Differential indirect effects of two plant viruses on an invasive and an indigenous whitefly vector: implications for competitive displacement

The role of vector–begomovirus–plant interactions in the widespread invasion by some members of the whitefly species complex Bemisia tabaci is poorly understood. The invasive B biotype of B. tabaci entered China in the late 1990s and had become the predominant or only biotype of the whitefly in many regions of the country by 2005–2006. Meanwhile epidemics of begomoviruses have been observed in many crops including tomato for which Tomato yellow leaf curl China virus (TYLCCNV) and Tomato yellow leaf curl virus (TYLCV) have been identified as two major disease-causing agents. Here, we conducted laboratory experiments to compare the performance of the invasive B and indigenous ZHJ1 whitefly biotypes on uninfected, TYLCCNV-infected and TYLCV-infected plants of tomato cv. Hezuo903, a cultivar that has been widely cultivated in many regions of China. The infection of tomato plants by either of the viruses had no or only marginal effects on the development, survival and fecundity of the B biotype. In contrast, survival and fecundity of the ZHJ1 biotype were significantly reduced on virus-infected plants compared to those on uninfected plants. Populations of the B biotype on uninfected and TYLCCNV-infected plants increased at similar rates, whereas population increase of the ZHJ1 biotype on TYLCCNV-infected plants was affected adversely. These asymmetric responses to virus infection of tomato plants between the B and ZHJ1 biotypes are likely to offer advantages to the B biotype in its invasion and displacement of the indigenous biotype.     

豇豆轻斑驳病毒CPMMV感染菜豆对B型烟粉虱寄主选择和生物学特性的影响

豇豆轻斑驳病毒（Cowpea mild mottle virus,CPMMV）的流行与其媒介昆虫烟粉虱Bemisia tabaci密切相关,但CPMMV感染寄主植物对B型烟粉虱寄主选择行为和生物学特性的影响尚不清楚。本研究探究了1）CPMMV感染菜豆Phaseolus vulgaris不同时间对B型烟粉虱寄主选择和产卵偏好性的影响;2）CPMMV感染菜豆对B型烟粉虱生物学特性的影响。结果发现：1）相较于健康菜豆,摩擦接种CPMMV后1周,B型烟粉虱却偏好在CPMMV感染的植株上停留和产卵;而摩擦接种后4周,B型烟粉虱却偏好在健康的植株上停留和产卵;2）无论是在摩擦接种后1周和4周的CPMMV感染植株上,B型烟粉虱在健康和CPMMV感染植株上的产卵量和存活率差异不明显。可见,CPMMV感染菜豆对于B型烟粉虱的寄主选择偏好性具有时间效应,而CPMMV感染菜豆对于B型烟粉虱的生物学特性没有显著影响。     

烟粉虱和温室粉虱在甘蓝上的刺探取食行为比较

利用刺吸电波图技术研究B型、ZHJ_1型烟粉虱Bemisia tabaci(Gennadius)和温室粉虱Trialeurodes vaporariorum(Westwood)在甘蓝上的取食行为,将3种粉虱的电波图进行比较,其中,B型和ZHJ_1型烟粉虱记录到np,C,pd,E1,E2,F和G波7种波形,温室粉虱只记录到刺探波形,少有取食波形。B型的20个记录中只有1个没有持续吸食波形;ZHJ_1型的25个记录中有10个记录没有持续吸食波形;温室粉虱没有持续吸食记录。甘蓝叶片韧皮部的结构或汁液的化学成分与温室粉虱的抗性密切相关。     

Plant nitrogen status rapidly alters amino acid metabolism and excretion in Bemisia tabaci

The effect of plant nitrogen (N) status on the content and distribution of free amino acids in the bodies and honeydew of silverleaf whiteflies Bemisia tabaci (Gennadius) Biotype B (= B. argentifolii Bellows and Perring) was determined. Whiteflies fed for 4 days on cotton leaves that received high or low N fertility. For low-N plants, photosynthesis and leaf total N levels were decreased, and a much-reduced amount of free amino acids was recovered in phloem sap. Low N fertility did not affect whitefly total N content, but did markedly decrease the free amino acid content. Glutamine, alanine and proline accounted for over half of the insect free amino acid pool for both N treatments. On a relative basis, adjustments in glutamine levels in response to plant N status were much larger compared to the other amino acids. Large amounts of amino N, especially asparagine, were excreted from whiteflies fed on high-N plants whereas amino N excretion essentially ceased for whiteflies fed on low N plants. The distribution of amino acids in the insects and honeydew was not closely related to the phloem sap amino acids. However, total amino acid excretion was quite indicative of the plant N status and the quality of the insect diet. The results indicated that whitefly free amino acid pools and excretion of amino N were rapidly altered by plant N status.     

Difference in feeding behaviors of two invasive whiteflies on host plants with different suitability: implication for competitive displacement

In China, Bemisia tabaci Q (commonly known as biotype Q) has rapidly displaced B (commonly known as biotype B) in the past 6 years. The mechanisms underlying such phenomenon have been studied extensively in recent years; however, we have not come to a definitive conclusion yet. In the present study, the differences in host suitability between B and Q whitefly adults to five host plants (cabbage, cotton, cucumber, poinsettia, and tomato) were evaluated based on their respective feeding behaviors using a direct-current electrical penetration graph (DC-EPG) system. Pair-wise comparisons of B. tabaci B and Q feeding on each of the five host plants clearly indicate that Q feeds better than B on tomato, cotton and poinsettia, while B feeds better than Q on cabbage and cucumber. The EPG parameters related to both phloem and non-phloem phases confirm that cabbage and cucumber are best suited to B, while tomato, cotton, and poinsettia are best suited to Q. Our present results support the contention that host suitability and adult feeding behavior contribute to the competitive displacement of biotype B by biotype Q. The discrepancy between field (previous studies) and laboratory results (this study), however, suggests that 1) whitefly displacement is apparently contributed by multiple factors; and 2) factor(s) other than the host plant suitability may play a vital role in dictating the whitefly biotypes in the field.     

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.     

Vector-virus mutualism accelerates population increase of an invasive whitefly

The relationships between plant viruses, their herbivore vectors and host plants can be beneficial, neutral, or antagonistic, depending on the species involved. This variation in relationships may affect the process of biological invasion and the displacement of indigenous species by invaders when the invasive and indigenous organisms occur with niche overlap but differ in the interactions. The notorious invasive B biotype of the whitefly complex Bemisia tabaci entered China in the late 1990s and is now the predominant or only biotype in many regions of the country. Tobacco curly shoot virus (TbCSV) and Tomato yellow leaf curl China virus (TYLCCNV) are two whitefly-transmitted begomoviruses that have become widespread recently in south China. We compared the performance of the invasive B and indigenous ZHJ1 whitefly biotypes on healthy, TbCSV-infected and TYLCCNV-infected tobacco plants. Compared to its performance on healthy plants, the invasive B biotype increased its fecundity and longevity by 12 and 6 fold when feeding on TbCSV-infected plants, and by 18 and 7 fold when feeding on TYLCCNV-infected plants. Population density of the B biotype on TbCSV- and TYLCCNV-infected plants reached 2 and 13 times that on healthy plants respectively in 56 days. In contrast, the indigenous ZHJ1 performed similarly on healthy and virus-infected plants. Virus-infection status of the whiteflies per se of both biotypes showed limited effects on performance of vectors on cotton, a nonhost plant of the viruses. The indirect mutualism between the B biotype whitefly and these viruses via their host plants, and the apparent lack of such mutualism for the indigenous whitefly, may contribute to the ability of the B whitefly biotype to invade, the displacement of indigenous whiteflies, and the disease pandemics of the viruses associated with this vector.     

Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci

The sweet potato whitefly, Bemisia tabaci, harbors Portiera aleyrodidarum, an obligatory symbiotic bacterium, as well as several secondary symbionts including Rickettsia, Hamiltonella, Wolbachia, Arsenophonus, Cardinium and Fritschea, the function of which is unknown. Bemisia tabaci is a species complex composed of numerous biotypes, which may differ from each other both genetically and biologically. Only the B and Q biotypes have been reported from Israel. Secondary symbiont infection frequencies of Israeli laboratory and field populations of B. tabaci from various host plants were determined by PCR, in order to test for correlation between bacterial composition to biotype and host plant. Hamiltonella was detected only in populations of the B biotype, while Wolbachia and Arsenophonus were found only in the Q biotype (33% and 87% infection, respectively). Rickettsia was abundant in both biotypes. Cardinium and Fritschea were not found in any of the populations. No differences in secondary symbionts were found among host plants within the B biotype; but within the Q biotype, all whiteflies collected from sage harboured both Rickettsia and Arsenophonus, an infection frequency which was significantly higher than those found in association with all other host plants. The association found between whitefly biotypes and secondary symbionts suggests a possible contribution of these bacteria to host characteristics such as insecticide resistance, host range, virus transmission and speciation.     

Influence of plant combinations on population characteristics of Bemisia tabaci biotypes B and Q

In recent years, the dominant biotype of Bemisia tabaci (Gennadius) has shifted from biotype B to Q in many locations of China. Our field monitoring showed that B. tabaci biotype Q could be found on pepper Capsicum frutescens L. while biotype B could not be found on the plant. To study the role of the host plant in the displacement of biotype B by Q, the adult mortality, female fecundity, and adult emergence of both biotypes B and Q on different host combinations were studied using a model system involving pepper and eggplant. The results showed that pepper is not a preferred host for either biotype B or Q adults in comparison with eggplant. The negative impact of pepper to biotype B is, however, much greater than that to biotype Q. Because both the survival rates of the adult whitefly and the average number of emerged adults per female of biotype Q on pepper are higher than that of biotype B, biotype Q showed higher fitness in comparison with biotype B. Our results suggest that the existence and differential impact of a nonpreferred host might affect the population fitness and therefore could play a role in the displacement of biotype B in some regions.     

甘蓝与黄瓜寄主上B型烟粉虱和温室白粉虱蜜露糖分、氨基酸和挥发物组分的比较分析

粉虱蜜露是粉虱寄生性天敌搜索寄主的主要利它素源。应用离子色谱分别对甘蓝与黄瓜上B型烟粉虱(Bemisia tabaci B-biotype)蜜露以及黄瓜上温室白粉虱Trialeurodes vaporariorum蜜露的接触性利它素糖和氨基酸组分和含量进行了比较研究。结果表明：2种粉虱在不同寄主植物上的蜜露均富含糖和氨基酸,其中糖含量占绝对优势,甘蓝上B型烟粉虱蜜露、黄瓜上B型烟粉虱蜜露和黄瓜上温室白粉虱蜜露中的糖含量分别是相应氨基酸含量的42.5、2.6和5.4倍,其中糖类物质中又以寡糖含量占绝对优势,分别占89.3%、81.7%和88.2%。不同寄主植物和粉虱种类显著影响蜜露中糖和氨基酸的组成和含量。其中,甘蓝上B型烟粉虱蜜露中的寡糖以二糖占优势,占97.3%;二糖中又以蔗糖异构糖和松二糖占优势,分别占52.7%和35.4%。黄瓜上B型烟粉虱蜜露和温室白粉虱蜜露寡糖中以三糖和四糖占优势,分别占73.1%和85.4%;优势糖水苏（四）糖和松三糖分别占40.3%和 26.2%及49.9%和27.0%。甘蓝上B型烟粉虱蜜露中氨基酸以丙氨酸占优势,含量为66.5%;而黄瓜上B型烟粉虱及温室白粉虱蜜露中氨基酸以甘氨酸含量最高,分别占氨基酸总量的38.2%和51.7%。应用GC-MS对甘蓝上B型烟粉虱蜜露和黄瓜上温室白粉虱蜜露挥发物组分的鉴定结果显示,两种粉虱蜜露中共同含有的主要挥发物为邻苯二甲酸二（2-乙基）己酯。     

利用RAPD-PCR方法鉴定我国烟粉虱的生物型

收集了国内北京、山东、广东和海南等14个省市23个地区的蔬菜、园林花卉和杂草上的23个烟粉虱Bemisia tabaci (Gennadius)种群,根据报道合成了一个随机引物H₁₆,运用RAPD-PCR技术对所收集的烟粉虱种群进行了生物型鉴定。结果表明在23个烟粉虱种群中,有17个种群同属于危害严重的“B生物型”,这些种群主要分布在交通便利的城市或沿海地区,而非B生物型则主要分布在交通不便的山区或内陆。对烟粉虱B生物型的分布与寄主植物和环境条件进行了初步的探讨。     

Silicon influence on resistance induction against Bemisia tabaci biotype B (Genn.) (Hemiptera: Aleyrodidae) and on vegetative development in two soybean cultivars

The potential of populations of Bemisia tabaci (Genn.) to become resistant to insecticides has stimulated research into alternative tactics of integrated pest management such as the induction of host-plant resistance. Recent data have shown that silicon can increase the degree of resistance of host plants to insect pests. Therefore the aim of our work was to study the effects of silicon application on the vegetative development of soybean plants and on the induction of resistance to the silverleaf whitefly, B. tabaci biotype B. We performed choice and no-choice tests of oviposition preference on two soybean cultivars, IAC-19 (moderately resistant to B. tabaci biotype B) and MONSOY-8001 (susceptible), with and without application of silicon. Silicon did not affect silverleaf whitefly oviposition preferences, but caused significant mortality in nymphs. Thus, silicon increased the degree of resistance to silverleaf whitefly. Silicon decreased the production of phenolic compounds, but did not affect lignin production. However, when applied to cultivar IAC-19, it increased the production of non-protein organic nitrogen. Silicon had no effect on the vegetative development of soybean plants, but it increased the degree of resistance to the silverleaf whitefly. We conclude that silicon applications combined with cultivar IAC-19 can significantly decrease silverleaf whitefly populations, having a positive impact both on the soybean plant and on the environment.     

华东、华南和西南地区烟粉虱的种群及寄主分化

烟粉虱Bemisia tabaci是一个复合种,它具有的生物型分化、较强的传播病毒的能力和抗药性、较快的繁殖速率等特征使其成为我国农业生产中重要害虫之一。本研究利用细胞色素线粒体氧化酶Ⅰ基因,对采集自江苏、广东和云南三省的烟粉虱样本进行了生物型鉴定,并对烟粉虱生物型与寄主植物之间的关联性开展了调查。结果表明,在广东和云南省,都存在未鉴定的土著种群与入侵的B型、Q型共存的现象;同时,在本研究中广东省尚未采集到Q型烟粉虱,而在江苏采集到的粉虱样本全部为入侵型。研究结果还表明,相对于入侵种而言,土著种群显示出更强的寄主植物趋同性;丰富的寄主植物以及本身具有的多食性特性有助于B型、Q型等生物型在世界各地的广泛入侵。     

不同作物田烟粉虱发生的时空动态

2008～2009年连续2年系统调查了番茄、茄子、棉花、大豆、玉米等寄主植物上烟粉虱种群发生的时间与空间动态。结果表明：不同寄主植物上的烟粉虱成虫及其伪蛹数量有显著性差异,其密度大小依次为：茄子>棉花>番茄>大豆>玉米。其中,在玉米上除了发现极少量的成虫逗留外,没有发现烟粉虱的卵及若虫。在发生的时间序列上,烟粉虱成虫及伪蛹的数量呈现为先逐渐上升后又下降的变化过程,发生高峰期集中在8月5日到8月31日,9月初以后烟粉虱数量慢慢减少。在空间分布上,表现为烟粉虱成虫喜食寄主的上部叶片。统计分析显示,寄主对烟粉虱成虫和伪蛹的数量的影响极显著,而年份对其数量的影响没有显著差异。由此得出的烟粉虱发生和达到高峰的时间,可为烟粉虱预测预报和区域性综合治理提供重要理论依据。     

Assessment of Potential Sublethal Effects of Various Insecticides on Key Biological Traits of The Tobacco Whitefly,Bemisia tabaci

The tobacco whitefly Bemisia tabaci is one of the most devastating pests worldwide. Current management of B. tabaci relies upon the frequent applications of insecticides. In addition to direct mortality by typical acute toxicity (lethal effect), insecticides may also impair various key biological traits of the exposed insects through physiological and behavioral sublethal effects. Identifying and characterizing such effects could be crucial for understanding the global effects of insecticides on the pest and therefore for optimizing its management in the crops. We assessed the effects of sublethal and low-lethal concentrations of four widely used insecticides on the fecundity, honeydew excretion and feeding behavior of B. tabaci adults. The probing activity of the whiteflies feeding on treated cotton seedlings was recorded by an Electrical Penetration Graph (EPG). The results showed that imidacloprid and bifenthrin caused a reduction in phloem feeding even at sublethal concentrations. In addition, the honeydew excretions and fecundity levels of adults feeding on leaf discs treated with these concentrations were significantly lower than the untreated ones. While, sublethal concentrations of chlorpyrifos and carbosulfan did not affect feeding behavior, honeydew excretion and fecundity of the whitefly. We demonstrated an antifeedant effect of the imidacloprid and bifenthrin on B. tabaci, whereas behavioral changes in adults feeding on leaves treated with chlorpyrifos and carbosulfan were more likely caused by the direct effects of the insecticides on the insects'' nervous system itself. Our results show that aside from the lethal effect, the sublethal concentration of imidacloprid and bifenthrin impairs the phloem feeding, i.e. the most important feeding trait in a plant protection perspective. Indeed, this antifeedant property would give these insecticides potential to control insect pests indirectly. Therefore, the behavioral effects of sublethal concentrations of imidacloprid and bifenthrin may play an important role in the control of whitefly pests by increasing the toxicity persistence in treated crops.     

烟粉虱生物型研究进展

烟粉虱B em isia tabaci(G ennad ius)是一种取食植物汁液的重要农业害虫,同时也是许多植物病毒最重要的传播介体之一。烟粉虱被认为是由许多具有明显遗传分化的不同种群即生物型组成的复合种,其中B型烟粉虱是一种入侵性最强的生物型,几乎在世界各地均有分布。由于不同生物型的烟粉虱在寄主范围、传毒能力、地理分布、抗药性等许多生物学方面存在差异,因此对烟粉虱生物型的鉴定及其遗传分化研究对于该害虫的可持续控制具有重要的指导意义。烟粉虱生物型的鉴定方法包括生物学鉴定、酶谱鉴定以及分子标记鉴定的方法,其中使用的分子标记包括RAPD、AFLP、rDNA-ITS1、m tDNA CO I以及SSR等标记。目前,不同生物型的烟粉虱尤其B型烟粉虱的分类地位仍然存在争议。介绍了不同生物型烟粉虱的生物学差异、鉴定方法及其遗传分化研究的最新进展,同时探讨了不同生物型烟粉虱的分类地位和研究方向。     

New insights into the mitochondrial phylogeny of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in the Mediterranean Basin

The whitefly Bemisia tabaci is vector of plant infecting viruses and it is considered as one of the most important agricultural pests around the Mediterranean basin. At present, five biotypes of B. tabaci have been reported in the Mediterranean Basin: B, Q, S, T and M. To establish the phylogeographic relationship of these Mediterranean biotypes with others, 54 samples collected in Europe and Africa were analysed by sequencing the mitochondrial cytochrome oxidase I gene (mtCOI). The phylogeny showed that Spanish samples corresponding to the biotype S were related to the haplotype Uganda 2 of the African clade, associated with recent epidemic upsurges of cassava mosaic virus (CMD) in that country. This phylogeographic relationship gave support to a distinct subgroup revealed within the African clade. Bemisia tabaci collected from Euphorbia plants in Italy (biotype T) formed one of the three distinct subgroups existing within the Southeast/Far East Asian clade, while samples from Turkey (biotype M) clustered together with reference mitochondrial sequences from whiteflies from Pakistan and Thailand. Recent reports indicate that Bemisia populations corresponding to the biotypes S and T are distributed in areas larger than those initially delimited. Other results indicated that samples collected in Sudan grouped within the Mediterranean–North Africa clade together with reference sequences of the biotype Q corresponding to insects collected in Spain and Morocco. Mitochondrial haplotypes of B. tabaci samples collected on sweet potato in Ghana clustered with reference sequences of samples from Cameroon corresponding to one of the five Sub-Saharan subgroups already described in the African clade. These data extends the phylogenetic information of the B. tabaci species complex and present new questions to be investigated.     

施用钾肥对烟粉虱实验种群生命表参数的影响

设置0,30,60,120和240mg/L5种钾肥浓度处理黄瓜植株,测定不同处理黄瓜叶片的含钾量及相应处理上烟粉虱Bemisiatabaci(Gennadius)种群的生命表参数。结果表明,黄瓜叶片含钾量不随钾肥施用量增加而增大,30mg/L钾肥溶液处理的黄瓜叶片含钾量最高。在上述5种钾浓度处理黄瓜植株上,烟粉虱种群的内禀增长率rm分别为0.14,0.17,0.17,0.15和0.13,净增殖率R0依次为47.79,111.55,115.18,61.96和49.58。因此,黄瓜叶片中含钾量高有利于烟粉虱的种群增长。讨论研究结果对生产上烟粉虱种群调控的意义。     

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.     

B型烟粉虱对不同蔬菜品种趋性的评价

B型烟粉虱是目前我国蔬菜作物上的主要害虫之一。为探索有效的B型烟粉虱非化学防治方法 ,作者于 2 0 0 1年 8月至 9月进行了该粉虱对 2 1个蔬菜品种趋性的田间评价。结果表明 ,B型烟粉虱最嗜好西瓜 ,对结球茴香最不敏感。在可选择的条件下 ,B型烟粉虱成虫对作物的趋性依次为西瓜 >黄瓜 ,十字花科类 ,番茄 >甜 (辣 )椒 >结球茴香