Bemisia tabaci: The current situation in the UK and the prospect of developing strategies for eradication using entomopathogens

Abstract The sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) remains a serious threat to crops worldwide. The damaging B‐biotype is of specific economic concern because it is an effective vector of over 111 viruses from several families, particularly geminiviruses. Bemisia tabaci is regularly intercepted on plants coming into the UK where it is subjected to a policy of eradication. The UK maintains Protective Zone status against this pest. A main pathway of entry of B. tabaci into the Protected Zone involves propagating material, especially Poinsettia (Euphorbia pulcherrima). With increased insecticide resistance continuously being recorded, B. tabaci is becoming more difficult to control/eradicate. Recent research involving both entomopathogenic nematodes and fungi is showing much potential for the development of control programs for this pest. Both the nematode Steinernema feltiae and the fungus Lecanicillium muscarium have been shown to be most effective against second instar B. tabaci. Fine‐tuning of the environmental conditions required has also increased their efficacy. The entomopathogens have also shown a high level of compatibility with chemical insecticides, all increasing their potential to be incorporated into control strategies against B. tabaci.     

Insecticide resistance monitoring in whitefly (Bemisia tabaci) (Hemiptera: Aleyrodidae) in Oman

The sweet potato whitefly, Bemisia tabaci Gennadius, is an important insect pest of many crops including vegetables through direct feeding damage and as a vector of several plant viruses. Intensive use of insecticides has led to the development of insecticide resistance in global B. tabaci populations. This study was conducted to establish susceptibility levels to deltamethrin, thiamethoxam and pyriproxyfen in seven geographically different populations of B. tabaci MEAM1 adults in Oman. All B. tabaci populations showed very low to low level of resistance (2.1–12.3 fold) to deltamethrin. All B. tabaci populations showed no resistance to very low level of resistance to thiamethoxam (2.2–6.2 fold) and pyriproxyfen (2.4–3.5 fold). A likelihood analysis showed the possibility for control failure in two populations (Barka and Salalah) to deltamethrin, however, no possible failure was detected in all populations for thiamethoxam and pyriproxyfen. An insecticide resistance dynamics study in one population (SQU-1) showed a loss in susceptibility to deltamethrin with increase in the LC₅₀ value from 25.1 mg L⁻¹ to 84.5 mg L⁻¹ between 2017 and 2019 resulting in 5.3 fold increase in RF. The study results determined that several B. tabaci populations are at the initial stages of resistance development to deltamethrin and cross-resistance with thiamethoxam and pyriproxyfen. Vegetable farmers in Oman, the Barka and Salalah regions in particular, should be cautious in the repeated use of one class of insecticide alone.     

Insecticide resistance and control failure likelihood of the whitefly Bemisia tabaci (MEAM1; B biotype): a Neotropical scenario

Insecticide resistance is a standing concern for arthropod pest species, which may result in insecticide control failure. Nonetheless, while insecticide resistance has remained a focus of attention for decades, the incurring risk of insecticide control failure has been neglected. The recognition of both problems is paramount for arthropod pest management and particularly so when invasive species notoriously difficult to control and exhibiting frequent cases of insecticide resistance are considered. Such is the case of the putative whitefly species Middle East‐Asia Minor I (MEAM1) (Bemisia tabaci B‐biotype), for which little information is available in the Neotropics. Thus, the likely occurrence and levels of resistance to seven insecticides were surveyed among Brazilian populations of this species. The likelihood of control failure to the five insecticides registered for this species was also determined. Resistance was detected to all insecticides assessed reaching instances of high (i.e. >100×) to very high levels (>1000×) in all of them. Overall efficacy was particularly low (<60%) and the control failure likelihood was high (>25%) and frequent (70%) for the bioinsecticide azadirachtin, followed by spiromesifen and lambda‐cyhalothrin. In contrast, the likelihood of control failure was low for diafenthiuron, and mainly imidacloprid. As cartap and chlorantraniliprole are not used against whiteflies, but are frequently applied on the same host plants, inadvertent selection probably took place leading to high levels of resistance, particularly for the latter. The resistance levels of cartap and chlorantraniliprole correlated with imidacloprid resistance (r > 0.65, P < 0.001), suggesting that the latter use may have somewhat favoured inadvertent selection for resistance to both compounds not used against the whitefly. A further concern is that chlorantraniliprole use in the reported scenario may allow cross selection to cyantraniliprole, a related diamide with recent registration against whiteflies demanding attention in designing resistance management programmes.     

Biotype and insecticide resistance status of Bemisia tabaci populations from Peninsular Malaysia

Bemisia tabaci, a resistance‐prone insect pest, is a cryptic species complex with important invasive biotypes such as B and Q. The biotype and resistance statuses of this pest in Malaysia remain unclear. This study assessed the biotype and resistance status of a number of contemporary populations of B. tabaci based on the mtCO1 marker and the dose‐response method, respectively. The Pahang (PHG) population was labelled as the Q biotype, while the remainder of the populations belonged to the Asia 1 biotype. A very low level of resistance for profenofos, cypermethrin, and imidacloprid was detected for all populations [resistance factor (RF) < 10]. Resistance to diafenthiuron ranged from very low to very high (RF > 100). All populations showed a very low level of resistance against pymetrozine except Q‐type PHG population, which exhibited a very high level of resistance. For most insecticides, the highest level of resistance was detected in the PHG population. The implications of these findings for better management of this noxious pest are discussed.     

Insecticide resistance in Bemisia tabaci from Cyprus

Abstract A comprehensive study on the Bemisia tabaci (biotype B) resistance to neonicotinoid insecticides imidacloprid, acetamiprid and thiamethoxam, and pyrethroid bifenthrin was conducted in Cyprus. The resistance level to eight field‐collected B. tabaci populations was investigated. The activities of enzymes involved in metabolic detoxification and the frequencies of pyrethroid and organophosphates target site resistance mutations were determined. Moderate to high levels of resistance were detected for imidacloprid (resistance factor [RF] 77–392) and thiamethoxam (RF 50–164) while low resistance levels were observed for acetamiprid (RF 7–12). Uniform responses by the Cypriot whiteflies could be observed against all neonicotinoid insecticides. No cross‐resistance between the neonicotinoids was detected as well as no association with the activity of the P450 microsomal oxidases. Only imidacloprid resistance correlated with carboxylesterase activity. Low to extremely high resistance was observed for insecticide bifenthrin (RF 49–1 243) which was associated with the frequency of the resistant allele in the sodium channel gene but not with the activity of the detoxification enzymes. Finally, the F331W mutation in the acetylcholinesterase enzyme ace1 gene was fixed in all B. tabaci populations from Cyprus.     

Morphological variation inBemisia endosymbionts

Summary The ultrastructure of the endosymbionts of several populations of whitefly (Homoptera: Aleyrodidae) was examined using transmission electron microscopy. Consistent differences in morphology and relative number of endosymbionts were observed between species and biotypes of whitefly within the Bemisia taxon.Bemisia argentifolii (=B. tabaci B biotype) individuals from Hawaii, Florida, and Arizona contained two morphological types of microorganisms housed within the mycetocyte cells of immature whiteflies. In contrast, individuals from populations ofB. tabaci A biotype from Arizona and Mexico, andB. tabaci Jatropha biotype from Puerto Rico, consistently contained three distinct morphological types of microorganisms within their mycetocytes. Organisms fromB. tabaci A and Jatropha biotypes differed from each other in the relative frequency of each type of microorganism. These observations suggest that different whitefly biotypes may have variable combinations of micro-fauna, with some possibly unique to each group, and furthers the hypothesis that variation in whitefly endosymbionts may be associated with the development of biotypes.     

Evaluating the potential of the extract of Perilla sp. as a natural insecticide for Bemisia tabaci (Hemiptera: Aleyrodidae) on sweet peppers

The sweetpotato whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae), is a major pest on greenhouse crops including sweet pepper (Capsicum annuum L.), which is one of the leading greenhouse crops in South Korea. Synthetic insecticides, especially the neonicotinoids, have been used to conventionally control this pest. There have been continuous efforts to develop plant‐derived compounds as insecticides, deterrents, and repellents to reduce spraying synthetic insecticides. To develop new plant‐extract insecticides, we investigated the insecticidal effects of Perilla sp. (Perilla frutescens var. crispa) extract on B. tabaci in laboratory conditions. The Perilla sp. extract induced 90 % mortality within one hour, but phytotoxicity symptoms on sweet pepper leaves were also observed. We monitored the population change and spatial distribution of adult B. tabaci in an experimental sweet pepper greenhouse using yellow sticky traps, and analyzed distribution patterns by spatial analysis with distance indices (SADIE). Based on monitoring data and SADIE analysis, we concluded that B. tabaci aggregated near the greenhouse entrances, and it showed aggregation and association pattern as time passed. Therefore, we recommend spraying Perilla sp. extract near the entrances or wild host before the pest population penetrates. It will be one of the alternative pest management strategies to reduce B. tabaci population with fewer negative effects from chemical insecticide. Further study is required to reduce the phytotoxicity symptoms from Perilla sp. extract spray and insecticidal effect should be evaluated under field conditions.     

Sweetpotato whitefly resistance to insecticides in Hawaii: Intra-island variation is related to insecticide use

Susceptibility to acephate, methomyl, and permethrin was determined with laboratory bioassays of field-collected adults from 15 populations of the B biotype of sweetpotato whitefly,Bemisia tabaci (Gennadius) (Homoptera:Aleyrodidae), from Hawaii. Comparisons at the LC₅₀ showed up to 24-fold resistance to acephate, 18-fold resistance to methomyl, and 4-fold resistance to permethrin. Analysis of variance showed significant intra-island variation in susceptibility to each insecticide, but no significant variation among islands. Insecticide use varied from 4 to 103 insecticide sprays per site per season. Acephate and methomyl were used more often than permethrin. The frequency of application and LC₅₀ for each insecticide were positively correlated across sites. These results suggest that local variation in insecticide use was a primary cause of variation in susceptibility. If local insecticide use is a key determinant of resistance, as our results suggest, growers can retard resistance development locally by reducing their own insecticide use.     

Performance on different host plants of an alien and an indigenous Bemisia tabaci from China

The capacity of the Middle East‐Asia Minor 1 putative species of the whitefly Bemisia tabaci (Gennadius) species complex, commonly referred to as the ‘B biotype’, to invade has often been linked to its presumed wider host range than the indigenous competitors. To determine whether this alien putative species and the indigenous Asia II 1 whitefly putative species, commonly referred to as the ‘ZHJ2 biotype’, differ in their ability to use different host plants, we compared their development, survival and reproduction on eight crop species/cultivars that are commonly cultivated in Zhejiang, China. Of the eight host plants tested, B performed substantially better than ZHJ2 on squash, tomato and tobacco, B and ZHJ2 preformed equally well on cotton and sweet potato, while ZHJ2 performed better than B on kidney bean and pepper. These results indicate that while B generally has a wider host range than many indigenous B. tabaci, an indigenous B. tabaci can perform as well as or better on some host plants. These results combined with the cropping patterns in Zhejiang suggested that the differential capacity to use various host plants between whitefly species is important in mediating the process of invasion by an alien whitefly species.     

Records of Natural Enemies of Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) Biotype B in Brazil

Collections of natural enemies of Bemisia tabaci biotype B (Genn.) (Hemiptera: Aleyrodidae) were made in Lavras, state of Minas Gerais, Brazil. In the greenhouse, 6,495 predators and 16,628 parasitoids belonging to three families were collected. In the field, 267 predators and 344 parasitoids belonging to five families were found. For the first time in Brazil, five species of predators associated with this whitefly were reported. Because of the diversity of natural enemies of B. tabaci biotype B recorded, this study points out the importance of these data for studies on integrated pest management.     

Trap catches of the sweetpotato whitefly （Homoptera： Aleyrodidae） in the Imperial Valley, California, from 1996 to 2002

An outbreak of the sweetpotato whitefly, Bemisia tabaci （Gennadius）, biotype B occurred in the Imperial Valley, California in 1991. The insects destroyed melon crops and seriously damaged other vegetables, ornamentals and row crops. As a result of the need for sampling technology, we developed a whitefly trap （named the CC trap） that could be left in the field for extended time periods. We used the traps to monitor populations ofB. tabaci adults during year-round samplings from 1996 to 2002 to study variations in the weekly trap catches of the insect. The greatest number ofB. tabaci adults was recorded in 1996, followed by a continuing annual decrease in trap catches each year through 2002. The overall decline of B. tabaci is attributed in part to the adoption of an integrated pest management （IPM） program initiated in 1992 and reduced melon hectares from 1996 to 2002. Other factors may also have contributed to the population reductions. Seasonally, B. tabaci trap catches decreased during the late summer and fall concurrent with decreasing minimum tempera- tares that are suggested to be a significant factor affecting seasonal activity and reproduction.     

The integrated use of chemical insecticides and the entomopathogenic nematode,Steinernema carpocapsae (Nematoda: Steinernematidae), for the control of sweetpotato whitefly,Bemisia tabaci (Hemiptera: Aleyrodidae)

The integration of chemical insecticides and infective juveniles of the entomopathogenic nematode Steinernema carpocapsae (Wesier) (Nematoda: Steinernematidae), to control second instars of the sweetpotato whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) was investigated. Using a sand bioassay, the effects of direct exposure of S. carpocapsae for 24 h to field rate dilutions of four insecticides (spiromesifen, thiacloprid, imidacloprid and pymetrozine) on infectivity to Galleria mellonella larvae were tested. Although all chemicals tested, except spiromesifen, produced acceptable nematode infectivity rates, they were all significantly less than the water control. The effect of insecticide treatment (dry residues of spiromesifen, thiacloprid and pymetrozine and soil drench of imidacloprid) on the efficacy of the nematode against B. tabaci was also investigated. Nematodes in combination with thiacloprid and spiromesifen gave higher B. tabaci mortality (86.5% and 94.3% respectively) compared to using nematodes alone (75.2%) on tomato plants. There was no significant difference in B. tabaci mortality when using the chemicals imidacloprid, pymetrozine and spiromesifen in conjunction with nematodes compared to using the chemicals alone. However, using thiacloprid in combination with the nematodes produced significantly higher B. tabaci mortality than using the chemical alone. The integration of S. carpocapsae and these chemical agents into current integrated pest management programmes for the control of B. tabaci is discussed.     

Population genetic structure of the newly invasive Q biotype of Bemisia tabaci in Taiwan

The sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is among the top 100 invasive pests in the world, and it causes serious agricultural damage and economic losses in many countries. More than 24 biotypes of the sweetpotato whitefly have been detected worldwide, of which the Q biotype has recently been reported to be a new invasive pest spreading throughout the world via trade in poinsettias, Euphorbia pulcherrima Willd. ex Klotzsch (Euphorbiaceae). In 2006, the Q biotype was first recorded in Taiwan in greenhouses, but not in the field, suggesting that the invasion of this biotype might be at an early stage in that country. The mitochondrial cytochrome oxidase I (COI) gene and 12 microsatellite loci were used to investigate the genetic structure of multiple B. tabaci Q biotype populations. The presence of only a few COI haplotypes and a low number of nucleotide differences suggest high genetic similarity among these populations. Microsatellite analyses also revealed low genetic differentiation and frequent gene flow among greenhouses. The molecular evidence supports the occurrence of a recent genetic bottleneck in the B. tabaci Q biotype. Bayesian cluster analyses indicated that at least two invasion events have occurred in Taiwan. Phylogenetic analyses of microsatellites support Q biotype migration among greenhouses, which was likely facilitated by the frequent movement of poinsettias between greenhouses. Future management strategies should focus on developing plantlet trade regulations to avoid further anthropogenic dispersal of the B. tabaci Q biotype among greenhouses in Taiwan.     

Can insecticide mixtures be considered to surmount neonicotinoid resistance in Bemisia tabaci?

Cotton whitefly, Bemisia tabaci is an important polyphagous pest worldwide. It is exposed to various chemical insecticides throughout the year, resulting in the rapid development of insecticide resistance. Mixtures of insecticides with distinct modes of action could enhance the toxicity of chemicals more effectively than sequences or rotations in resistant pest populations. Bioassays were conducted to study the efficacy of mixtures of neonicotinoid and ketoenol insecticides at different ratios against a laboratory susceptible (Lab-WB) and a neonicotinoid resistant (TMX-SEL) strain of B. tabaci Asia I. The results showed that mixtures of imidacloprid, acetamiprid, thiamethoxam or dinotefuran with spiromesifen at 1:1, 1:10 and 1:20 ratios and of imidacloprid, thiamethoxam or dinotefuran with spirotetramat at 1:1 ratio significantly increased (p < 0.05) toxicity to neonicotinoids in TMX-SEL strain. The combination indices of each tested neonicotinoids + ketoenols at 1:1 ratio and of acetamiprid + spiromesifen, and imidacloprid or dinotefuran + spirotetramat at 1:10 ratio for TMX-SEL strain were significantly below 1, suggesting synergistic interactions. The inhibitors PBO and DEF largely overcame resistance to the tested neonicotinoids, while none of the synergists significantly restored the susceptibility of B. tabaci to ketoenols. Increased activities of P450 monooxygenase and esterase were observed in TMX-SEL strain with an elevated 2.76 and 1.32-fold, respectively. Mixtures of neonicotinoids with spiromesifen or spirotetramat at a 1:1 ratio could be used to restore the neonicotinoid susceptibility in B. tabaci.     

Thermotolerance and gene expression following heat stress in the whitefly Bemisia tabaci B and Q biotypes

The whitefly Bemisia tabaci (Gennadius) causes tremendous losses to agriculture by direct feeding on plants and by vectoring several families of plant viruses. The B. tabaci species complex comprises over 10 genetic groups (biotypes) that are well defined by DNA markers and biological characteristics. B and Q are amongst the most dominant and damaging biotypes, differing considerably in fecundity, host range, insecticide resistance, virus vectoriality, and the symbiotic bacteria they harbor. We used a spotted B. tabaci cDNA microarray to compare the expression patterns of 6000 ESTs of B and Q biotypes under standard 25 °C regime and heat stress at 40 °C. Overall, the number of genes affected by increasing temperature in the two biotypes was similar. Gene expression under 25 °C normal rearing temperature showed clear differences between the two biotypes: B exhibited higher expression of mitochondrial genes, and lower cytoskeleton, heat-shock and stress-related genes, compared to Q. Exposing B biotype whiteflies to heat stress was accompanied by rapid alteration of gene expression. For the first time, the results here present differences in gene expression between very closely related and sympatric B. tabaci biotypes, and suggest that these clear-cut differences are due to better adaptation of one biotype over another and might eventually lead to changes in the local and global distribution of both biotypes.     

Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests

Identifying molecular mechanisms of insecticide resistance is important for preserving insecticide efficacy, developing new insecticides and implementing insect control. The metabolic detoxification of insecticides is a widespread resistance mechanism. Enzymes with the potential to detoxify insecticides are commonly encoded by members of the large cytochrome P450, glutathione S-transferase and carboxylesterase gene families, all rapidly evolving in insects. Here, we demonstrate that the model insect Drosophila melanogaster is useful for functionally validating the role of metabolic enzymes in conferring metabolism-based insecticide resistance. Alleles of three well-characterized genes from different pest insects were expressed in transgenic D. melanogaster : a carboxylesterase gene (αE7) from the Australian sheep blowfly Lucilia cuprina, a glutathione S-transferase gene (GstE2) from the mosquito Anopheles gambiae and a cytochrome P450 gene (Cyp6cm1) from the whitefly Bemisia tabaci. For all genes, expression in D. melanogaster resulted in insecticide resistance phenotypes mirroring those observed in resistant populations of the pest species. Using D. melanogaster to assess the potential for novel metabolic resistance mechanisms to evolve in pest species is discussed.     

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.     

Comparison of performance on different host plants between the B biotype and a non-B biotype of Bemisia tabaci from Zhejiang, China

The capacity of the B biotype of the whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), to invade has often been linked to its presumably wider host range than the non‐B indigenous biotypes. However, there are few experimental studies of the relative performance of the B biotype and non‐B biotypes on different host‐plant species. Here, we compared the performance of the B biotype and an indigenous non‐B biotype (China‐ZHJ‐1) of B. tabaci from Zhejiang, China on five commonly cultivated host plants, each from a different family: cotton, tobacco, cabbage, squash, and kidney bean. We also examined the effect of rearing host plants on the performance of the B biotype. Overall, the performance of the B biotype on the five species of plants was much better than that of the indigenous non‐B population. On tobacco, cabbage, and kidney bean, no individuals of ZHJ‐1 completed development to adulthood, whereas the B biotype developed successfully from egg to adult on all three plants. On squash, the B biotype survived better, developed to adulthood earlier and had a higher fecundity than ZHJ‐1. The two biotypes performed more equally on cotton, but even on this plant the B biotype female adults lived nearly twice as long as that of ZHJ‐1 and may have realized a higher life‐time fecundity. The B biotype also showed a substantial capacity to acclimatize to alternative host plants for improved survival and reproduction, on both highly suitable and marginally suitable host plants. We conclude that the host range of the B biotype of B. tabaci may be much wider than those of some indigenous biotypes, and this advantage of the B biotype over the non‐B biotypes may assist in its invasion and displacement of some indigenous biotypes in the field.