Differences in host selection and performance between B and Q putative species of Bemisia tabaci on three host plants
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DOI: 10.1111/eea.12040 Differences in host selection and performance between B and Q putative species of Bemisia tabaci on three host plants Xiaoguo Jiao1,2†, Wen Xie1†, Shaoli Wang1, Qingjun Wu1, Huipeng Pan1, Baiming Liu1 & Youjun Zhang1* 1 Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China, and 2College of Life Sciences, Hubei University, Wuhan 430062, China Accepted: 6 December 2012 Key words: oviposition preference, host suitability, competitive displacement, Hemiptera, Aleyrodidae, Brassica oleracea, Euphorbia pulcherrima, Gossypium hirsutum Abstract B and Q are two putative species of the Bemisia tabaci complex (Hemiptera: Aleyrodidae), and are among the most invasive and destructive pests of crops and horticultural plants worldwide. In China, Q predominates and is displacing B. Although researchers have proposed that the higher capacity of Q to utilize host plants plays an important role in its replacement of B, there are few relevant field sur- veys and experimental studies. The difference in host assessment between B and Q in multiple-choice rather than in no-choice situations may be essential to understanding the displacement. Here, we compared settling and oviposition preferences, and adult and nymph performance, for the putative species B and Q of the B. tabaci complex on three common host species: poinsettia [Euphorbia pul- cherrima Wild. ex Klotsch (Euphorbiaceae)], cotton [Gossypium hirsutum L. (Malvaceae)], and cab- bage [Brassica oleracea L. (Brassicaceae)]. Although the preferred hosts for settling and oviposition were the same as those that supported maximum fitness (adult longevity, fecundity, and nymph sur- vivorship), these hosts differed between B and Q. When given a choice, B preferred to settle and ovi- posit on cabbage over poinsettia and cotton, whereas Q preferred to settle and oviposit on poinsettia and cotton over cabbage. In a no-choice experiment, adult longevity, fecundity, and nymphal sur- vival for B were greater on cabbage than on poinsettia and cotton, but the opposite was true for Q. (Brown et al., 1995) as well as weeds (Calvitti & Remotti, Introduction 1998; Mu~ niz, 2000; Gachoka et al., 2005). The whitefly, Bemisia tabaci (Gennadius) (Hemiptera: The presence of morphologically indistinguishable bio- Aleyrodidae), is a serious agricultural pest of many crops types (Costa & Brown, 1991) and/or host races (Brown worldwide (Oliveira et al., 2001). Damage to host plants is et al., 1995) of B. tabaci that differ in host range, host caused by phloem-feeding of the nymphs and adults plant adaptability, and capacity to transmit viruses has (Byrne & Bellows, 1991; Oliveira et al., 2001; Perring, been well documented (Perring, 2001), and a recent phylo- 2001), excretion of honeydew, induction of phytotoxic genetic analysis suggested that B. tabaci is a complex of 11 disorders (Costa & Brown, 1991), and transmission of well-defined, high-level groups containing at least 24 plant viruses (Brown, 2000; Pan et al., 2012). Bemisia morphologically indistinguishable putative/cryptic species tabaci has more than 600 host plants, which include crops (Dinsdale et al., 2010; Xu et al., 2010; De Barro et al., and ornamentals grown in both the field and greenhouses 2011). The two most widespread putative species are referred to as B (Middle East–Asia Minor 1) and Q (Medi- terranean), both of which are invasive pests throughout *Correspondence: Youjun Zhang, Institute of Vegetables and Flow- the world (Delatte et al., 2009; Dinsdale et al., 2010; Xu ers, Chinese Academy of Agricultural Sciences, Beijing 100081, China. et al., 2010; De Barro et al., 2011). In many invaded E-mail: zhangyoujun@caas.cn regions, introduction of B whiteflies has led to the dis- † These authors have equally contributed to this work. placement of some relatively innocuous, indigenous © 2013 The Authors Entomologia Experimentalis et Applicata 147: 1-8, 2013 Entomologia Experimentalis et Applicata © 2013 The Netherlands Entomological Society 1
2 Jiao et al. B. tabaci belonging to different putative species (Perring, with host suitability for offspring performance, and 1996; Liu et al., 2007; De Barro et al., 2011). It is generally females are expected to oviposit on high quality host suspected that the higher capacity of B to use various host species to maximize their fitness (Jaenike, 1978; Gripen- plants relative to indigenous B. tabaci plays an important berg et al., 2010). However, female oviposition prefer- role in mediating the displacement (Zang et al., 2006; De ence and offspring performance are not always Barro et al., 2011; Xu et al., 2011). Although B and Q correlated (Thompson, 1988; Gripenberg et al., 2010). putative species of B. tabaci are polyphagous, previous The apparent mismatch between female oviposition studies have shown that they vary substantially in numer- preference and offspring performance may be shaped by ous fitness parameters when feeding on various host spe- several evolutionary and ecological factors (Thompson, cies. For example, Q outperforms B on kidney bean, 1988; Gripenberg et al., 2010). Consequently, the inves- pepper, and certain weeds (Mu~ niz, 2000; Mu~ niz & Nom- tigation of host suitability for herbivorous insects in bela, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; no-choice situations may not be a good predictor of Saleh et al., 2012). host plant damage and/or herbivore population increase In Japan and China, the putative species Q of B. tabaci is under natural conditions. In free-choice situations, predominant and has been displacing the putative species females of some herbivorous insects avoid feeding and B (Chu et al., 2010; Pan et al., 2011; Tsueda & Tsuchida, laying eggs on those host species that are highly suitable 2011). Although the exact mechanism behind the for their larval growth and development (Gripenberg displacement is not known, at least three possible causes et al., 2010). For example, although the vine weevil for the displacement have been studied. First, a high resis- Otiorhynchus sulcatus (Fabricius) consumed more foliage tance of Q to insecticides such as pyriproxyfen and some of some cultivars of red raspberry than of other hosts in neonicotinoids may contribute to the displacement of B no-choice situations, they tended to avoid feeding and by Q (Horowitz et al., 2003, 2005; Dennehy et al., 2010). laying eggs on these cultivars in free-choice situations Second, the displacement of B by Q could result from the (Clark et al., 2012). Omondi et al. (2005) indicated that greater reproductive capacity of Q on various host plants. the suitability of cassava and okra putative species of Although invasive putative species B of B. tabaci outper- B. tabaci did not correlate with female landing and ovi- forms native putative species in terms of reproduction on position preferences. Eggplant, for instance, supported several host plants (Zang et al., 2006; Liu et al., 2007; De 83% survival of okra whiteflies nymphs in no-choice Barro et al., 2011; Xu et al., 2011), the reproductive capac- bioassay, but attracted only 7% of females for settling ities of invasive B and Q under the same conditions have and ovipositing in a free-choice experiment (Omondi been compared in only a few studies (Mu~ niz, 2000; Mu~niz et al., 2005). & Nombela, 2001; Iida et al., 2009; Tsueda & Tsuchida, In this study, we determined whether female oviposi- 2011). Third, Q is generally thought to have a wider host tion preference was positively correlated with nymph range than B, and a wider host range could result in a performance for putative species B and Q of B. tabaci greater invasive capacity (Mu~ niz, 2000; Mu~niz & Nombe- on three common host plants: poinsettia Euphorbia pul- la, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; Saleh cherrima Wild. ex Klotsch (Euphorbiaceae), cotton Gos- et al., 2012). However, statements concerning host range sypium hirsutum L. (var. DP99B) (Malvaceae), and differences between B and Q are mostly based on assump- cabbage Brassica oleracea (var. Jingfeng1) (Brassicaceae). tions, and there are few relevant field surveys and experi- We also determined whether B and Q differed in their mental studies. settling and oviposition preference when given a choice Many researchers have inferred that the capacity of Q between these three host plants. This information to use a wider range of host plants than B underlies the should contribute to our understanding of the invasive- displacement of B by Q (Mu~ niz, 2000; Mu~niz & Nombela, ness of the putative species B and Q and on the 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; displacement of B by Q. Saleh et al., 2012), but comparative experiments with B and Q on different host plants are limited, and more experiments with a wider range of host plants are Materials and methods needed. In addition, most experiments that compare Q Insects and host plants and B reproduction on host plants do not offer the The putative species B of B. tabaci was originally insects a choice of hosts, which is not realistic. For most collected from cabbage (B. oleracea var. Jingfeng1) in herbivore insects, larval mobility is limited, which Beijing and then maintained on cucumber (Cucumis means that they rely on host plant choice by the mater- sativa var. Zhongnong12), which is a highly suitable host nal adults. Oviposition preference generally correlates for both B and Q in the glasshouse (Bird & Kr€ uger,
Host choice and performance between B and Q whiteflies 3 2006). The putative species Q of B. tabaci was originally combination of putative species and host was replicated 21 obtained from poinsettia (E. pulcherrima) in Beijing and –25 times. The survival of the females and males in the clip subsequently maintained on cucumber (C. sativa var. cages was assessed daily. The clip cages with whiteflies were Zhongnong12) in a separate glasshouse. Stock cultures gently moved to new leaves on the same plant every of B and Q were maintained on cucumber in separate 2 days, and the eggs laid by each female were counted until insect-proof screened cages (60 9 60 9 60 cm) in the female death. When the paired whiteflies in the clip cages, laboratory at 25 1 °C, 60 10% r.h., and L14:D10. regardless of female or male, died within 2 days, the data The purity of the cultures was monitored every 2–3 were excluded from further analysis. generations based on determination of DNA sequence of the haplotypes following amplification by mtCOI prim- Nymphal survivorship ers (Zhang et al., 2005). The host plants used for the Nymphal survivorship of putative species B and Q of experiments, which were poinsettia, cotton, and cabbage, B. tabaci on different plant species was measured in the were established individually in 12-cm diameter plastic laboratory. Five insect-free host plants of each host species pots. When they were 30 cm tall, plants of similar size were placed in the insect-proof screened cages containing were selected for each experiment. one of the putative species. After 8 h, the plants were removed from the cage. Three extended leaves per plant Female settling and oviposition preference were selected and marked. The eggs distributed on the An experiment concerning whitefly settling and oviposi- unselected leaves were removed with the aid of a binocular tion preference was conducted as described by Omondi microscope. The abaxial surface of each selected leaf was et al. (2005). Briefly, individual plants of poinsettia, drawn, and the position of every egg was indicated. These cotton, and cabbage of approximately the same size were drawings allowed us to follow each whitefly from egg until placed in a screen cage (60 9 60 9 60 cm); within the adult emergence. There were 30–50 eggs per selected leaf. cage, the three plants were arranged in the form of an As noted, the remaining eggs were removed. The plants even-sided triangle with 20-cm sides. About 300 female with marked leaves were placed in climatic chambers at whiteflies were collected from each putative species of 27 °C, 60 10% r.h., and L14:D10; six chambers were B. tabaci between 07:00 and 08:00 hours and released used so that there was one chamber for each combination from an aspirator into the center of the screen cage above of host and putative whitefly species. When fourth-stage the plant canopy. The aspirator sampling bottle containing nymphs were observed on a given host plant, the host whiteflies was held inside a clear plastic tumbler hung at plant was placed in an insect-proof net, and all of the the center of the cage, about 30 cm above the plant can- emerged adults were collected and frozen two times each opy. Whiteflies moved to the open top and flew away from day. Nymph stages (eggs and nymphs by stage) and adults the sampling bottle to approach the plants from above. were recorded and counted daily for each host species. The number of whiteflies on each plant was determined Nymphal survivorship was expressed as the proportion of after 12, 24, 36, 48, 60, 72, 84, 96, and 108 h. To prevent the eggs that produced adult whiteflies. Each selected leaf whiteflies from moving between leaves and host species was considered a replicate in each treatment, and there during counting, the whiteflies were counted out under were 15 replicates per treatment. dim light just before 07:00 hours and just after 19:00 hours. At the end the settling bioassay, all leaves Data analysis from each host species were removed and examined with a Data were first checked for normality and transformed dissecting microscope; the number of eggs laid (an indica- when necessary to meet the assumption of normal distri- tor of oviposition preference) was determined. The experi- bution. The percentage of eggs distributed on various host ment was replicated six times. species was arcsine-square root transformed before analy- ses. The effects of whitefly species and host species on Adult longevity and fecundity female settling preference were tested by repeated- Newly emerged (
4 Jiao et al. Results 80 B a 70 Q Female settling and oviposition preference b Female settling preference was significantly affected by % eggs on host species 60 host species (F2,30 = 5.451, P = 0.01) and by the whitefly 50 species*host species interaction (F2,30 = 76.844, P
Host choice and performance between B and Q whiteflies 5 A 40 a B 30 B a a a Female adult longevity (days) Q a Male adult longevity (days) b 25 30 b b b b b 20 b 20 15 10 10 5 0 0 Figure 3 Fitness of putative species B and Q C 300 D 100 a a of the Bemisia tabaci complex as affected by a No. eggs laid per female 250 80 a % nymphs surviving host (poinsettia, cotton, and cabbage): (A) 200 b b b female longevity, (B) male longevity, (C) b 60 150 c bc b bc number of eggs laid per female during her 40 lifetime, and (D) nymphs surviving. Values 100 are means + SD. Within a panel, different 50 20 letters indicate significant difference 0 0 (Tukey’s test: P
6 Jiao et al. its high nitrogen and low carbon content relative to cotton and poinsettia (Xie et al., 2012). Considering that plants Acknowledgements with low nitrogen and high carbon content are commonly This study was funded by National Science Fund for recognized to negatively affect phytophagous insects Distinguished Young Scholars (31025020), National Basic (Hartley & Jones, 1997), our present study suggests that Q Research Program of China (2012CB017359), National may be more tolerant to low host nutrition than B. Assum- Natural Science Foundation of China (31171857), and ing that plants with low nitrogen and high carbon contents Key Laboratory of Biology and Genetic Improvement of are more common than plants with high nitrogen and low Horticultural Crops, Ministry of Agriculture, China. carbon contents, this could help explain displacement of B Special thanks to the anonymous reviewers for their by Q. comments and constructive criticisms. 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