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 surveys 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 pulcherrima Wild. ex Klotsch (Euphorbiaceae)], cotton [Gossypium hirsutum L. (Malvaceae)], and cabbage [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 survivorship), these hosts differed between B and Q. When given a choice, B preferred to settle and oviposit 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 survival for B were greater on cabbage than on poinsettia and cotton, but the opposite was true for Q.
Introduction The whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is a serious agricultural pest of many crops worldwide (Oliveira et al., 2001). Damage to host plants is caused by phloem-feeding of the nymphs and adults (Byrne & Bellows, 1991; Oliveira et al., 2001; Perring, 2001), excretion of honeydew, induction of phytotoxic disorders (Costa & Brown, 1991), and transmission of plant viruses (Brown, 2000; Pan et al., 2012). Bemisia tabaci has more than 600 host plants, which include crops and ornamentals grown in both the field and greenhouses
*Correspondence: Youjun Zhang, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China. E-mail:
[email protected] †
These authors have equally contributed to this work.
(Brown et al., 1995) as well as weeds (Calvitti & Remotti, 1998; Mu~ niz, 2000; Gachoka et al., 2005). The presence of morphologically indistinguishable biotypes (Costa & Brown, 1991) and/or host races (Brown et al., 1995) of B. tabaci that differ in host range, host plant adaptability, and capacity to transmit viruses has been well documented (Perring, 2001), and a recent phylogenetic analysis suggested that B. tabaci is a complex of 11 well-defined, high-level groups containing at least 24 morphologically indistinguishable putative/cryptic species (Dinsdale et al., 2010; Xu et al., 2010; De Barro et al., 2011). The two most widespread putative species are referred to as B (Middle East–Asia Minor 1) and Q (Mediterranean), both of which are invasive pests throughout the world (Delatte et al., 2009; Dinsdale et al., 2010; Xu et al., 2010; De Barro et al., 2011). In many invaded regions, introduction of B whiteflies has led to the displacement 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, 1996; Liu et al., 2007; De Barro et al., 2011). It is generally suspected that the higher capacity of B to use various host plants relative to indigenous B. tabaci plays an important role in mediating the displacement (Zang et al., 2006; De Barro et al., 2011; Xu et al., 2011). Although B and Q putative species of B. tabaci are polyphagous, previous studies have shown that they vary substantially in numerous fitness parameters when feeding on various host species. For example, Q outperforms B on kidney bean, pepper, and certain weeds (Mu~ niz, 2000; Mu~ niz & Nombela, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; Saleh et al., 2012). In Japan and China, the putative species Q of B. tabaci is predominant and has been displacing the putative species B (Chu et al., 2010; Pan et al., 2011; Tsueda & Tsuchida, 2011). Although the exact mechanism behind the displacement is not known, at least three possible causes for the displacement have been studied. First, a high resistance of Q to insecticides such as pyriproxyfen and some neonicotinoids may contribute to the displacement of B by Q (Horowitz et al., 2003, 2005; Dennehy et al., 2010). Second, the displacement of B by Q could result from the greater reproductive capacity of Q on various host plants. Although invasive putative species B of B. tabaci outperforms native putative species in terms of reproduction on several host plants (Zang et al., 2006; Liu et al., 2007; De Barro et al., 2011; Xu et al., 2011), the reproductive capacities of invasive B and Q under the same conditions have been compared in only a few studies (Mu~ niz, 2000; Mu~ niz & Nombela, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011). Third, Q is generally thought to have a wider host range than B, and a wider host range could result in a greater invasive capacity (Mu~ niz, 2000; Mu~ niz & Nombela, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; Saleh et al., 2012). However, statements concerning host range differences between B and Q are mostly based on assumptions, and there are few relevant field surveys and experimental studies. Many researchers have inferred that the capacity of Q to use a wider range of host plants than B underlies the displacement of B by Q (Mu~ niz, 2000; Mu~ niz & Nombela, 2001; Iida et al., 2009; Tsueda & Tsuchida, 2011; 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 needed. In addition, most experiments that compare Q and B reproduction on host plants do not offer the insects a choice of hosts, which is not realistic. For most herbivore insects, larval mobility is limited, which means that they rely on host plant choice by the maternal adults. Oviposition preference generally correlates
with host suitability for offspring performance, and females are expected to oviposit on high quality host species to maximize their fitness (Jaenike, 1978; Gripenberg et al., 2010). However, female oviposition preference and offspring performance are not always correlated (Thompson, 1988; Gripenberg et al., 2010). The apparent mismatch between female oviposition preference and offspring performance may be shaped by several evolutionary and ecological factors (Thompson, 1988; Gripenberg et al., 2010). Consequently, the investigation of host suitability for herbivorous insects in no-choice situations may not be a good predictor of host plant damage and/or herbivore population increase under natural conditions. In free-choice situations, females of some herbivorous insects avoid feeding and laying eggs on those host species that are highly suitable for their larval growth and development (Gripenberg et al., 2010). For example, although the vine weevil Otiorhynchus sulcatus (Fabricius) consumed more foliage of some cultivars of red raspberry than of other hosts in no-choice situations, they tended to avoid feeding and laying eggs on these cultivars in free-choice situations (Clark et al., 2012). Omondi et al. (2005) indicated that the suitability of cassava and okra putative species of B. tabaci did not correlate with female landing and oviposition preferences. Eggplant, for instance, supported 83% survival of okra whiteflies nymphs in no-choice bioassay, but attracted only 7% of females for settling and ovipositing in a free-choice experiment (Omondi et al., 2005). In this study, we determined whether female oviposition preference was positively correlated with nymph performance for putative species B and Q of B. tabaci on three common host plants: poinsettia Euphorbia pulcherrima Wild. ex Klotsch (Euphorbiaceae), cotton Gossypium hirsutum L. (var. DP99B) (Malvaceae), and cabbage Brassica oleracea (var. Jingfeng1) (Brassicaceae). We also determined whether B and Q differed in their settling and oviposition preference when given a choice between these three host plants. This information should contribute to our understanding of the invasiveness of the putative species B and Q and on the displacement of B by Q.
Materials and methods Insects and host plants
The putative species B of B. tabaci was originally collected from cabbage (B. oleracea var. Jingfeng1) in Beijing and then maintained on cucumber (Cucumis sativa var. Zhongnong12), which is a highly suitable host 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 obtained from poinsettia (E. pulcherrima) in Beijing and subsequently maintained on cucumber (C. sativa var. Zhongnong12) in a separate glasshouse. Stock cultures of B and Q were maintained on cucumber in separate insect-proof screened cages (60 9 60 9 60 cm) in the laboratory at 25 1 °C, 60 10% r.h., and L14:D10. The purity of the cultures was monitored every 2–3 generations based on determination of DNA sequence of the haplotypes following amplification by mtCOI primers (Zhang et al., 2005). The host plants used for the experiments, which were poinsettia, cotton, and cabbage, were established individually in 12-cm diameter plastic pots. When they were 30 cm tall, plants of similar size were selected for each experiment. Female settling and oviposition preference
An experiment concerning whitefly settling and oviposition preference was conducted as described by Omondi et al. (2005). Briefly, individual plants of poinsettia, cotton, and cabbage of approximately the same size were placed in a screen cage (60 9 60 9 60 cm); within the cage, the three plants were arranged in the form of an even-sided triangle with 20-cm sides. About 300 female whiteflies were collected from each putative species of B. tabaci between 07:00 and 08:00 hours and released from an aspirator into the center of the screen cage above the plant canopy. The aspirator sampling bottle containing whiteflies was held inside a clear plastic tumbler hung at the center of the cage, about 30 cm above the plant canopy. Whiteflies moved to the open top and flew away from the sampling bottle to approach the plants from above. The number of whiteflies on each plant was determined after 12, 24, 36, 48, 60, 72, 84, 96, and 108 h. To prevent whiteflies from moving between leaves and host species during counting, the whiteflies were counted out under dim light just before 07:00 hours and just after 19:00 hours. At the end the settling bioassay, all leaves from each host species were removed and examined with a dissecting microscope; the number of eggs laid (an indicator of oviposition preference) was determined. The experiment was replicated six times. Adult longevity and fecundity
Newly emerged (
