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 12 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, PHost 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: P6 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.
In this study, Q whiteflies were reluctant to settle and
oviposit on the nutritionally superior cabbage, and Q
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