Chromosome‐level genome assembly of the greenhouse whitefly (Trialeurodes vaporariorum Westwood)

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is an agricultural pest of global importance. Here we report a 787‐Mb high‐quality draft genome sequence of T. vaporariorum assembled from PacBio long reads and Hi‐C chromatin interaction maps, which has scaffold and contig N50 lengths of 70 Mb and 500 kb, respectively, and contains 18,275 protein‐coding genes. About 98.8% of the assembled contigs were placed onto the 11 T. vaporariorum chromosomes. Comparative genomic analysis reveals significantly expanded gene families such as aspartyl proteases in T. vaporariorum compared to Bemisia tabaci Mediterranean (MED) and Middle East‐Asia Minor 1 (MEAM1). Furthermore, the cytochrome CYP6 subfamily shows significant expansion in T. vaporariorum and several genes in this subfamily display developmental stage‐specific expression patterns. The high‐quality T. vaporariorum genome provides a valuable resource for research in a broad range of areas such as fundamental molecular ecology, insect–plant/insect–microorganism or virus interactions and pest resistance management.     

Life history of Amitus fuscipennis (Hym., Platygastridae) as parasitoid of the greenhouse whitefly Trialeurodes vaporariorum (Hom., Aleyrodidae) on tomato as function of temperature

Life history parameters of Amitus fuscipennis MacGown and Nebeker as parasitoid of Trialeurodes vaporariorum (Westwood) were determined at 15, 20, 25 and 30°C on tomato using three different methods. For each method, immature development, mortality, longevity, fecundity, oviposition frequency and post-oviposition period were determined and temperature-dependent relations were estimated. Oviposition frequency was also estimated as a function of parasitoid age. Immature development had a maximum of 61 days at 15°C that decreased to 22 days at 30°C. Mortality in the grey stage was less than 2% at temperatures lower than 30°C, where it was 60%. Longevity fluctuated between 3 and 18 days. Fecundity increased from 338 eggs/female at 15°C to a maximum of 430 eggs/female at 25°C and then decreased to 119 eggs/female at 30°C. Oviposition frequency varied between 3 and 46 eggs/female per day and had its maximum on the first day after emergence of the parasitoid. Net reproduction rate, generation time and intrinsic rate of increase were calculated. The intrinsic rate of increase increased from 0.090 at 15°C to a maximum of 0.233 at 25°C and then decreased to 0.159 at 30°C. The influence of the methods to determine the life history parameters on the results is discussed. The results are compared also with the life history of Encarsia formosa Gahan (Hym., Aphelinidae) a parasitoid of the same host. The advantages and disadvantages of the pro-ovigenic A. fuscipennis in comparison with the synovigenic E. formosa are discussed.     

Impacts of two conventional insecticides on different stages of Encarsia inaron Walker parasitizing the whitefly,Trialeurodes vaporariorum Westwood under greenhouse condition

In this research, for the first time, compatibility of imidacloprid and pyriproxyfen was assayed with both pupa and adult stages of Encarsia inaron Walker parasitizing Trialeurodes vaporariorum Westwood. First, the insecticides were sprayed on bean plants containing the parasitoid pupae, thenceforth, survival of the adult parasitoid was evaluated 24 h post-exposure to fresh, 1-, 4-, 7-, 14-, and 21-day-old residues of them on bean leaflets in Petri dishes. Both insecticides significantly reduce E. inaron adult emergence. Mortality of the parasitoid pupa in treatment with imidacloprid (69.7%) was significantly higher than mortality with pyriproxyfen (28.6%). Pyriproxyfen was non-toxic to the adult parasitoid when residues were dried in fresh and aged through the experiment, while in the same condition, imidacloprid significantly killed the adult parasitoids up to 7 days after application. Results have been discussed on the potential compatibility of the insecticides with E. inaron in an integrated pest management (IPM) approach.     

Resistance of tomato genotypes to the greenhouse whitefly Trialeurodes vaporariorum (West.) (Hemiptera: Aleyrodidae)

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is the most common and abundant whitefly in Argentine horticultural greenhouse crops, especially in tomato (Solanum lycopersicum). Resistance in some wild tomato relatives, such as S. peruvianum, S. habrochaites and S. pennellii to the greenhouse whitefly has been described. The Mi gene confers effective resistance against several species of insects, among them the sweet potato whitefly, Bemisia tabaci Gennadius. Resistance to T. vaporariorum was found in the prebreeding line FCN 93-6-2, derived from a cross between S. lycopersicum cultivar Uco Plata INTA (MiMi) and the wild line FCN 3-5 S. habrochaites. The purpose of this study was to evaluate resistance to T. vaporariorum in tomato genotypes and to study the relationship between this resistance and the presence of the REX-1 marker, which is linked to the Mi gene. In a free-choice assay, the average number of adults per leaf and the number of immatures on the middle and basal plant parts were analyzed. In a no-choice assay, the oviposition rate and adult survival rate were calculated. For all variables analyzed, FCN 3-5 was the most resistant strain. Variations were found in the F2 progeny between the prebreeding line FCN 13-1-6-1 and cv. Uco Plata INTA. Results from the F2 progeny indicate that resistance to T. vaporariorum may be polygenic with transgressive segregation. Whitefly resistance was found to be independent of the REX-1 marker.     

Dispersal of the broad mite,Polyphagotarsonemus latus (Banks) (Heterostigmata: Tarsonemidae), by the greenhouse whitefly,Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae)

The greenhouse whitefly, Trialeurodes vaporariorum (Westwood), (Homoptera: Aleyrodidae) was found to disperse the broad mite, Polyphagotarsonemus latus (Banks) (Heterostigmata: Tarsonemidae). Mite presence on whiteflies was highly aggregated. This is the second whitefly species reported to disperse the broad mite, suggesting some recognition of the insects by P. latus.     

Phototactic behavior of Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae) under visible wavelengths

The greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), is one of the most important pests of greenhouse crops. The intensive use of chemical insecticides has resulted in insecticide resistance in T. vaporariorum and the critical level of pesticides residue in crops. It is therefore necessary to develop new control methods based on ecological pest management. The present study was designed to control greenhouse whitefly by finding and using insect repellent wavelengths. The repellent wavelength experiment was conducted by a two-way phototactic apparatus given a choice between darkness and visible wavelength spectrum from violet (380–450 nm) to red (620–750 nm). The phototactic responses of the greenhouse whitefly were then investigated in a four-way phototactic apparatus given a choice between two light regimes, light-emitting diode (LED) and sunlight. The results indicated that the lowest (69.2%) and highest (97.8%) number of whiteflies were attracted to violet and orange (590–625 nm) spectra, respectively. In addition, the present study indicated a significant attraction of T. vaporariorum adults to sunlight compared with LED. Furthermore, the eggplants grown under growth LEDs showed a significantly higher growth rate than the plants grown under sunlight. These findings suggest that this type of LED not only has positive effects on plant growth but it also has a repellent activity on T. vaporariorum adults, leading us to develop an effective behavioral control of the greenhouse whitefly.     

A model of greenhouse whitefly Trialeurodes vaporariorum (Westwood) population development and management on Camarosa variety strawberry plants

A deterministic parameterized model of development of a greenhouse whitefly (Trialeurodes vaporariorum) population on field grown strawberry plants (Fragaria × ananassa) is presented (var. Camarosa). The model calculates the timing of the physiological development of individual whiteflies and population size as a function of temperature, mortality, oviposition, and plant condition using parameters from the literature and field observations from California. Simulated dynamics of a T. vaporariorum population accurately reflected the observed population development in an untreated strawberry field, and its response to applications of pyriproxyfen and imidacloprid under production conditions in central coastal California. It was validated with an independent field observation where both imidacloprid and pyriproxyfen were applied at different periods of strawberry plant development. These results present an opportunity to predict effects of management strategies targeting T. vaporariorum populations on variety Camarosa strawberry plants.     

Seasonal population dynamics of the greenhouse whitefly Trialeurodes vaporariorum (Homoptera: Aleyrodidae) on strawberries in Southern California

The greenhouse whitefly, Trialeurodes vaporariorum (Westwood), has recently become a major insect pest of strawberries in Southern California. The population dynamics of this pest were monitored over 2 yr in six commercial strawberry fields near the coastal communities of Oxnard and Ventura under two crop-production regimes, summer- and fall-planted strawberries. Adult whitefly numbers generally peaked during the February through May period for fall-planted strawberries and during the October through November period for summer-planted strawberries. Population densities varied greatly among fields within each regime and the differences were likely caused by surrounding alternate host crops.     

温室白粉虱对几种园艺植物的偏好性

温室白粉虱Trialeurodesvaporariorum是世界性害虫,每年都造成巨大的经济损失。研究了温室白粉虱在多种园艺植物混栽温室内对不同植物的选择性,结果表明在2 0种常见蔬菜和花卉中,可危害其中1 3种;温室白粉虱对其中6种寄主植物(旱金莲、一品红、菊花、番茄、小白菜和羽叶甘蓝)的选择性有显著差异,其种群数量为旱金莲和番茄显著多于小白菜、一品红和菊花,羽叶甘蓝显著少于其它5种植物;不同的虫态之间排序有小变动;温室白粉虱在番茄植株上部的垂直分布表现为卵和成虫在第3叶居多,若虫在第5叶居多,伪蛹在第9叶居多。     

Incidence of resistance to neonicotinoid insecticides in greenhouse populations of the whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) from Greece

The greenhouse whitefly, Trialeurodes vaporariorum Westwood, is an important pest of field and greenhouse crops of horticultural and ornamental plants. In integrated pest management programs its control is mainly based on the release of biological control agents and application of chemical insecticides. Neonicotinoids are relatively new chemicals currently applied for the chemical control of T. vaporariorum. However, cases of development of insecticide resistance to neonicotinoids have already been reported. The state of resistance to neonicotinoid insecticides for populations of the greenhouse whitefly in Greece is currently unknown. The objective of our study was to screen a number of whitefly populations for resistance to the neonicotinoids imidacloprid and thiacloprid. Seven whitefly populations were collected from tomato greenhouse crops from different areas of central and northern Greece. LC₅₀ values were estimated for all populations following the method proposed by the Insecticide Resistance Action Committee (IRAC). The development of resistance to both neonicotinoids was confirmed for all tested populations with resistance ratios ranging from 1.5 to 4.4-fold and from 1.4 to 12.2-fold for imidacloprid and thiacloprid, respectively. We discuss our results with regard to the development of neonicotinoid resistance in T. vaporariorum populations and its implications for whitefly control.     

Spatial distribution of greenhouse whitefly (Trialeurodes vaporariorum Westwood) and a suggested sampling plan for estimating its density in greenhouses

Spatial distribution of the greenhouse whitefly population infesting tomato plants in greenhouses was analyzed. A leaf of tomato consists of 7 leaflets, each being used as a basic sampling unit. Distribution patterns between plants, between leaves and between leaflets were analyzed by the analysis of variance and the method. It was found that populations of all the developmental stages were composed of contagiously distributed colonies or individuals between leaves and between leaflets. On the other hand, they showed random distribution of colonies between plants. On leaflets, egg populations were distributed as colonies, each consisting of several eggs, while in larval and adult populations, individuals were distributed rather independently of each other. A three-stage sampling plan was developed to estimate the density at the assigned level of precision.     

Effect of lemon essential oil on the developmental stages of Trialeurodes vaporariorum West (Homoptera: Aleyrodidae)

Trialeurodes vaporariorum (Homoptera: Aleyrodidae), is a destructive pest of many ornamental and greenhouse crops throughout the world. In this research, effect of essential oil derived from lemon peel, Citrus aurantifolia (Hook.) on mortality of eggs, first-instar nymphs and on adult oviposition of T. vaporariorum (Westwood) was determined under laboratory conditions. Analysis of Citrus aurantifolia essential oil used for insect fumigation by phase gas chromatography revealed the presence of 16 compounds including Limonene (56.6%), β-pinene (16.3%) and α-terpineol (11.3%). Five concentrations of essential oil – 0.002, 0.004, 0.008, 0.016 and 0.032 (μl/ml) – were applied in fumigant toxicity experiments. Greater mortality was observed with increasing dose of essential oil. First-instar nymphs were more sensitive to essential oil treatments compared with eggs and adults that reduced the survival rate of T. vaporariorum by 58, 70 and 56% after treatment of eggs, nymphs and adult, respectively. Based on this study, essential oil derived from C. aurantifolia could be used as an effective and environmentally sustainable bioinsecticide for the control of T. vaporariorum.     

Toxicity of abamectin and imidacloprid on different life stages of Trialeurodes vaporariorum (Westwood) reared on two different host plants under greenhouse conditions

Chemical application is the common control technique of the pest Trialeurodes vaporariorum (Westwood) (Hom.: Aleyrodidae). Toxicity of two insecticides abamectin and imidacloprid in 2009 was evaluated on different life stages of the pest. Bioassay tests were carried out under controlled environmental conditions (25?±?2?°C 50?±?5% RH and a photoperiod of 18:6 L/D) on different stages of whitefly (1-,3- and 5-day-old ages of eggs, first, second and third nymphal instars, pupa and adult). Both insecticides showed their best efficacy on the primary stages; though, with increasing the age, the susceptibility of all stages to chemicals was decreased. It was shown that sensitivity of eggs and first nymphal stage to abamectin in each host was different. But in imidacloprid treatment, only the eggs showed different sensitivity on both host plants. It seems that application of abamectin in primary stages induce higher mortality rates than of imidacloprid.     

Growth and development of Encarsia formosa (Hymenoptera: Aphelinidae) in the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae): effect of host age

The tiny parasitoid wasp, Encarsia formosa, has been used successfully to control greenhouse whiteflies (GHWFs) in greenhouses in many countries throughout the world. Therefore, there has been considerable interest in developing methods for artificially rearing this wasp. However, little information is available concerning the regulation of its development including the host-parasitoid interactions that are required for the parasitoid to complete its life cycle. Here we confirm that parasitoid developmental rates differ significantly based upon the host instar parasitized. Development was faster when 3rd and 4th instar GHWFs were offered for parasitization than when 1st or 2nd instars were used. Our results show that it is primarily the embryo and the first two parasitoid instars that exhibit prolonged developmental times when 1st and 2nd instar whiteflies are parasitized. Although percent emergence was not affected by host age at the time of parasitization, adult longevity as well as adult emergence pattern varied greatly depending upon the instar parasitized. When 3rd and 4th instar GHWFs were selected for oviposition, adult wasps lived significantly longer than when 1st or 2nd instars were used; also, there was a sharp emergence peak on the 2nd day after emergence was first observed (reduced or absent when 1st or 2nd instar GHWFs were parasitized) and the emergence period was reduced from between 8 and 11 days to 5 days. In general, the younger the host instar parasitized, the less synchronous was parasitoid development. Previous reports that E. formosa will not molt to the 2nd instar until the host has reached its 4th instar were not confirmed. When 1st instar host nymphs were parasitized, 2nd instar parasitoids were detected in 3rd instar hosts. Importantly, however, no matter which instar was parasitized, the parasitoid never molted to its last instar until the host had reached Stage 5 of its last instar, a stage in which host pharate adult formation has been initiated. It appears, then, that a condition(s) associated with host pharate adult formation is required for the parasitoid's final larval molt. Results reported here should facilitate the development of in vitro rearing systems for E. formosa.     

Induction of metabolite organic compounds by mutualistic endophytic fungi to reduce the greenhouse whitefly Trialeurodes vaporariorum (Westwood) infection on tomato

Background and aims

Six mutualistic endophytic fungi that are known to colonize the endorhiza have shown biological control properties against plant-parasitic nematodes. In this study we aim to investigate the potential of these endophytic fungi to reduce the phloem-feeding insect Trialeurodes vaporariorum (Westwood) on tomato.

Methods

To determine the host plant choice of T. vaporariorum, the total number of insects present on each plant was counted daily for 10 days, and then the second leaf below the shoot apex were examined for its chlorophyll content index (CCI).To separate and quantify the active compounds produced in the tomato leaves, a reversed phase high liquid chromatography (RP-HPLC) analysis was performed.

Principle results

A greenhouse choice test showed that Trichoderma atroviride strain MT-20, T. atroviride strain S-2 and Fusarium oxysporum strain 162 (Fo162) reduced the number of greenhouse whiteflies fifty percent when compared to the untreated control during ten days after insect release. The highest level of biocontrol activity was attained with Fo162. The strains MT20, S-2, and Fo162 all demonstrated acropedal induction of resistance to the insects. The isolate Fusarium sp. strain Bonn-7 enhanced plant growth. The negative effect on insect attraction to the leaves of the endophyte treated plants was not associated with leaf altered chlorophyll content. RP-HPLC analysis revealed that inoculation of the fungus Fo162 induced a change in the accumulation of specific organic compounds in the tomato leaves that could be the cause of insect repellence.

Conclusions

This study demonstrated the high potential of mutualintic endophytic fungi, in particular of Fo162, to induce resistance in tomato against the phloemfeeding T. vaporariorum.     

B型烟粉虱与温室白粉虱不同虫态的碱性磷酸酶性质比较

为了探明B型烟粉虱Bemisia tabaci B-biotype 和温室白粉虱Trialeurodes vaporariorum体内的碱性磷酸酶(alkaline phosphatase,ALP)在两者竞争替代中所起的作用,以对硝基苯磷酸二钠 (pNPP)为底物,采用个体测定和群体测定的方法,研究比较了2种粉虱不同虫态中该酶的性质。结果表明：2种粉虱的碱性磷酸酶比活力在整个发育历期均逐渐增加,成虫期达到最大。温室白粉虱2至4龄若虫（伪蛹）期的碱性磷酸酶比活力分别是B型烟粉虱对应龄期酶比活力的2.58、2.68和3.14倍; B型烟粉虱雌雄成虫的碱性磷酸酶比活力分别是温室白粉虱雌雄成虫酶比活力的1.24和1.26倍,且2种粉虱雌虫的酶比活力显著大于其雄虫。2种粉虱2龄若虫到成虫的碱性磷酸酶最适pH均为7.8,最适温度均为47℃;在1龄若虫中均未能检测到该酶活性。测定并比较2种粉虱不同虫态碱性磷酸酶动力学特征参数的结果显示,温室白粉虱碱性磷酸酶在3、4龄若虫的亲和力以及在2, 3, 4龄若虫的酶蛋白浓度均显著大于B型烟粉虱的对应值,而在成虫期2种粉虱的亲和力、酶蛋白浓度无差异,B型烟粉虱的活化能显著小于温室白粉虱。据此推测,B型烟粉虱利用碱性磷酸酶在若虫期进行组织骨化和生长发育不如温室白粉虱,但羽化为成虫后利用其进行解毒代谢则可能强于温室白粉虱。     

Laboratory and field evaluation of biological active substances of plant origin against greenhouse whitefly,Trialeurodes vaporariorum Westw. (Homoptera: Aleyrodidae)

Abstract

The behavioural responses of greenhouse whitefly to substances of plant origin were investigated in laboratory and greenhouse conditions. The following species of plants were found to provide the most active chemicals to monitor and control greenhouse whitefly – laurel Laurus nobilis L., mullein Verbascum thapsus L., tansy Tanacetum vulgare L., wormwood Artemisia vulgare L.     

Light emitting diode(LED)‐based trapping of the greenhouse whitefly (Trialeurodes vaporariorum)

Visual traps like yellow sticky card traps are used for monitoring and control of the greenhouse whitefly (Trialeurodes vaporariorum). However, reflected intensity (brightness) and hence, attractiveness depend on the ambient light conditions, and the colour (wavelength) might not fit with the sensitivity of whitefly photoreceptors. The use of light emitting diodes (LEDs) is a promising approach to increase the attractiveness, specificity and adaptability of visual traps. We constructed LED‐based visual traps equipped with blue and green high‐power LEDs and ultraviolet (UV) standard LEDs according to the putative spectral sensitivities of the insects' photoreceptors. In a series of small‐scale choice and no‐choice recapture experiments, the factors time of day as well as light intensity and light quality (colour) of LED traps were studied in terms of attractiveness compared to yellow traps without LEDs. Green LED traps (517 nm peak wavelength) were comparably attractive in no‐choice experiments but clearly preferred over yellow traps in all choice experiments. The time of day had a clear effect on the flight activity of the whiteflies and thereby on the trapping success. Blue LEDs (474 nm) suppressed the attractiveness of the light traps when combined with green LEDs suggesting that a yet undetected photoreceptor, sensitive for blue light, and an inhibiting interaction with the green receptor, might exist in T. vaporariorum. In choice experiments between LED traps emitting green light only or in combination with UV (368 nm), the green‐UV combination was preferred. In no‐choice night‐time experiments, UV LEDs considerably increased whitefly flight activity and efficacy of trapping. Most likely, the reason for the modifying effect of UV is the stimulating influence on flight activity. In conclusion, it seems that the use of green LEDs alone or in combination with UV LEDs could be an innovative option for improving attractiveness of visual traps.