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

Abstract The sweetpotato whitefly, 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 arthropod predators and seven species of entomopathogenic fungi were recorded in our surveys. Aphelinid parasitoids from Encarsia and Eretmocerus genera, lady beetles 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.     

Prevalence of Wolbachia supergroups A and B in Bemisia tabaci (Hemiptera: Aleyrodidae) and some of its natural enemies

Wolbachia, a bacterial symbiont, is maternally transmitted in arthropods and nematodes. We report a systematic survey of Wolbachia taxonomy in the sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), and in some of its natural enemies. For the first time, Wolbachia infections in B. tabaci are correlated with various whitefly genetic groups, host plants, and natural enemies as well as with geographical regions. Polymerase chain reaction using 16S rDNA and fisZ genes revealed two Wolbachia supergroups, A and B, exist as single or double infections in B. tabaci as well as in some of its aphelinid parasitoids and predatory beetles. Approximately 89% of B. tabaci sampled were infected by Wolbachia, among which 34% were infected by A, 51% were infected by B, and 5% were infected by both A and B supergroups. These infection frequencies differed among B. tabaci genetic groups and locations. The invasive B. tabaci genetic group from the Middle East Asia Minor 1 (also referred as B biotype) and Mediterranean (also referred as Q biotype) was more likely to harbor A than B, whereas native genetic groups in AsiaI and AsiaII were more likely to harbor B than A. Although 60% of aphelinid parasitoids and 72% of coccinellid beetles also were infected by Wolbachia, they were more likely to host B than A. Furthermore, for the first time we report Wolbachia in B biotype from specimens collected outside of China. Construction of a phylogenetic tree clearly indicated that the Wolbachia sequences from different genetic groups of B. tabaci were not only similar to each other but also to sequences from beetles and parasitoids, which may provide evidence of coevolution and horizontal transmission of Wolbachia populations.     

Interspecific interactions between Bemisia tabaci biotype B and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)

Bemisia tabaci (Gennadius) biotype B and Trialeurodes vaporariorum (Westwood) are invasive whitefly 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 interspecific competitive interactions between the two species in single or mixed cultures at 24 ± 1 °C, 40 ± 5% RH, and L14:D10 h photoperiod. Female longevity on tomato was not significantly 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, five 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.     

Inheritance of resistance to pyriproxyfen in Bemisia tabaci (Hemiptera: Aleyrodidae) males and females (B biotype)

We evaluated effects of the insect growth regulator pyriproxyfen on Bemisia tabaci (Gennadius) (B biotype) (Hemiptera: Aleyrodidae) males and females in laboratory bioassays. Insects were treated with pyriproxyfen as either eggs or nymphs. In all tests, the LC50 for a laboratory-selected resistant strain was at least 620 times greater than for an unselected susceptible strain. When insects were treated as eggs, survival did not differ between males and females of either strain. When insects were treated as nymphs, survival did not differ between susceptible males and susceptible females, but resistant males had higher mortality than resistant females. The dominance of resistance decreased as pyriproxyfen concentration increased. Resistance was partially or completely dominant at the lowest concentration tested and completely recessive at the highest concentration tested. Hybrid female progeny from reciprocal crosses between the susceptible and resistant strains responded alike in bioassays; thus, maternal effects were not evident. Rapid evolution of resistance to pyriproxyfen could occur if individuals in field populations had resistance with traits similar to those of the laboratory-selected strain examined here.     

Effects of selected fertilizers on the life history of Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B

We tested the effects among a purportedly sustainable water-soluble fertilizer, a conventional water-soluble fertilizer, an alternation of these, a controlled-release fertilizer, and a clear water control on the life-history traits of sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae; =Bemisia argentifolii Bellows & Perring) biotype B reared on poinsettia (Euphorbia pulcherrima Willdenow ex Klotzch). Free amino acids in petioles were measured to estimate plant nutrient assimilation and phloem nutritional quality for B. tabaci biotype B. The sustainable fertilizer produced plants with the highest concentration of amino acids. In contrast, fecundity of whiteflies was lowest in plants treated with the sustainable fertilizer and the water control. The relationship between total amino acids in phloem and survival was significantly quadratic, with the highest survival at intermediate levels. Fecundity, however, was negatively correlated with total amino acid content of the maternal host plant. Variation in total amino acid concentration in petioles of plants treated within fertilizer treatments makes it difficult to predict whether a particular fertilizer will produce plants with enough amino acids to deleteriously affect both survivorship and fecundity and yet yield a plant of good quality. Despite this limitation, we can conclude that the use of this sustainable fertilizer will not cause increases in whitefly populations relative to plants fertilized with water-soluble and slow-release fertilizers that deliver the same level of nitrogen to the plant.     

Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B colonisation and leaf morphology relationships in upland cotton cultivars

Cultivars of upland cotton, Gossypium hirsutum L., are widely grown throughout the world for fibre production. They are also good reproductive hosts for Bemisia tabaci (Gennadius) biotype B. We studied the relationships between cotton leaf morphology and whitefly population densities in eight United States Deltapine and six Australian cotton cultivars and breeding lines at Holtville, California, in 1996. Results showed that okra-leaf cultivars and lines were colonised with fewer whitefly adults, eggs and nymphs compared to normal-leaf cultivars. The distance from underleaf surfaces of cotton leaves to the centres of nearest minor vascular bundles was negatively correlated with whitefly adult, egg and nymphal densities on leaves for all genotypes with the exception of the Australian breeding line 89013–114. Our results suggest that okra-leaf and distance from underleaf surfaces to the centre of nearest minor vascular bundles of cotton leaves are genetic traits that have potential for breeding whitefly-resistant upland cotton cultivars.     

Baseline susceptibility of Bemisia tabaci B biotype (Hemiptera: Aleyrodidae) populations from California and Arizona to spiromesifen

Susceptibility to spiromesifen, a tetronic acid derivative, was determined for three imidacloprid-resistant strains and 12 geographically discrete natural populations of Bemisia tabaci (Gennadius) (=Bemisia argentifolii Bellows & Perring) (Hemiptera: Aleyrodidae) from California and Arizona by laboratory bioassays. Newly emerged first instars were sprayed with aqueous serial dilutions of spiromesifen and evaluated for toxicity to establish baseline susceptibility data. Interpopulation variability in susceptibility to spiromesifen was observed among the natural populations of whiteflies up to 29-fold; however, there was only 30-fold difference in susceptibility among natural and resistant populations tested. In general, spiromesifen was quite toxic to first instars across most of their geographic range, with LC50 values ranging from 0.210 to 6.08 microg (AI)/ml. The magnitude of variation was smaller among the three-resistant strains. These results suggest that the observed variability reflect natural variation in spiromesifen susceptibility among all the test populations, possibly due to previous exposure to insecticides at each location. The effectiveness of spiromesifen also was evaluated against all immature stages of whiteflies from three field and two resistant strains. Spiromesifen was significantly more active against early instars of whiteflies based on lower LC50 values recorded compared with the fourth instars. Spiromesifen was effective against the resistant strains including a Q-biotype of B. tabaci from Spain, which is highly resistant to neonicotinoids. Results of this study indicate absence of cross-resistance between spiromesifen and more commonly used neonicotinoids. Our findings suggest that spiromesifen should be considered an ideal candidate for whitefly resistance management programs in rotation with other effective chemistries.     

国内烟粉虱B生物型的分布及其控制措施研究

收集了国内 15个省 2 6个不同地区的烟粉虱种群 ,根据有关报道合成了一个随即引物H16 ,对不同地区的烟粉虱DNA进行了RAPD -PCR扩增 ,根据扩增结果分析了不同烟粉虱种群的生物型。结果表明 ,在以上不同省市和地区中 ,北京、山东等 11个省 19个地区都有烟粉虱B型的分布。以烟粉虱B型为防治对象 ,比较了使用高效氯氰菊酯、高效大功臣 2种化学农药 ,和应用桨角蚜小蜂、粉虱座壳孢 2种寄生性天敌 ,对黄瓜上烟粉虱种群的控制效果 ,结果表明在一个世代内 ,喷施高效大功臣 (10 0 0× ,1次 ) ,喷施粉虱座壳孢 (5× 10 6 个孢子 /ml,2次 ) ,和释放桨角蚜小蜂 (3头雌蜂 /株 ,2次 ) ,对烟粉虱种群的控制作用分别达到 78.2 1%、95 .74 %和 5 7.5 8% ,三者都可以对烟粉虱起到较好的防治效果。     

Biological aspects of Bemisia tabaci (Genn.) B biotype (Hemiptera: Aleyrodidae) on six bean genotypes

The silverleaf whitefly is one of the most harmful pests that attack bean crops, mainly for extracting large quantities of phloem sap and transmitting the bean golden mosaic virus. Resistant germoplasm plants can be an important method for controlling this pest. The biological aspects of Bemisia tabaci B biotype on bean (Phaseolus vulgaris) genotypes were evaluated. The tests were conducted under laboratory conditions, with the following genotypes: Arc 1, Arc 3s, Arc 5s, G13028, G11056 and Porrillo 70. The bean plants in a stage IV-1 were infested during one day with silverleaf whiteflies. Afterwards the eggs and nymphs were observed until adult emergence. Longevity and fecundity of emerged insects were also evaluated. The longest development time occurred for nymphs fed on Arc 3s genotype (26.5 days), following by G11056 (25.9 days) and G13028 (25.3 days). The development period was 5.5 days longer in Arc 3s when compared with Porrillo 70. Also, the wild genotypes Arc 3s and G11056 showed higher mortality rates (94.7% and 83.1%, respectively), which may suggest antibiosis and/or feeding nonpreference resistance type. For this reason, although longevity and fecundity were not influenced when the whitefly fed on resistant genotypes (Arc 3s, G11056, G13028 and Arc 5s), those genotypes can be used for bean breeding program towards B. tabaci B biotype.     

Susceptibility of the tobacco whitefly,Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q to entomopathogenic fungi

Recently, the Q biotype of tobacco whitefly has been recognized as the most hazardous strain of Bemisia tabaci worldwide because of increased resistance to some insecticide groups requiring alternative strategies for its control. We studied the susceptibility of this biotype of B. tabaci to 21 isolates of Beauveria bassiana, three isolates of Isaria fumosorosea, one isolate of I. cateni, three isolates of Lecanicillium lecanii, one isolate of L. attenuatum, and one isolate of Aschersonia aleyrodis. These isolates were evaluated on pruned eggplant seedlings, at a concentration of 10⁸ conidia/mL (deposited at 6000±586 conidia mm^?2). The mortality based on mycosis varied from 18 to 97% after 6 days. Isaria fumosorosea isolate Pf04, B. bassiana isolates Bb06, Bb12, and L. lecanii L14 were found the most effective. Furthermore, five isolates were chosen for concentration–mortality response assays and compared to B. bassiana GHA as a standard. The numbers of nymphs infected by fungi were correlated with the spore concentration. L. lecanii L14 and I. fumosorosea Pf04 had the shortest LT₅₀ at 3.5 and 3.3 days at 6000±586 conidia mm^?2. Mortality declined and LT₅₀ values were longer as the concentration of conidia was reduced. The LD₅₀ values were calculated as 87, 147, 191, 263, and 269 conidia mm^?2 for isolates L14, GHA, AS1260, Bb13, and Pf04, respectively. These results indicated that the Q biotype of sweetpotato whitefly was susceptible to the five isolates of entomopathogenic fungi and these isolates have potential to be developed as microbial pesticides for whitefly control.     

A new record for Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) species complex of Turkey

In this study, species complex of Turkish Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) populations was determined by PCR‐based DNA analysis. According to phylogenetic analyses, the B. tabaci samples have been identified within three generic groups. A major part of the samples belonged to two invasive species, either Middle East–Asia Minor 1 (MEAM1) or Mediterranean (MED). In addition to these two invasive species, several samples collected from greenhouses and cotton fields have been found to be related to Middle East–Asia Minor 2 (MEAM2), which is the first record of Turkish B. tabaci species complex.     

Biology and non-preference for oviposition by Bemisia tabaci (Gennadius) biotype B (Hemiptera: Aleyrodidae) on cotton cultivars

The purposes of this work were to evaluate some biological aspects of Bemisia tabaci (Gennadius) biotype B at egg and nymphal stages and to evaluate the non-preference for oviposition and its correlation with the number and type of trichomes on the cotton cultivars BRS Ipê, BRS 186-Precoce 3, BRS Acala, BRS Verde, BRS-200 Marrom, BRS Cedro, BRS Ita 90-2 and BRS Aroeira. The experiments were conducted in climatic chambers at 28 +/- 2 degrees C, 70% RH and photophase of 14h, and in greenhouse. Egg fertility was not affected by the cotton cultivars but survival in egg-adult period was influenced by the host plant. There was no influence of cultivars neither on the duration of egg stage, nymphs at 2nd, 3rd and 4th instars nor on the duration from egg to adult, but nymphs reared on the cultivar BRS Ipê had their 1st instar extended. Low number of eggs was detected on the cultivars BRS Aroeira, BRS Verde and BRS Ita 90-2 in both experiments with and without oviposition choice, indicating a possible mechanism of resistance, but no correlation could be established between trichome densisty and oviposition non-preference.     

Endosymbiont metacommunities,mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex

Bemisia tabaci, an invasive pest that causes crop damage worldwide, is a highly differentiated species complex, divided into biotypes that have mainly been defined based on mitochondrial DNA sequences. Although endosymbionts can potentially induce population differentiation, specialization and indirect selection on mtDNA, studies have largely ignored these influential passengers in B. tabaci, despite as many as seven bacterial endosymbionts have been identified. Here, we investigate the composition of the whole bacterial community in worldwide populations of B. tabaci, together with host genetic differentiation, focusing on the invasive B and Q biotypes. Among 653 individuals studied, more than 95% of them harbour at least one secondary endosymbiont, and multiple infections are very common. In addition, sequence analyses reveal a very high diversity of facultative endosymbionts in B. tabaci, with some bacterial genus being represented by more than one strain. In the B and Q biotypes, nine different strains of bacteria have been identified. The mtDNA‐based phylogeny of B. tabaci also reveals a very high nucleotide diversity that partitions the two ITS clades (B and Q) into six CO1 genetic groups. Each genetic group is in linkage disequilibrium with a specific combination of endosymbionts. All together, our results demonstrate the rapid dynamics of the bacterial endosymbiont–host associations at a small evolutionary scale, questioning the role of endosymbiotic communities in the evolution of the Bemisia tabaci species complex and strengthening the need to develop a metacommunity theory of inherited endosymbionts.     

Genetic differentiation of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype Q based on mitochondrial DNA markers

In the present study, genetic differentiation of Bemisia tabaci (Gennadius) biotype Q was analyzed based on mitochondrial cytochrome oxidase I (mt COI) gene sequence. The results showed that B. tabaci biotype Q could be separated into two subclades, which were labeled as subclades Q1 and Q2. Subclade Q1 was probably indigenous to the regions around the Mediterranean area and subclade Q2 to Israel or Cyprus. It was because B. tabaci was composed of several genetically distinct groups with a strong geographical association between more closely related biotypes. Not all of the B. tabaci biotype Q in the non‐Mediterranean countries come from the same regions. Until now, all B. tabaci biotype Q in China were grouped into subclade Q1. The B. tabaci biotype Q introduced into the US included both subclades Q1 and Q2. The genetic structure analysis showed higher genetic variation of subclade Q1 than that of subclade Q2.     

Resistance of soybean genotypes to Bemisia tabaci (Genn.) Biotype B (Hemiptera: Aleyrodidae)

The silverleaf whitefly Bemisia tabaci (Genn.) biotype B has become a serious problem for soybean cultivation because it can significantly reduce soybean productivity. The use of soybean cultivars resistant to whitefly attack is an important strategy in an integrated pest management (IPM) program. This study evaluated the preference for oviposition and colonization by B. tabaci biotype B on different soybean genotypes. In the free-choice test, the genotypes studied were 'IAC 17' and 'IAC 19' as the standards for resistance and 'IAC Holambra Stwart' as the standard for susceptibility, as well as BABR01-0492, BABR01-0173, BABR01-1259, BABR01-1576, BABR99-4021HC, BABR99-4021HP, 'Barreiras', 'Conquista', 'Corisco', 'BRS Gralha', PI274454, PI227687, and PI171451. In the no-choice test, the four best genotypes selected in the free-choice test, in addition to the susceptible and resistant standards were evaluated. Our data indicated 'Barreiras' as the most resistant genotype against B. tabaci biotype B. 'BRS Gralha', which was the least attractive to whitefly adults in the free-choice test, did not show resistance to insect attack when they were confined in cages in the no-choice test. Despite the high number of eggs observed, BABR01-1576 and BABR99-4021HC showed a reduced number of nymphs, indicating antibiosis. The genotypes with a high level of resistance can be used as a tool against B. tabaci in IPM or as a source of resistance in plant-breeding programs.     

Multiple generation effects of high temperature on the development and fecundity of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B

Insects are ectotherms and their ability to resist temperature stress is limited. The immediate effects of sub‐lethal heat stress on insects are well documented, but longer‐term effects of such stresses are rarely reported. In this study, survival, development and reproduction of the whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B, were compared over five consecutive generations at 27, 31 and 35 °C and for one generation at 37 °C. Both temperature and generation significantly affected the fitness of the whitefly. These impacts were more dramatic with increasing generations and temperatures. Among the experimental temperatures, the most favorable for development and reproduction were 27 °C and 31 °C. At 27 °C, survival, development and fecundity were all stable over these five generations. At 31 °C, immature survival rate was the highest in the fifth generation, but female fecundities decreased in the fourth and fifth generations. At 35 °C, egg hatching rate, immature survival rate and female fecundity decreased significantly in the fourth and fifth generations. At 37 °C, survival of B. tabaci was not adversely affected, but female fecundity at 37 °C was less than 10% of that at 27 °C or 31 °C. These results demonstrate that the lethal high temperature for B. tabaci is over 37 °C, and the whitefly population continued expanding in the five generations at 35 °C. The ability of B. tabaci biotype B to survive high temperature stress will play an important role in its population extension under global warming.     

Temperature-dependent development models of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Q biotype on three host plants

Temperature-dependent development of the sweet potato whitefly, Bemisia tabaci (Gennadius), Q biotype was examined on three host plants (bell pepper, oriental melon, and eggplant) at nine temperatures (15, 17.5, 20, 22.5, 25, 27.5, 30, 32.5, and 35 °C). Egg development time (least squares [LS]-mean ± LS-standard error [SE]) varied from 31.78 ± 0.29 days at 15 °C to 4.93 ± 0.25 days at 32.5 °C on bell pepper, from 21.27 ± 0.20 days at 17.5 °C to 4.02 ± 0.23 days at 32.5 °C on oriental melon, and from 26.92 ± 0.19 days at 15 °C to 5.14 ± 0.18 days at 30 °C on eggplant. Nymph development time (LS-mean ± LS-SE) varied from 76.54 ± 0.96 days at 15 °C to 12.96 ± 0.68 days at 27.5 °C on bell pepper, from 48.78 ± 0.38 days at 17.5 °C to 11.32 ± 0.38 days at 32.5 °C on oriental melon, and from 73.08 ± 1.23 days at 15 °C to 11.89 ± 0.70 days at 27.5 °C on eggplant. A non-linear relationship between developmental rate and temperature was described by the Taylor model, and developmental variation was described by the two-parameter Weibull function.     

Asymmetry in thermal tolerance trade-offs between the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae)

We investigated life history trade-offs related to thermal tolerance in two sibling species, commonly referred to as the B and Q biotypes, of Bemisia tabaci. We focused on basal resistance to short unpredicted heat stress, which reflects the organism investment, during both optimal and stressful conditions, in insuring its survival. At 27 °C, the relative reproductive performance of B was seven-fold higher than Q. After short stress of 42 °C, these differences increased to 23-fold. A turnover took place after short stress of 43 and 45 °C, in which Q adults performed better. As the expression of the analysed Hsp70 and other stress-related genes was found to be higher in the Q species, our data likely reflects two different strategies for optimal performance. B lowers soma protection for achieving maximum reproduction ('direct inhibitory' trade-off model), whereas Q invests significant resources in being always 'ready' for a challenge.