chinensis c,e,f,g,h OS,SE,M 2 306 Rosa multiflora b,g OM,N 1 307 Rosa rugosa c,e,f,g,h OS,SE,M 2 308 Spiraea japonica c,f OS,SE 2 309 Rubiaceae Gardenia jasminoides c,e OS,SE 1 310 Gardenia jasminoides var. dortu c OS 1 311 Hedyotis auricularia c WS 1 312 Hamelia patens c OS 1 313 Rutaceae Citrus madurensis c FS 1 314 Clausena lansium c FS 1 315 Forunella margarita c.e,f FS,SE 1 316 Murraya paniculata c OS 1 317 Zanthoxylum bungeanum f,g ESE,M 1 318 Sapindaceae Koelreuteria paniculata c,f OS,SE 1 319 Sapotaceae Manilkura zapota b,g OM,N 1 320 Saxifragaceae Hydrangea macrophylla c,g OS,M 1 321 Scrophulariaceae Lindernia crustacean a,f ESE 1 322 Rehmarnia glufinosa b,g EM,N 1 323 Simaroubaceae Picrasma quassioides f,g ESE,M 1 324 Solanaceae Brunfelsia latibolia b,g,h O SE, M, N 2 325 Capsicum annuum a,c,e,h VS,SE 1 326 Capsicum annuum var. grossum c VS 1 327 Capsicum frutescens a,h VSE 2 328 Capsicum frutescens var. conoides b,c,f,g V S, SE, M, N 1

to be continued

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Table 1 Continued.

No. Family Plant species† Host type‡ Location§ Grade of infection rates¶

329 Capsicum frutescens var. longum c,g VS,M 2 330 Capsicum annujm var. cerasiforme b,g VM,N 1 331 Cestrum nocturnum b,g OM,N 1 332 Datura candida plena b,g OM,N 1 333 Datura stramonium b,c,g W S,M,N 1 334 Lycospersicum esculentum a,b,c,d,e,f,g,h V S, SE, M, N 4 335 Lycospersicum esculentum var. cerasiforme b,c,d,e,g,h V S, SE, M, N 4 336 Lycospersicum esculentum var. pyriforme c VS 4 337 Lycium chinense c,e,f,g ES,SE,M 1 338 Nicotiana tabacum c,f,h ES,SE 3 339 Petunia hybrida f,h WSE 3 340 Physalis angulata h WSE 1 341 Solanum melongena a,b,c,d,e,f,g,h V S, SE, M, N 4 342 Solanum muricatum h OSE 1 343 Solanum nigrum c,f,h WS,SE 3 344 Solanum pseudo-capsicum h OSE 1 345 Solanum tuberosum a,c,d,e,f,g OS,SE,M 1 346 Sterculiaceae Firmiana platanifolia b,f,g O SE, M, N 1 347 Theaceae Camellia japomica c,f OS,SE 1 348 Thymelaeaceae Daphne odora f,g OSE,M 1 349 Umbelliferae Apium graveolens var. dulce a,b,c,e,f,g,h V S, SE, M, N 1 350 Coriandrum sativum c,h VS,SE,M 1 351 Urticaceae Boehmeria nivea c,e ES,SE 1 352 Pilea mollis c,f WS,SE 1 353 Verbenaceae Clerodendrum fragrans c WS 1 354 Clerodendrum kaempferi c WS 1 355 Clerodendrum japonicum c,g WS,M 1 356 Duranta repens c OS 1 357 Lantana camara c WS 1 358 Vitaceae Cayratia japonicae WSE 2 359 Parthenocissus heterophylla c,f,g OS,SE,M 1 360 Parthenocissus tricuspidata c,f OS,SE 1 361 Vitis vinifera c,e,f,g,h F S, SE, M, NW 1

†The letters a–h mean this plant has been previously reported. a: He et al., 2003; b: Luo et al., 2000; c: Qiu et al., 2001; d: Sun et al., 2005; e: Xu et al., 2007a; f: Xu et al., 2007b; g: Zhang et al., 2005; h: Zhou et al., 2003. ‡E = economic crops, F = fruit, O = ornamental plants and flowers, V = vegetables, W = weeds. §S, SE, SW,M, N, NW represent the regions of south China, southeast China, southwest China, middle China, north China and northwest China, respectively. ¶The infection grades 1–4 represent the populations of B. tabaci <10, 11–30, 31–50 and >50 nymphs and pupae in 10 cm2 /leaf area, respectively.

In our present investigations, host plants in the Com- Our findings are much similar to those previous reports positae, Cruciferae, Cucurbitaceae, Solanaceae as well of Luo et al. (2000), Qiu et al. (2001), He et al. (2003), as Leguminosae were the most preferred species for B. Zhou et al. (2003) and Zhang et al. (2005) in China. How- tabaci, thus large populations were frequently recorded on ever, although the most visited plants by B. tabaci were these species, regardless of the geographical distributions. recorded on vegetables and crops, the vector plants that

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 112 S. J. Li et al.

Table 2 The top 10 families based on the number of host species and their infection rates by Bemisia tabaci.

No. of host plant species in infection grade† Rank Family No. of species 1234

1 Compositae 44 24 16 4 0 2 Leguminosae 26 14 9 2 1 3 Cruciferae 23 8 6 8 1 4 Solanaceae 22 12 3 3 4 5 Cucurbitaceae 19 2 8 6 3 6 Rosaceae 14 11 3 0 0 7 Euphorbiaceae 13 6 4 2 1 8 Amaranthacea 12 10 2 0 0 9 Malvaceae 12 4 6 1 1 10 Oleaceae 8 7 1 0 0

†Infection grade 1–4 represent the populations of B. tabaci <10, 11–30, 31–50 and >50 nymphs and pupae in 10 cm2 /leaf area, respectively. help B. tabaci to invade or spread objectively are the or- carsia,twoEretmocerus and one Amitus species. Ren namentals in Euphorbiaceae, Malvaceae and Compositae et al. (2001) reported 18 parasitoids, 17 predators and as proved by Dalton (2006). The first record of Q biotype one species of entomopathogenic fungi of B. tabaci in of B. tabaci in China was found on poinsettia in China. In the present survey, most of the parasitoids were province, Southwest China, the invasion of which was aphelinid wasps belonging to the genera Encarsia and hypothesized to be due to the international transportation Eretmocerus and most of the predators were lady beetles of poinsettia plants between China and Mediterranean followed by lacewings. As stated by Gerling et al. (2001), countries (Chu et al., 2006). Therefore, quarantine regu- the key difficulty during the survey is to identify preda- lations on imported plants, especially ornamental plants, tors of B. tabaci, especially in crops that harbor numerous is one of the key measures to keep invasive pests out of predator and prey species. Fortunately, the development non-invasive regions. of sequence-characterized amplified region (SCAR) tech- Natural enemy insects are most effective in controlling nology (Zhang et al., 2007) has helped overcome this B. tabaci populations in greenhouse environments than problem. All the predators collected in the current survey under field conditions (Nomikou et al., 2001). Predators subsequently had B. tabaci remains detected in their mid- and parasitoids of B. tabaci have been described and stud- guts by SCAR-PCR (polymerase chain reaction) method. ied for many years. Mound and Halsey (1978) reported Results from our surveys indicated that the populations 18 species of B. tabaci natural enemies, including nine of B. tabaci natural enemies were much higher in south species of parasitoids in and nine species China than in the other regions (data not shown in text) and of predators in the Acarina, Coleoptera, Diptera and Neu- it was considered that temperature may play an important roptera. In a study by Gerling et al. (2001) concerning role in determining the populations of natural enemies. the worldwide natural enemy resources of B. tabaci,79 In our surveys, Encarsia bimaculata and Eretmocerus sp. species of predators and 55 species of parasitoids were nr. furuhashii are the two dominate species parasitizing recorded. The predators included 24 species of lady bee- B. tabaci in South China, while the population of En- tles, 25 species of true bugs, 16 species of lacewings as carsia formosa is abundant in north China in protected well as 14 other species of predatory insects belonging to fields such as greenhouses. Similarly, the lady Ax- the Coleoptera, Diptera, Hymenoptera and Thysanoptera, inoscymnus cardilobus is a dominant predator of B. tabaci while the parasitoids included 35 Encarsia and 14 Eretmo- in south China, while its population is much lower or non- cerus species of wasps in the , three in the existent in the western regions of China (Huang et al., Platygasteridae, two and one species in the Signiphoridae 2003). The different geographical distributions of these and Encyrtidae, repectively. natural enemies may be due to their different suitability In China, 22 species of parasitoids were recorded in to the local temperatures as well as the seasonal dynamic Fujian Province (Huang et al., 2000), including 19 En- change of their host/prey populations.

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 Plants and natural enemies of Bemisia tabaci 113

Table 3 The parasitoids of Bemisia tabaci in China.

No. Name† Whitefly host species Distribution in China Distribution globally

Aphelinidae Ablerus 1 Ablerus macrochaetaf Aleurocanthus inceratus Guangxi, Yunnan Bemisia tabaci Encarsia 2 Encarsia bimaculataa B. tabaci, Guangdong, Fujian, Guangxi India, , USA, Trialeurodes vaporariorum, Oceania Aleurocanthus spiniferus 3 Encarsia abundantiae B. tabaci, Dialeurodes citri, Taiwan Dialeurodes kirkaldyi, Dialeurodes tetrastigmae 4 Encarsia albiscutellumd,e B. tabaci Fujian, Taiwan 5 Encarsia ancistrocerad,e B. tabaci, Aleurolobus marlatti, Taiwan Aleurotrachelus caerulescens, Dialeurodes fici 6 Encarsia asetad,e B. tabaci, Fujian Dialeurolonga elongata 7 Encarsia azimic B. tabaci, Fujian, Taiwan Aleurolobus rhododendri, D. fici, D. piperis, Odontaleyrodes rhododendri, Parabemisia myricae 8 Encarsia bemisiaea B. tabaci, B. myricae Zhejiang, Guangdong 9 Encarsia bennettid,e Aleurocanthus woglum, Taiwan A. cinnamomi, B. tabaci 10 Encarsia bothrocerad,e Aleurothrixus smilaceti, Taiwan Aleurotrachelus elatostema, B. myricae, B. tabaci 11 Encarsia cibcensisa,,c Aleurotuberculatus ficicola, Taiwan B. myricae, B. tabaci, Dialeurodes agalmae, Singhius hibisci, Taiwanaleyrodes meliosmae 12 Encarsia collectad,e B. tabaci, P. m y r i c a e Fujian 13 Encarsia duorungaa,,c B. tabaci Taiwan 14 Encarsia echinocerad,e A. ficicola, B. tabaci Taiwan 15 Encarsia elegansd,e Aleurocanthus husaini, Fujian, Taiwan Egypt A. marlatti, Aleurolobus niloticus, B. tabaci 16 Encarsia formosaa,b,c Aleurotrachelus trachoides, Beijing, Shandong, Xinjiang, United Kingdom, Aleyrodes lonicerae, B. tabaci, Guangdong, Germany, Canada, Dialeurodes chittendeni, USA, New Zealand, D. citri, T. vaporariorum Russia 17 Encarsia fujianensisd,e Aleurolobus szechwanensia, Fujian B. tabaci 18 Encarsia gerlingid,e B. tabaci Fujian

to be continued

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Table 3 Continued.

No. Name† Whitefly host species Distribution in China Distribution globally

19 Encarsia hamataa,b B. tabaci Fujian 20 Encarsia inarona,c Acaudaleyrodes citri, Taiwan United Kingdom Aleyrodes lonicerae, Aleyrodes proletella, Aleyrodes singularis, B. tabaci, Bulgarialeurodes cotesii, Perliua quercua, Siphoninus immaculatus 21 Encarsia ishiid,e A. spiniferus, A. woglumi, Fujian, Hunan, Jiangsu, Aleuroplatus pectinferrus, Zhejiang, Guangxi, Hong B. tabaci Kong, Taiwan 22 Encarsia japonicaa,b,c Aleurocybotus indicus, Fujian, Taiwan B. tabaci, T. vaporariorum 23 Encarsia lahorensisd,e B. tabaci, D. citri, D. kirkaldyi, Guangdong, Taiwan Tuberaleyrodes machili 24 Encarsia longicaudad,e Aleurotuberculatus murrayae Taiwan 25 Encarsia longifasciataa,c A. spiniferus, Fujian, Guangxi, Taiwan Aleurolobus setigerus, B. tabaci 26 Encarsia longivalvulac B. tabaci, D. citir Taiwan 27 Encarsia lounsburyib A. spiniferus Fujian 28 Encarsia luteaa,c Aleurotuberlatus psidii, Fujian, Guangdong, Guangxi, Egypt, Iraq, Israel, India, Aleurotuberculatus aucubae, Taiwan Pakistan, Sudan, Russia Aleztrocanthus cinnamomi, B. tabaci, D. citri 29 Encarsia magnivenad,e B. tabaci, D. citri Taiwan 30 Encarsia mercetif Aleurocanthus citriperdus Fujian, Guangdong B. tabaci 31 Encarsia mohyuddinic Aleurotuberculatus takahashi Fujian B. tabaci 32 Encarsia nipponicad,e A. spiniferus, Fujian, Taiwan Japan Aleurotuberculatus , B. tabaci 33 Encarsia obtusiclavab A. spiniferus, B. tabaci Fujian, Taiwan 34 Encarsia opulentad,e A. spiniferus, A.inceratus, Fujian, Anhui B. tabaci 35 Encarsia perflavad,e Aleurotrachelus elatostemae, Fujian, Taiwan A. ficicola, B. tabaci, Taiwanaleyrodes carpini 36 Encarsia perplexad,e A. woglumi, Fujian, Taiwan Aleurotuberculatus kuwani, Aleuroplatus pectiniferus, B. tabaci 37 Encarsia protransvenaa B. tabaci, D. citri, Guangdong, Taiwan D. citrifolii, D. krikaldyi

to be continued

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Table 3 Continued.

No. Name† Whitefly host species Distribution in China Distribution globally

38 Encarsia smithib A. spiniferus B. tabaci Fujian, Anhui, Zhejiang, Shandong, , Guangdong, Guangxi, Hunan, Taiwan 39 Encarsia sophiaa,b Aleurodicus disperses, Fujian, Guangdong, Taiwan USA, A. indicus, B. tabaci, D. citri, P. m y r i c a e , Pealius longispinus, T. vaporariorum 40 Encarsia strenuac Bemisia giffardi, B. tabaci, Fujian, Guangdong, Hong Singapore D. citri, D. kirkaldyi, P. m y r i c a e Kong, 41 Encarsia synaptocerac Aleurotuberculatus malloti, Taiwan B. tabaci, Pealius polygoni 42 Encarsia tristisa B. tabaci, Taiwan Nomaskellia andropogonis, Neomaskellia bergi Eretmocerus 43 Eretmocerus cornid Aleyrodes corni, Fujian, Shandong Italy, Egypt, Hawaii B. tabaci, T. vaporariorum, Trialeurodes packardi 44 Eretmocerus emiratusa B. tabaci Zhejiang UAE, USA 45 Eretmocerus furuhashiia B. tabaci, T. vaporariorum Guangdong, Japan, USA Hebei, Taiwan, Zhejiang 46 Eretmocerus gunturiensisd Aleyrodes sp., B. tabaci Fujian, Anhui 47 Eretmocerus hayatia B. tabaci Zhejiang Australia, India, Japan, Pakistan, USA 48 Eretmocerus longiscapusb Aleurolobus sp. nr. niloticus, Fujian B. tabaci 49 Eretmocerus B. tabaci Zhejiang, Taiwan melanoscutusf 50 Eretmocerus orientalisa,c A. spiniferus, A. inceratus, Fujian, Guangdong B. tabaci 51 Eretmocerus Acaudaleyrodes rhachipora, Fujian rajasthanicusc B. tabaci 52 Eretmocerus sculpturatusf B. tabaci Zhejiang 53 Eretmocerus seriusf A. spiniferus, B. tabaci Anhui, Hunan, Guangdong, 54 Eretmocerus silverstriid A. spiniferus Fujian Platygasteridae Amitus 55 Amitus longicornisd A. spiniferus, B. tabaci Fujian, Jiangxi, Anhui, Hunan 56 Amitus hesperidumd A. spiniferus, A. takahashi, Anhui, Jiangxi, Hunan, Japan B. tabaci Zhejiang, Guangdong, Shandong

†The letters a–f mean the parasitoid has been previously reported in the related references. a: Gerling et al., 2001; b: Huang et al., 2000; c: Ren et al., 2001; d: Huang, 2002; e: Huang and Polaszek, 1998; f: present census.

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 116 S. J. Li et al.

Table 4 The predatory arthropods of Bemisia tabaci in China.

No. Name† Whitefly host species Distribution in China Distribution globally

Araneae Agelenidae 1 Agelena labyrinthicac A. spiniferus, B. tabaci Beijing, Hebei, Shandong, Zhejiang, Hunan, Guangdong Araneidae 2 Neoscona arabescaa B. tabaci Taiwan 3 Neoscona doenitzic A. spiniferus, B. tabaci, Fujian T. vaporariorum 4 Neoscona theisic A. spiniferus, B. tabaci Zhejiang 5 Singa hamatac A. spiniferus, B. tabaci Heilongjiang, Liaoning, Hebei, Zhejiang, Shandong, Xinjiang Linyphiidae 6 Erigonidium graminicolumc A. spiniferus, B. tabaci Fujian Lycosidae 7 Lycosa pseudoannulatac A. spiniferus, B. tabaci Guangdong Philodromidae 8 Philodromus anreolusc A. spiniferus, B. tabaci, Liaoning, Ningxia, Jilin, Japan T. vaporariorum Xinjiang Salticidae 9 Euophrys undulatovittatac A. spiniferus, Guizhou B. tabaci, D. citri 10 Marpissa magisterc A. spiniferus, B. tabaci, Hubei, Shandong, Henan, T. vaporariorum Zhejiang, Guangdong 11 Plexippus paykullic A. spiniferus, B. tabaci, Hebei D. citri 12 Plexippus setipesc B. tabaci, D. citri Fujian Tetragnathidae 13 Tetragnatha japoniac A. spiniferus, B. tabaci Fujian Theridiidae 14 Theridula gonygastera B. tabaci Sichuan, Guangxi Thomisidae 15 Misumenops tricuspidataa A. spiniferus, B. tabaci Zhejiang, Jiangsu 16 Xysticus ephippiatusc A. spiniferus, B. tabaci, Jilin, Xinjiang, , Shandong T. vaporariorum Coleoptera 17 Adalia bipunctatac A. spiniferus, B. tabaci Jilin, Liaoning, Xinjinag, Shanxi 18 Anisolemnia dilatalac A. spiniferus, B. tabaci Fujian, Guangdong 19 Axinosymnus cardilobusb B. tabaci Guangdong 20 Chilocorus gressittic A. spiniferus, B. tabaci Guangdong, Hainan 21 Chilocorus kuwanaec A. spiniferus, B. tabaci Hainan 22 Chilocorus rubidusc A. spiniferus, B. tabaci Anhui 23 Coccinella septempunctataa B. tabaci Fujian, Guangdong, Mongolia, Japan, Korea, Shandong, Zhejiang India, Russia 24 Coccinella undecimpunctataa B. tabaci Gansu, Ningxia, Xinjiang, Europe, North Africa , Hebei, Shandong, Shanxi

to be continued

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 Plants and natural enemies of Bemisia tabaci 117

Table 4 Continued.

No. Name† Whitefly host species Distribution in China Distribution globally

25 Cryptolaemus montrouzieria,b B. tabaci Guangdong, Taiwan, Japan, India, Southeast Asia, Spain, Egypt, Australia, New Zealand, Kenya 26 Harmonia dimidiatea,b B. tabaci Fujian 27 Hippodamia tredecimpunctataa B. tabaci, Bejing, Gansu, Xinjiang, T. vaporariorum Ningxia, 28 Hyperaspis repensisc A. spiniferus, B. tabaci Guangdong, Guangxi, Zhejiang, Hebei 29 Hyperspis sinensisc A. spiniferus, B. tabaci Zhejiang 30 Leis axyridisc A. spiniferus, B. tabaci Beijing, Zhejiang, Guangdong, T. vaporariorum Shandong 31 Lemnia biplagiatab B. tabaci, Jiangxi, Zhejiang, Fujian, Korea, Japan, India, D. citri Guangdong, Hong Kong, Indonesia, , Guangxi, Sichuan, Yunnan, Malaysia, the Tibet 32 Macronaemia hauseric A. spiniferus, B. tabaci Hubei, Jiangxi 33 Menochilus sexmaculatab B. tabaci, Shandong, Liaoning, Gansu, Japan, India, , T. vaporariorum Shaanxi, Jilin, Henan, Jiangsu, Sri Lanka, the Zhejiang, Jiangxi, Hunan, Philippines, Indonesia, Fujian, Guangdong, Hong Malaysia, Thailand, Kong, Guangxi, Hainan, Afghanistan, Iran Sichuan, Guizhou, Yunnan 34 Micraspis inopsa B. tabaci Guangdong, Japan, Vietnam, India, Guangxi , Thailand, Indonesia 35 Phrynocaria congenerb B. tabaci Fujian, Taiwan, Guangdong, Japan, Vietnam, India Guangxi, Hong Kong, Sichuan, Yunnan 36 Propylaea japonicac A. spiniferus, B. tabaci Beijing, Shandong, Guangdong, Fujian 37 Rodolia cardinalisc A. spiniferus, B. tabaci, Guangdong T. vaporariorum 38 Serangium japonicumb B. tabaci, Shanxi, Zhejiang, Shanghai, South Korea, Japan T. vaporariorum Fujian, Guangdong, Guangxi, Taiwan, Sichuan, Guizhou, Yunnan 39 Telsimia emarginatac A. spiniferus, B. tabaci, Guangdong, Guangxi T. vaporariorum Nitidulidae 40 Cybocephalus niponicusa B. tabaci, D. citir, Guangdong, Guangxi Japan T. vaporariorum Staphylinidae 41 Paederus fuscipesa B. tabaci, D. citir, Guangdong, Guangxi, Fujian T. vaporariorum

to be continued

C 2011 The Authors Journal compilation C Institute of Zoology, Chinese Academy of Sciences, Insect Science, 18, 101–120 118 S. J. Li et al.

Table 4 Continued.

No. Name† Whitefly host species Distribution in China Distribution globally

Hemiptera Anthocoridae 42 Orius albidipennisa B. tabaci, D. citir, Shandong Israel T. vaporariorum 43 Orius insidiosusa B. tabaci, T. vaporariorum Anhui USA 44 Orius sauteric B. tabaci, T. vaporariorum Liaoning, Beijing, Tianjin, Hebei, Shanxi, Hubei, Sichuan 45 Orius similesb B. tabaci Guangdong 46 Orius strigicollisa,b B. tabaci Guangdong, Guangxi, Fujian, Thailand, Hong Kong, Taiwan the Philippines 47 Orius tantillusa,b B. tabaci Guangdong, Guangxi, Fujian, Thailand, the Philippines, Hong Kong, Taiwan Australia Neuroptera Chrysopidae 48 Chrysocerca formosaa,b B. tabaci Guangdong Taiwan, 49 Chrysopa boninsisa,b B. tabaci Jiangxi 50 Chrysopa formosaa A. spiniferus, B. tabaci, Beijing, Shanxi, Shandong, Jilin, T. vaporariorum Xinjiang 51 Chrysopa sinicac B. tabaci, T. vaporariorum Beijing, Shandong, Jiangsu, Zhejiang 52 Chrysoperla carneaa A. spiniferus, B. tabaci Beijing, Xinjiang, Shaanxi Japan, India 53 Mallada boninensisa B. tabaci Taiwan Coniopterygidae 54 Semidalis aleyrodiformisc B. tabaci Beijing, Chongqing, Guangdong

†The letters a–c mean the predator has been previously reported in the related references. a: Gerling et al., 2001; b: Ren et al., 2001; c: present census.

The continuous increase in chemical resistance by (Fujian Agriculture and Forestry University, China) and B. tabaci has largely reduced the effectiveness of most Zong-Qi Liang (Guizhou University, China) for iden- available pesticides in China. As a result, integrated pest tifying the species of host plants, parasitoids and en- management programs are increasingly becoming more tomopathogenic fungi, respectively. This research was effective in B. tabaci control. Hereby, an exhaustive sur- funded by the National Basic Research Program of China vey of host plants and natural enemies is the foundation (973 Project, 2009CB119203), the China National Nat- for B. tabaci integrated pest management. Our surveys ural Science Foundation (30871678, 31071732) and Na- reported the host plants and natural enemies of B. tabaci tional Department Public Benefit Research Foundation in China in a more comprehensive pattern. Undoubtedly, (nyhyzx200803005). it will help us to have a better understanding of the pop- ulation development of B. tabaci in these areas and drive forward the integrated pest management of this pest. References

Acknowledgments Attique, M.R., Rafiq, M., Ghaffar, A., Ahmad, Z. and Mohyud- din, A.I. (2003) Hosts of Bemisia tabaci (Genn.) (Homoptera: The authors thank the anonymous reviewers for Aleyrodidae) in cotton areas of Punjab, Pakistan. Crop Pro- their constructive comments on the previous version tection, 22, 715–720. of this manuscript. Thanks also to Tong-Xing Sun Avidov, Z. and Harpaz, I. (1969) Plant Pests of Israel. University (Qingdao Agricultural University, China), Jian Huang Press, Jerusalem. pp. 76–84.

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