Interspecific Interactions Between Two Whitefly Species 141

PHYSIOLOGICAL ECOLOGY Interspeciﬁc Interactions Between Bemisia tabaci Biotype B and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)

1 1,2 4 1,3 2 GUI-FEN ZHANG, DONG-CHAO LI, TONG-XIAN LIU, FANG-HAO WAN, AND JIN-JUN WANG

Environ. Entomol. 40(1): 140Ð150 (2011); DOI: 10.1603/EN10135

ABSTRACT Bemisia tabaci (Gennadius) biotype B and Trialeurodes vaporariorum (Westwood) are Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 invasive whiteßy species that often co-occur on greenhouse-grown vegetables in northern China. Although B. tabaci biotype B has been present in China for a relatively short period of time, it has become dominant over T. vaporariorum. We studied the interspeciÞc competitive interactions between the two species in single or mixed cultures at 24 Ϯ 1ЊC, 40 Ϯ 5% RH, and L14:D10 h photoperiod. Female longevity on tomato was not signiÞcantly different between species, but B. tabaci reproduced 4.3 to 4.9 fold more progeny. The ratio of female to male progeny in both instances was greater for B. tabaci. When cultured on tomato, cotton, and tobacco, B. tabaci developed 0.8, 3.3, and 4.7 d earlier in single culture, and 1.8, 3.9, and 4.3 d earlier in mixed culture. B. tabaci displaced T. vaporariorum in four, Þve and six generations when the initial ratios of B. tabaci to T. vaporariorum were 15:15, 20:10, or 10:20 on tomato. Populations of B. tabaci were 2.3 fold higher than that of T. vaporariorum on tomato plants for seven consecutive generations in single culture. B. tabaci performed better in development, survival, fecundity, and female ratio. We conclude that B. tabaci could displace T. vaporariorum in as short as four generations in a controlled greenhouse environment when they start at equal proportions. Warmer greenhouse conditions and an increase in total greenhouse area could be contributing factors in the recent dominance of B. tabaci.

KEY WORDS co-occurrence, alien species, interspeciÞc interaction, Bemisia tabaci, Trialeurodes vaporariorum

Bemisia tabaci (Gennadius) biotype B (ϭB. argenti- disorders (B. tabaci biotype B), spreading plant patho- folii Bellows & Perring) (Hemiptera: Aleyrodidae), genic viruses, and excreting honeydew that causes one of the B. tabaci species complex (Dinsdale et al. stickiness and accelerates the growth of sooty mold 2010, Xu et al. 2010, De Barro et al. 2011), is a highly (Lei and Xu 1993, Bedford et al. 1994, Blua and To- polyphagous whiteßy that colonizes Ͼ600 different scano 1994, Duffus et al. 1996, Oliveira et al. 2001, plant species cultivated in Þelds and greenhouses (in- Ramos et al. 2002, Bakshi et al. 2003). Luo et al. (2004) cluding food, Þber, and ornamental plants) as well as reported that the importance of T. vaporariorum as a weeds and other wild species (Bellows et al. 1994, pest has been gradually declining since 2000, whereas Oliveira et al. 2001, Simmons et al. 2008). It has be- that of B. tabaci biotype B has been increasing in come a major pest in China (Liu et al. 2007) since its northern China. initial invasion in the late 1990s. Trialeurodes vapo- The biotype B, one of the most invasive members of rariorum (Westwood) (Hemiptera: Aleyrodidae) was B. tabaci species complex (Crowder et al. 2010, Dins- Þrst recorded in China in the 1940s and is another dale et al. 2010), is native to the Middle East-Asia polyphagous species that has been a serious pest of Minor 1 (Dinsdale et al. 2010) but has a well-estab- vegetables and ornamental crops grown in green- lished record of displacing indigenous biotypes houses since the 1970s. Worldwide, both whiteßy spe- around the world (Costa et al. 1993, Perring 1996, cies as phloem feeders cause considerable damage to Quintero et al. 2001, Rekha et al. 2005, Liu et al. 2007). crops by reducing plant vigor, inducing phytotoxic For example, B. tabaci biotype A, an indigenous species known from the southern United States since the The Þrst two authors contributed equally to the work. late 1890s, was gradually displaced by the B biotype 1 State Key Laboratory for Biology of Plant Diseases and Insect during the early 1990s (Costa et al. 1993, Perring 1996). Pests, Institute of Plant Protection, Chinese Academy of Agricultural In southern India, B. tabaci biotype B is now more Sciences, Beijing 100193, China. 2 College of Plant Protection, Southwest University, Chongqing common than the indigenous B. tabaci even though 400716, China. the new biotype has been present for only a few years 3 Corresponding author: Institute of Plant Protection, CAAS, #12 (Rekha et al. 2005). In China, B. tabaci biotype B is the Zhong-Guan-Cun South Street, Beijing 100081, China (e-mail: predominant biotype in many regions nowadays, es- [email protected]). 4 Department of Entomology, Texas AgriLife Research, Texas A&M pecially in the areas close to large cities with frequent University System, Weslaco, TX 78596 (e-mail: [email protected]). transportation of ornamental and vegetable plants

0046-225X/11/0140Ð0150$04.00/0 ᭧ 2011 Entomological Society of America February 2011 ZHANG ET AL.: INTERSPECIFIC INTERACTIONS BETWEEN TWO WHITEFLY SPECIES 141

(Liu et al. 2007). Recent laboratory studies demon- number of progeny per female of B. tabaci biotype B strated that B. tabaci biotype B has the capacity to was greater than biotype AN (Australian) when both displace an indigenous non-B population, biotype biotypes occurred together, and that biotype B per- ZHJ-1 (Zang et al. 2006, Liu et al. 2007). In Spain, formed better in the presence of biotype AN than Pascual and Callejas (2004) reported that B. tabaci when isolated. Based on the previous evidence that B. biotype B can displace biotype Q under laboratory tabaci may have higher Þtness than T. vaporariorum conditions. Further studies conducted by Pascual under certain conditions (e.g., Tsueda and Tsuchida (2006) conÞrmed that the biological potential of bio- 1998, Luo et al. 2004, De Barro et al. 2006), the fol- type B of B. tabaci is larger than that of biotype Q lowing hypothesis was formed: in mixed populations under laboratory conditions. However, an observed of B. tabaci biotype B and T. vaporariorum, the per- decrease of B. tabaci biotype B under Þeld conditions formance of B. tabaci biotype B will be superior to T. in Spain was explained by modiÞcation of the com- vaporariorum based on various life history (namely,

petition conditions caused by the application of in- development, survival, fecundity and longevity, and Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 secticides that favored the more insecticide-resistant proportion of female density changes during interspe- biotype Q (Pascual 2006, Luo et al. 2009). Dinsdale et ciÞc interaction) measures. As a corollary to this hy- al. (2010) stated that the various recognized biotypes pothesis and based on various examples from the B. of B. tabaci may encompass 24 cryptic species. Al- tabaci biotype B literature, we predict that displace- though the taxonomy is still controversial, it is possible ment of T. vaporariorum by B. tabaci biotype B is that the previous work on B. tabaci biotypes men- possible given that both will compete for Þnite re- tioned above may actually have been dealing with sources in a greenhouse. We tested and veriÞed our different, but closely related species (Dinsdale et al. hypothesis, and herein report the results that have 2010, Xu et al. 2010, De Barro et al. 2011). implications for understanding interspeciÞc compet- Denno et al. (1995) stated that many homopteran or itive interactions between whiteßy species and other hemipteran species possess life history traits that pro- insect species that occupy similar niches on the same mote competitive interactions, including rapid popu- host plants. lation growth, aggregation, sessile behavior through- out much of their life cycle, and feeding on a common phloem resource. Usually, competition is more intense Materials and Methods among related taxa that exhibit ecological overlap as is the case with B. tabaci biotype B and T. vaporariorum Insects and Plant Materials. B. tabaci biotype B (i.e., both are highly polyphagous, share many of the adopted for this experiment was originally reared on same host plant species, adopt a sessile habit in their cabbage, Brassica oleracea variety capitata L. (Jingfeng most immature stages, etc.) (DeBach and Sundby No. 1) (Brassicaceae), at the Institute of Vegetables 1963; Liu et al. 1994a, b; Denno et al. 1995; Tsueda and and Flowers, Chinese Academy of Agricultural Sci- Tsuchida 1998; Ramos et al. 2002; Luo et al. 2004; ences (CAAS) beginning in 2000. This biotype B cul- Kaplan and Denno 2007; Inbar and Gerling 2008). ture was transferred into our laboratory in October Thus, some interspeciÞc interactions affecting Þtness 2002 and reared on cabbage for 2 yr before being components of each species (such as development moved permanently to cotton, Gossypium hirsutum L. period, reproductive success, survivorship, etc.) are to (cultivar DPL 99B, a transgenic Bacillus thuringiensis be expected (Denno et al. 1995). Berliner [Bt] cotton). In 2005, the B. tabaci culture The research conducted by Crowder et al. (2010) was transferred to tomato, Lycopersicon esculentum L. suggested that whiteßy species with superior life his- (cultivar Zhongshu No. 5). It was screened for purity tory and behavioral traits would exclude inferior spe- every 2 mo through polymerase chain reaction eval- cies. Liu et al. (1994a) reported that both B. tabaci and uation of mitochondrial cytochrome oxidase I gene T. vaporariorum co-occurred on the same leaf of green sequences according to the protocol outlined in bean or poinsettia for 50Ð60 d before the former was Frohlich et al. (1999). T. vaporariorum was collected displaced by the latter on bean or the latter was dis- from tomato plants at Jushan Farm, Beijing, in 2005. It placed by the former on poinsettia. The investigation was reared on tomato (cultivar Zhongshu No. 5) in a conducted by Luo et al. (2004) in Beijing, China in- greenhouse at 20Ð26ЊC, 60 Ϯ 10% RH and L16:D8 h dicated that the ratio of B. tabaci biotype B has been photoperiod. increasing while that of T. vaporariorum decreasing Tomato plants were used in the interspeciÞc com- since 2000 (T. vaporariorum: from 100% before 2000Ð petition experiment, and three species of host plants 15.5% in 2002; B. tabaci: from 0 to 84.5%). Tsueda and were included in the life history experiments: viz., Tsuchida (1998) stated that the total developmental tomato (cultivar Zhongshu No. 5), cotton (cultivar period in isolated culture is longer than in mixed DPL 99B), and common tobacco (Nicotiana tabacum culture for B. argentifolii and T. vaporariorum at 20ЊC L. cultivar Samsun NN). Plants were cultivated in a and 30ЊC, and that the higher survivorship and earlier mixed potting medium (soil, vermiculite, and plant development of B. argentifolii than T. vaporariorum at ash, 1:1:1) in plastic pots (130 ϫ 175 mm in diameter), 30ЊC could be caused by an asymmetric interspeciÞc and were maintained in whiteßy and thrips-proof interaction during an early developmental stage when screen cages (70 cm long, 50 cm wide, and 70 cm high; they were in mixed culture. The experiments con- Kelin Hengda Technology Development Co., Ltd., ducted by De Barro et al. (2006) showed that the Beijing, China). 142 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 1

Table 1. Various densities of adult male and female whiteﬂies of each species, B. tabaci and T. vaporariorum, used in either single or mixed species culture for competition experiments

Culture Treatment Species Females Males Subtotal Total Single species 1 B. tabaci 15 15 30 30 2 T. vaporariorum 15 15 30 30 Mixed species 3 B. tabaci 20 20 40 60 T. vaporariorum 10 10 20 4 B. tabaci 15 15 30 60 T. vaporariorum 15 15 30 5 B. tabaci 10 10 20 60 T. vaporariorum 20 20 40 Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 Interspeciﬁc Interactions: Longevity, Fecundity, were caged on the abaxial leaf surface and then re- Development, and Survival. Both whiteßy species moved 12 h later to ensure age uniformity of all im- adopted in the experiment had been separately matures. The numbers of eggs remaining after the maintained on tomato plants for 8Ð9 generations. All adults were removed were 20Ð30 eggs of each whiteßy treatments were conducted in a climatic chamber species on each leaf in mixed culture or 40Ð60 in single (PRX-450D, SAFE, Ningbo Haishu Safe Experiment culture. Survival and development of all immature Instrument Company, Ningbo, Zhejiang, China) at stages were monitored daily until adult emergence. 24 Ϯ 1ЊC, 40 Ϯ 5% RH, and L14:D10 h photoperiod. Eggs and nymphs of the two whiteßy species were This temperature was selected based on a range of separated as described by Liu and Oetting (1993). temperatures in greenhouses in northern China dur- Dead immatures of B. tabaci and T. vaporariorum were ing the time of peak populations (spring and autumn) estimated together in the mixed cultures because the of both whiteßy species, that is, 20Ð28ЊC. young ones were not easily distinguished by visual Female Longevity and Fecundity on Tomato. The inspection. objective of this experiment was to determine the Interspeciﬁc Competition and Displacement Over longevity and fecundity of each whiteßy species on Seven Generations. Competition experiments were tomato. Adults of B. tabaci and T. vaporariorum reared carried out by establishing various densities of B. on tomato plants were collected and attached to the tabaci and T. vaporariorum on caged tomato plants. lower leaf surface of tomato leaves in transparent Five treatments were tested simultaneously for the plastic truncated clip-on cages (4.3 ϫ 2.4 cm diameter, two whiteßy species (Table 1). Newly emerged white- 2.7 cm high). One newly emerged (Ͻ8 h old) female ßy adults (Ͻ10 h) were isolated in glass tubes (34 by and two male adults of B. tabaci or T. vaporariorum 10 mm in diameter) to ensure their virginity, as B. were caged onto the abaxial surface of the same com- tabaci and T. vaporariorum adults Ͻ12 h-old do not pound leaf of tomato plants (4Ð6 leaf stage). There mate (Li et al. 1989, Luan et al. 2008). The adults were were three treatments: B. tabaci only (one female ϩ then sexed under a stereomicroscope and released two males), T. vaporariorum only (one female ϩ two onto six tomato plants with four to six fully extended males), and B. tabaci and T. vaporariorum mixture true leaves. Equal numbers of males and females were (one female and two males of each species). Each released in accordance with the treatment subtotals of treatment involved 10 pairs and was repeated Þve each species as described in Table 1. The plants bear- times. Survival of the females and males was recorded ing whiteßies were enclosed in insect proof screen daily, and dead males were replaced. The adults were cages (70 cm long, 50 cm wide, and 70 cm high). Each gently transferred to a new position on the same com- treatment was repeated Þve times at 7Ð10 d intervals. pound leaf (or on the next upper one when no leaßets After introducing the adults, the cages were main- were available) in 2-d intervals. The leaßets bearing tained in a controlled greenhouse (20Ð26ЊC). Fifteen eggs were detached, and the number of eggs on each days later, all the live adults were removed from the six leaßet was counted under a stereomicroscope as de- plants in each treatment. Twenty-Þve days later (based scribed by Liu and Oetting (1993). The experiment on our previous observation, each whiteßy species com- was terminated when all the adult females were dead. pleted a generation on tomato plants under our green- Development and Survival of Immatures. This ex- house conditions in Ϸ25 d), when most of Þrst genera- periment was conducted to determine development tion (F1) adults had emerged, the adults were collected and survival during the immature stages of the two from two of the six plants every5dbyamouth aspirator, whiteßy species on tomato (cultivar Zhongshu No. 5), three times for each of the seven generations. Species, cotton (cultivar DPL 99B), and common tobacco (cul- sex, and number of collected adults were determined tivar Samsun NN) in single or mixed species. The under a stereomicroscope in the laboratory. Two clean plants were used when they reached the 4Ð6 leaf tomato plants were added after the collections of white- stage. Twenty adults of B. tabaci or T. vaporariorum ßies at each generation to ensure at least six plants avail- (female:male ϭ 1:1) were used in each of the three able. The experiment was completed when one of the treatments: B. tabaci single species, T. vaporariorum whiteßy species could not be found for 50 d in succes- single species, B. tabaci and T. vaporariorum mixed. sion. Population increases over the seven generations Each treatment was repeated Þve times. The adults were calculated by applying the following formula: I ϭ February 2011 ZHANG ET AL.: INTERSPECIFIC INTERACTIONS BETWEEN TWO WHITEFLY SPECIES 143 Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021

Fig. 1. Female longevity (A) and fecundity (B) of B. tabaci biotype B (BT) and T. vaporariorum (TV) reared in single or mixed cultures on tomato at the temperature of 24 Ϯ 1ЊC. Means between single and mixed cultures within the same whiteßy species followed by different lower case letters and those between BT and TV followed by different upper case letters differ at P Ͻ 0.05 (two-way ANOVA, LSD test).

N1/N0; where I is the population trend index, N0 is the tabaci and T. vaporariorum females reared on tomato number of initial adults in F0, and N1 is the number of plants in single culture were not signiÞcantly different Ͼ adults emerged in Fn. Percentage of B. tabaci in F1 to F7 (P 0.05) from those in mixed culture, nor was there individuals from mixed cultures was estimated as: % ϭ a signiÞcant distinction between the longevities of ϫ Nbt/Nbttv 100% in which Nbt is the number of B. tabaci either species. The mean numbers of eggs laid per B. adults, Nbttv is the number of total adults of both B. tabaci tabaci female in single or mixed culture were 276.2 and and T. vaporariorum, that of T. vaporariorum was esti- 263.8, respectively, which were 4.3 fold and 4.9 fold ϭ ϫ mated as: % Ntv/Nbttv 100%. Percentage of female higher than that of T. vaporariorum when both species adults of both species in each generation was estimated were reared on the same leaves of tomato plants. ϭ ϫ as: % Nf/Nfm 100% in which Nf is the number of Although there was no intraspeciÞc difference in fe- female adults, Nfm is the total number of male and female cundity (Fig. 1B) of either species in single or mixed adults. culture (P Ͼ 0.05), the greater number of eggs pro- Data Analysis. Percentage data were arcsine trans- duced by B. tabaci compared with T. vaporariorum was formed and numbers of female progeny per female were highly signiÞcant (P Ͻ 0.001) in the interspeciÞc com- square root transformed before analysis of variance parison.

(ANOVA). The interspeciÞc competition experiment Progeny Sex Ratio in the F1. The percentages of between B. tabaci and T. vaporariorum produced mean females of B. tabaci or T. vaporariorum were not in- numbers and percentages of adults or females of both B. ßuenced by the initial ratios of B. tabaci to T. vapo- ϭ ϭ tabaci and T. vaporariorum per plant in each generation, rariorum (B. tabaci: F3, 16 0.265, P 0.850; T. vapo- ϭ ϭ as well as population trend index, number of female rariorum: F3, 16 1.895, P 0.171) in the intraspeciÞc progeny, and percentage of females in the F1. Such data comparisons; however, a signiÞcant discrepancy was were compared by two-way ANOVA (whiteßy species detected in the comparison between the two species ϭ Ͻ and initial ratio of B. tabaci to T. vaporariorum) (SAS (F1, 17 16.804; P 0.001; Table 2). Although no Institute 2006). The fecundity, longevity, development, signiÞcant difference was observed when both white- and survival of the two whiteßy species on the same plant ßy species co-occurred in mixed cultures in equal species in single and mixed cultures or among different initial numbers (15:15), the percentages of B. tabaci host plant species were subjected to two- or three-way females in the F1 were 10.3% higher than those of T. ANOVA (whiteßy species, culture, and host plants), and vaporariorum when its initial numbers were dominant means were separated through the least signiÞcant dif- (20:10) (P ϭ 0.007), and 30.4% higher when its initial ference (LSD) test (SAS Institute 2006). The population numbers were inferior (10:20) to T. vaporariorum (P ϭ trends of both whiteßy species were described by using 0.041) (Table 2). Moreover, the percentage of B. the logistic model according to the observed data of B. tabaci females in the F1 did not signiÞcantly differ tabaci and T. vaporariorum in generations one to seven. among the treatments with different initial numbers, in contrast to those of T. vaporariorum that were sig- niÞcantly different among treatments with equal and Results dominant numbers (P ϭ 0.035).

Interspeciﬁc Interactions: Longevity, Fecundity, Number of Female Progeny in F1. The initial ratios Development, and Survival. Female Longevity and Fe- of B. tabaci to T. vaporariorum impacted the numbers cundity. As shown in Fig. 1A, the longevities of B. of female progenies produced per female of both spe- 144 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 1

Table 2. Population trend index (I1), no. of female progeny and percentage of females in the ﬁrst generation of B. tabaci biotype B (BT) and T. vaporariorum (TV) established at different initial ratios on tomato plants

Number of female progeny/& I b (mean Ϯ SE) Progeny sex ratio (&% Ϯ SE)d Initial ratio of BT to TV 1 (mean Ϯ SE)c (pair)a BT TV BT TV BT TV Single species (15:0 or 0:15) 22.7 Ϯ 2.9aA 13.6 Ϯ 1.4aB 28.4 Ϯ 3.2aA 15.2 Ϯ 1.3aB 63.1 Ϯ 1.5aA 56.4 Ϯ 2.2abB 20:10 14.3 Ϯ 1.2bA 13.4 Ϯ 1.7acA 18.2 Ϯ 1.5bA 13.9 Ϯ 2.6abA 64.0 Ϯ 0.9aA 58.0 Ϯ 1.4abB 15:15 14.0 Ϯ 2.8bA 7.5 Ϯ 1.2bA 17.7 Ϯ 3.4bA 9.0 Ϯ 1.3abB 63.5 Ϯ 1.4aA 60.7 Ϯ 1.4aA 10:20 19.1 Ϯ 1.7abA 8.3 Ϯ 2.4bcB 24.8 Ϯ 2.5abA 8.9 Ϯ 3.3bB 64.9 Ϯ 2.2aA 49.8 Ϯ 6.0bB

Means within a column followed by different lower case letters and those between BT and TV within the same sub-row followed by different upper case letters differ at P Ͻ 0.05 (two-way ANOVA, LSD test). a The sex ratio of each whiteßy species was 1:1 in the Þve treatments. b

ϭ Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 Population trend index in the F1;I1 no. of adults emerged in F1/no. of initial adults in F0. c Data were square root-transformed to meet normality assumptions. d Data were arcsine-transformed to meet normality assumptions.

ϭ ϭ cies (F3, 35 3.516; P 0.025), and a clear distinction and 4.7 d earlier in single cultures and 1.8, 3.9, and 4.3 d ϭ Ͻ was observed between the two species (F1, 17 32.035; earlier in mixed ones, respectively; P 0.05). Both P Ͻ 0.001; Table 2). The number of B. tabaci female whiteßy species (in single and mixed cultures) devel- progeny in the F1 produced per adult female was oped the earliest on tomato, intermediate on tobacco, signiÞcantly greater than those produced by T. vapo- and latest on cotton (P Ͻ 0.01; Fig. 2). rariorum in single culture (P ϭ 0.003). The same was Survival in Immature Stages. The survival rates of true in mixed cultures when initial numbers of B. immature stages of both whiteßy species were higher ϭ ϭ ϭ tabaci were equal to (P 0.043) or inferior to (P on tomato than on cotton and tobacco (F2, 40 6.139; 0.005) T. vaporariorum (Table 2). The initial species P ϭ 0.005), but no differences between the two species ratio in the mixed cultures had a signiÞcant effect on in single culture on the three host plant species (Fig. the number of female progeny produced by B. tabaci 3). Different survival rates were detected in mixed or T. vaporariorum compared with those in the single cultures from those in single cultures on different host culture, whether the initial ratio had equal numbers plants. The survival rates were not signiÞcantly dif- (B. tabaci: P ϭ 0.014) or had one species dominant ferent in single or in mixed culture on tomato and over the other (B. tabaci: P ϭ 0.027; T. vaporariorum: cotton, but were different on tobacco with a higher P ϭ 0.033; Table 2). survival rate in mixed culture than in single culture ϭ ϭ Population Trend Index in F1. The initial ratios of (F2, 12 4.667; P 0.032). B. tabaci to T. vaporariorum impacted the population Interspeciﬁc Competition and Interaction Over ϭ ϭ increases of both species (F3, 35 4.168; P 0.013), Seven Generations. Competition for Seven Generations. and prominent differences were observed between The data over the seven generations indicate that ϭ Ͻ the two whiteßy species (F1, 17 20.670; P 0.001; depending on the initial ratio of the two species, B. Table 2). The population increase of B. tabaci in the tabaci had the capacity to displace T. vaporariorum in

F1 on tomato was signiÞcantly greater than that of T. four to six generations under controlled greenhouse vaporariorum when both were in single culture (P ϭ 0.021), but also when initial numbers of B. tabaci were inferior to (P ϭ 0.012) T. vaporariorum in mixed culture (Table 2). Furthermore, the population trend indexes of B. tabaci and T. vaporariorum were lower in mixed cultures (dominant and equal initial numbers) ϭ ϭ than in single ones (B. tabaci: F3, 16 3.379, P 0.044; ϭ ϭ T. vaporariorum: F3, 16 3.585, P 0.037). The population increase of B. tabaci in the F1 was not signif- icantly different among the initial ratios of B. tabaci to T. vaporariorum, but that of T. vaporariorum was sig- niÞcantly lower in treatments with equal numbers than inferior numbers (P ϭ 0.027; Table 2). Development in Immature Stages. The development of immature stages (from egg to adult) on tomato, cotton, and tobacco was not affected by Fig. 2. Development time from egg to emergence of B. whether or not the culture was single or mixed (P Ͼ tabaci biotype B (BT) and T. vaporariorum (TV) reared on tomato, cotton, and tobacco in single and mixed cultures at 0.05; Fig. 2). However, the development of both spe- Ϯ Њ ϭ the temperature of 24 1 C. Means among different types cies differed on different host plants (F2, 57 64.304; of cultures or species within the same host plant followed by P Ͻ 0.01). During immature stages, B. tabaci devel- different lower case letters as well as among different host oped faster than T. vaporariorum on the three tested plant species followed by different upper case letters differ host plants in both single and mixed cultures (0.8, 3.3, at P Ͻ 0.05 (three-way ANOVA, LSD test). February 2011 ZHANG ET AL.: INTERSPECIFIC INTERACTIONS BETWEEN TWO WHITEFLY SPECIES 145

Barro and Hart 2000, Pascual and Callejas 2004, De Barro et al. 2006, Liu et al. 2007, Zang and Liu 2007). In addition, a superior life history (Crowder et al. 2010) that includes higher fecundity and greater capacity for resource acquisition can also determine whether species exclusion occurs between whiteßies and for other insects as well (Reitz and Trumble 2002, Crowder et al. 2010). Many of these mechanisms have been demonstrated in B. tabaci biotype B and have contributed to its capacity to invade new areas and gradually displace indigenous biotypes (De Barro et al. 2006). The greater competitive ability of B. tabaci

biotype B that is derived from these mechanisms re- Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 sults not only in higher numbers of offsprings, but also in the ability to produce proportionately more females Fig. 3. Survival of immature B. tabaci biotype B (BT) and from the same resources (De Barro and Hart 2000, De Trialeurodes vaporariorum (TV) reared on tomato, cotton, Barro et al. 2006, Liu et al. 2007). B. tabaci biotype B and tobacco in single and mixed cultures at the temperature and T. vaporariorum are different whiteßy species but Ϯ Њ of 24 1 C. Means among different types of cultures or ecologically very similar to one another (Liu et al. species within the same plant species followed by different 1994a,b; Tsueda and Tsuchida 1998; Ramos et al. 2002; lower case letters and those among different host plant species followed by different upper case letters differ at P Ͻ 0.05 Luo et al. 2004; Inbar and Gerling 2008). Mechanisms (three-way ANOVA, LSD test). Survival of immature instars of interspeciÞc interaction affecting reproductive suc- in mixed cultures was estimated for both species together. cess should also play important roles in the compet- Data were arcsine-transformed to meet normality assump- itive interaction between the two species (Reitz and tions. Trumble 2002, Crowder et al. 2010). We found that the fecundity of B. tabaci was 4.3 fold to 4.9 fold greater than that of T. vaporariorum. The numbers of B. tabaci conditions (Fig. 4AÐC). B. tabaci completely dis- female progeny in the F1 produced per adult female placed T. vaporariorum in Þve generations when the were greater than those produced by T. vaporariorum initial ratio favored B. tabaci (20:10; Fig. 4A), in four in single (P ϭ 0.003) and mixed cultures when the generations when the two species were in the same initial ratios of B. tabaci to T. vaporariorum were 15:15 proportion (15:15; Fig. 4B), or in six generations when (P ϭ 0.043) and 10:20 (P ϭ 0.005). A similar phenom- the initial ratio of B. tabaci was inferior to T. vapo- enon was reported between B. tabaci biotypes B and rariorum (10:20; Fig. 4C). AN, the latter an indigenous biotype to Australia, as Percentage of Females. The percentage of B. tabaci the relative fecundity of biotype B increased markedly females in each of the seven generations was higher as the overall density of biotype AN increased (De than that of T. vaporariorum in single culture (t ϭ Barro et al. 2006). 8.079, df ϭ 6, P Ͻ 0.001; paired samples statistics by Ecological displacement of one species, or biotype, generation) (Fig. 5A) and in mixed cultures when by another may occur because of differences in Þtness initial numbers of B. tabaci and T. vaporariorum were levels that ultimately result in a lack of resources for equal (t ϭ 3.564, df ϭ 3, P ϭ 0.038; Fig. 5C) or inferior the displaced species (Reitz and Trumble 2002, Crow- (t ϭ 3.038, df ϭ 5, P ϭ 0.029; Fig. 5D) on tomato plants. der et al. 2010). Differential resource acquisition may No signiÞcant difference was observed when the ini- have been involved in the displacement of T. vapo- tial numbers of B. tabaci were higher than those of T. rariorum by B. tabaci biotype B, similar to that which vaporariorum (t ϭ 2.074, df ϭ 4, P ϭ 0.107; Fig. 5B). has been reported for the leafminers Liriomyza trifolii Population Trends. The increase in population of B. Burgess and L. sativae Blanchard (Inbar et al. 1999a, tabaci was more than that of T. vaporariorum on to- Mayer et al. 2002, Zhang et al. 2005) or between B. mato for seven consecutive generations (t ϭ 4.720; argentifolii and cabbage looper larvae, Trichoplusia ni df ϭ 6; P ϭ 0.003) in single culture (Fig. 6). When (Hu¨ bner) (Inbar et al. 1999b), as well as for B. tabaci plotting population numbers against generations, the biotype B in competitive interactions with biotypes relationship was logistic and the nonlinear regressions ZHJ-1, AN, or Q (Crowder et al. 2010). Differential ϭ ϩ were YBT 482.625/(1 exp(3.661Ð1.4776xBT)) for B. resource acquisition in the above examples could be 2 ϭ ϭ ϩ tabaci (R 0.9782) and YTV 181/(1 exp(2.31311Ð the outcome of a shorter development time and higher 2 ϭ 1.0783xTV)) (R 0.9217) for T. vaporariorum (Fig. 6). survivorship of the better competitor (Inbar et al. 1999b, Reitz and Trumble 2002, Pascual and Callejas 2004, Crowder et al. 2010), which in the current study Discussion is represented by B. tabaci biotype B. The immatures The competition mechanisms operating in inter- of B. tabaci biotype B developed 0.8, 3.3, and 4.7 d biotype or species interactions of B. tabaci mainly earlier in single culture, and 1.8, 3.9, and 4.3 d earlier involve asymmetrical mating interference, male ag- in mixed culture than T. vaporariorum (P Ͻ 0.05) gression, and increase in frequency of copulation lead- when the two species were cultured on tomato, cot- ing to a greater proportion of female progeny (De ton, and tobacco plants, respectively (Fig. 2). How- 146 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 1 Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021

Fig. 4. Percentage of B. tabaci biotype B (BT) and T. vaporariorum (TV) in mixed cultures when BT began to co-occur with initial number of TV which was predominant (A), equal (B), or inferior (C) for seven generations on tomato plants under greenhouse conditions at the temperature from 20 to 26ЊC. ever, insects all have optimum thermal ranges that haplodiploid species, have been a driving force con- inßuence critical life history traits such as develop- tributing to widespread invasion and displacement by mental time (Shi and Ge 2010). In the current study, alien biotypes (Liu et al. 2007). Our study indicates environmental optima of the two whiteßy species are that B. tabaci is capable of displacing T. vaporariorum quite different. B. tabaci is better adapted to higher in a relatively short term on greenhouse-grown tomato temperature conditions than is T. vaporariorum, at 20Ð26ЊC. After four generations, the percentages of whereas T. vaporariorum is the better adapted species B. tabaci in the three mixed cultures increased from to lower temperature conditions (Tsueda and 66.7, 50.0, and 33.3% to 99.6, 99.8, and 98.0%, respec- Tsuchida 1998, Ramos et al. 2002, Cui et al. 2007, 2008). tively. Liu et al. (1994a) demonstrated that the same Our current experiment was carried out in growth two whiteßy species, B. tabaci and T. vaporariorum, chambers with constant temperature at 24 Ϯ 1ЊC that cannot co-occur on the same leaf of green bean or might have favored B. tabaci biotype B over T. vapo- poinsettia for a period longer than two generations. rariorum. These Þndings for the two different whiteßy species, Competition is routinely cited as one of the primary B. tabaci and T. vaporariorum, are similar to previous biotic factors that shape patterns of distribution, abun- research that recorded the displacement of indige- dance, and diversity in ecological communities (Be- nous biotypes of B. tabaci by the B biotype, for ex- gon et al. 2005). Various life histories among members ample, biotype A in southwestern United States (Per- of Hemiptera or Homoptera suggest that this order is ring et al. 1991, Bellows et al. 1994), the Australian predisposed to strong interspeciÞc competition and biotypes [indigenous eastern (EAN) and western potential ecological displacement (Denno et al. 1995, (WAN)] (De Barro and Hart 2000), and the indige- Mayer et al. 2002, Reitz and Trumble 2002, Inbar and nous China biotype ZHJ-1 (Liu et al. 2007). Liu et al. Gerling 2008, Crowder et al. 2010). Asymmetric mat- (2007) showed that in the mixed cohorts (each cohort ing interactions between closely related but previous initiated with 50% females), the percentages of female allopatric genetic groups of the whiteßy B. tabaci, a B. tabaci biotype B increased and reached 70Ð80% February 2011 ZHANG ET AL.: INTERSPECIFIC INTERACTIONS BETWEEN TWO WHITEFLY SPECIES 147 Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021

Fig. 5. Percentage of female B. tabaci biotype B (BT) and T. vaporariorum (TV) in single culture (A) and in mixed cultures when BT began to co-occur with initial number of TV which was predominant (B), equal (C), or inferior (D) for seven generations on tomato plants under greenhouse conditions at the temperature from 20 to 26ЊC. Data were arcsine-transformed to meet normality assumptions. between days 50Ð150, while that of biotype ZHJ-1 average) were higher than those of T. vaporariorum declined to 30Ð40% even though they started with the (56.6 and 51.7%, respectively) when the initial ratio of advantage of 87% ZHJ-1 to only 13% B biotype. B. tabaci was equal to (15:15) (P ϭ 0.038) or inferior The differences in performances between B. tabaci to (10:20) (P ϭ 0.029) those of T. vaporariorum. The and T. vaporariorum in the current study provided percentage of B. tabaci female progeny in the F1 re- more evidence of the competitive superiority of B. mained stable while that of T. vaporariorum female in ϭ tabaci, especially in the mixed cultures. For instance, the F1 decreased (P 0.035) when the initial ratio of percentages of B. tabaci females (61.6 and 62.6% in B. tabaci to T. vaporariorum declined from 1:1 (15:15)

Fig. 6. Dynamics of observed and predicted adult numbers of B. tabaci biotype B (BT) and T. vaporariorum (TV) from Њ F1 to F7 in single culture on tomato plants under greenhouse conditions at the temperature from 20 to 26 C. 148 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 1 to 1:2 (10:20). When established in mixed cultures together with the increasing greenhouse acreages in (the initial ratio of B. tabaci or T. vaporariorum was northern China in the last two decades. Further work equal and/or dominant in number), the number of on interspeciÞc interactions between behavior and female progeny (B. tabaci: P ϭ 0.042; T. vaporariorum: life history may provide a better understanding of the P ϭ 0.033) and population trend index of both whiteßy mechanism by which B. tabaci is able to replace T. species (B. tabaci: P ϭ 0.044; T. vaporariorum: P ϭ vaporariorum.

0.037) in the F1 declined signiÞcantly compared with B. tabaci or T. vaporariorum in single culture (Table 2). These results suggest that interference by males of the Acknowledgments opposite species could be interfering with ethology in We thank S. S. Liu (Institute of Insect Sciences, Zhejiang B. tabaci and T. vaporariorum (De Barro and Hart University, China) for discussion on the work and X. Q. Xian 2000, Liu et al. 2007). (Institute of Plant Protection, CAAS) for logistic model con- struction. We also thank the editor Gadi V. P. Reddy, two

Response surface experimental designs are suitable Downloaded from https://academic.oup.com/ee/article/40/1/140/406806 by guest on 29 September 2021 for a number of experimental objectives and can de- anonymous reviewers and one anonymous colleague for scribe the strength of intraspeciÞc and interspeciÞc their important constructive comments, as well as Y. E Chen competitions through applying a range of densities for for her technical assistance in the greenhouse. This work was funded by National Basic Research and Development Pro- each species (Inouye 2001). For example, Paini et al. gram of China, Grant No. 2009CB119200; National Key Tech- (2008) stated that applying a response surface design nologies Research and Development Program of China, and adapting a competition model can generate com- Grant No. 2006BAD08A14; and China Natural Science Foun- petition coefÞcients and quantify competition levels dation Project, Grant No. 30571254. between larvae of Frankliniella occidentalis (Per- gande) and F. tritici (Fitch). In our experiment dealing with the interactions between B. tabaci and T. References Cited vaporariorum, observations were replicated and con- Bakshi, A. K., Usha-Chauhan, K. C. Sharma, and Y. C. Gupta. ducted over multiple generations to determine which 2003. Hosts range of the greenhouse whiteßy, Trialeu- species was the superior competitor. The Logistic rodes vaporariorum (Westwood) (Homoptera: Aleyro- model is better in describing the population trends for didae) in mid-hill regions of Himachal Pradesh. 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