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.     

A simulation study of population interaction between the greenhouse whitefly,Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae), and the parasitoidEncarsia formosa gahan (Hymenoptera: Aphelinidae) I. Description of the model

A simple simulation model was developed to simulate the population dynamics of the system of the greenhouse whitefly (Trialeurodes vaporariorumWestwood ) and the parasitoid Encarsia formosaGahan . On the assumption that temperature is constant, the whitefly population was described as theLeslie Matrix model. Parasitization and host feeding by the parasitoid population were modelled by means of a modified disc equation. The validity of the model was demonstrated by comparing the predictions of the model with the observed values obtained in greenhouse experiments.     

Fitness of Encarsia sophia (Hymenoptera: Aphelinidae) parasitizing Trialeurodes vaporariorum and Bemisia tabaci (Hemiptera: Aleyrodidae)

Abstract Fitness and efficacy of Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae) as a biological control agent was compared on two species of whitefly (Hemiptera: Aleyrodidae) hosts, the relatively smaller sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype ‘B’, and the larger greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Significant differences were observed on green bean (Phaseolus vulgaris L.) in the laboratory at 27 ± 2°C, 55%± 5% RH, and a photoperiod of 14: 10 h (L: D). Adult parasitoids emerging from T. vaporariorum were larger than those emerging from B. tabaci, and almost all biological parameters of E. sophia parasitizing the larger host species were superior except for the developmental times of the parasitoids that were similar when parasitizing the two host species. Furthermore, parasitoids emerging from T. vaporariorum parasitized more of these hosts than did parasitoids emerging from B. tabaci. We conclude that E. sophia reared from larger hosts had better fitness than from smaller hosts. Those from either host also preferred the larger host for oviposition but were just as effective on smaller hosts. Therefore, larger hosts tended to produce better parasitoids than smaller hosts.     

Morphological and biological notes on Encarsia meritoria Gahan (Hymenoptera,Aphelinidae), a parasitoid of Trialeurodes vaporariorum (Westwood) (Homoptera,Aleyrodidae) new in Europe

Encarsia meritoria Gahan, a Neartic species recorded only in the USA, was found naturally occurring in Catalonia (north‐east Spain) in 1987. The morphology of immature stages, the rate of development in the range 12°C‐34°C, the longevity and fecundity at 24°C and some observations on its searching and host feeding behaviour are presented in this paper. Mean development times from egg laying to adult emergence ranged from 75 days at 12° C to 11 days at 28°C. The Lower Developmental Threshold computed from linear regression equations was 9°C. Females laid an average of 198 eggs (range 89–330) in an average of 34 days (longevity range 19–54 days). The intrinsic rate of increase at 24° C was 0.1717, slightly greater than the r_m of T. vaporariorum and smaller than the values reported for E. tricolor and E. formosa, which is not very promising for biological control. However, this may not be a definitive conclusion, because factors other than those considered in our experiments may play an important role infield conditions.     

A simulation study of population interaction between the greenhouse whitefly,Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae) and the parasitoidEncarsia formosa Gahan (Hymenoptera: Aphelinidae) II. Simulation analysis of population dynamics and strategy of biological control

Simulation studies were performed to analyze factors affecting the population dynamics of the system with the greenhouse whitefly (Trialeurodes vaporariorumWestwood ) and the parasitoid Encarsia formosaGahan and to develop strategies for the introduction of E. formosa. The reduction of parasitization efficiency with an increase in parasitoid density promotes the stability of the system, which coincides with the prediction from current theory. The stability of the system is also shown to be promoted by the effect of host feeding. The population levels of the system are remarkably suppressed with an increase in searching efficiency and a decrease in host oviposition. The control effect of the parasitoids is enhanced when the number of parasitoids is divided among many introductions. An optimal time, an optimal density ratio of parasitoids to hosts and optimal densities of hosts and parasitoids exist in the introduction programme of parasitoids.     

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.     

Spectral efficiency of the glasshouse whitefly Trialeurodes vaporariorum and Encarsia formosa its hymenopteran parasitoid

Using the electroretinogram (ERG) technique the spectral efficiency of the compound eye of the glasshouse whitefly Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) and its main parasitoid Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae) was measured at selected wavelengths between 340 nm and 670 nm. The form of the ERG for both T. vaporariorum and E. formosa was found to be monophasic in nature. For both male and female T. vaporariorum and female E. formosa a primary peak of efficiency occurred in the blue-green-yellow region, peak 520 nm and a secondary peak in the ultraviolet (UV) region. The compound eye of female E. formosa gave a significantly greater response in the UV region than either the dorsal or ventral regions of the compound eye of T. vaporariorum relative to the responses in the blue-green-yellow region. T. vaporariorum has divided compound eyes with distinct dorsal and ventral regions. In this study it was found that the percentage response in the UV, of the dorsal region of the eye, is significantly greater than that of the ventral region of the eye relative to the percentage response in the blue-green-yellow region and there is a significant shift in the blue-green yellow peak towards the right of the spectrum.     

Phototactic behaviour of the parasitoid Encarsia formosa (Hymenoptera: Aphelinidae)

We investigated the spectral sensitivity and response to light intensity of Encarsia formosa (Hymenoptera: Aphelinidae), which is a key natural enemy of the greenhouse whitefly, Trialeurodes vaporariorum, and the tobacco whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). To do so, we used 15 monochromatic lights (emitting various specific wavelengths from 340 to 649?nm) and white light. E. formosa adults, which are diurnal insects, showed a positive phototaxis to a broad spectrum of light, with peaks of sensitivity at 414, 340, 450, and 504?nm. These results show that this parasitoid is generally more sensitive to short wavelength lights than long wavelength lights across all spectral ranges tested. Furthermore, E. formosa adults showed an increased phototactic response at low intensities and a decreased response at high intensities, for both ultraviolet light and violet light. Thus, E. formosa showed both colour and intensity preferences. This experiment provides a scientific basis for the development of colour traps for insect pest management and improves understanding of the ecological significance of colour vision by E. formosa.     

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.     

两种杀虫真菌制剂与低用量吡虫啉对温室粉虱的协同防效评价

在昆明市郊蔬菜基地4间大棚(5m×100m·间^-1)栽培的生菜上,用球孢白僵菌(Beauveriabassiana)和玫烟色拟青霉(Paecilomyces fumasonoseus)的纯孢子乳悬剂(有效含孢量10^10·ml^-1)及其与1％和3％(w／v)的吡虫啉10％WP的混配剂对温室粉虱(Trialeurodes vaporariorum)进行了协同药效试验,吡虫啉添加量仅相当于推荐用量的6．4％～9．5％和19．1％～28．6％,试验含6个菌剂处理、2个低用量吡虫啉处理和1个清水对照,各有3个小区(7m×5m·小区^-1)重复,随机区组排列,稀释1000倍的菌液(含孢量10^7·ml^-1)和吡虫啉液于生菜移栽后第11d首次喷雾,15d后喷第二次,首次用菌前调查初始粉虱密度,用菌后每隔5d调查活虫数和死虫数,从8月20日起历时30d,结果表明,连续2次用菌有效地控制了粉虱对当季大棚生菜的危害,各菌剂处理的最终相对防效和虫口减退率均达到95％以上,极显著地高于低用量吡虫啉处理,其中,玫烟色拟青霉制剂对粉虱的控制效果一般优于球孢白僵菌制剂,且与吡虫啉的添加量呈正相关,但是,各菌剂处理间控虫效果的差异主要发生在首次用菌后第5d和10d,此后差异逐渐缩小,至第二次用菌后第10d各菌剂处理间无显著差异,本试验结果表明,两种真菌的孢子乳悬剂均可用于温室粉虱的防治,添加微量吡虫啉可增强菌剂的防效。     

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.     

Visual behaviour of the greenhouse whitefly, Trialeurodes vaporariorum

ABSTRACT. The behaviour of Trialeurodes vaporariorum (Westwood) (Homoptera, Aleyrodidae) in violet and green light (400 and 550 nm) was examined using several responses. Under 400 nm the whiteflies took-off more readily and walked faster than under 500 nm. In flight, they oriented towards 400 nm when simultaneously illuminated with equal quanta of 550 and 400 nm light. The ecological significance of this behaviour is discussed, and it is concluded that in nature flying adults would orient towards the sky (i.e. c. 400 nm) but would tend to land on a green plant because plants reflect maximally at 550 nm. Once landed on a suitable food-plant the position on that plant where the insect finally feeds and reproduces is probably also determined by visual stimuli, since whiteflies will walk to the shaded side of a leaf regardless of whether that is below or above.     

Toxicity of plant essential oils to Trialeurodes vaporariorum (Homoptera: Aleyrodidae)

A total of 53 plant essential oils were tested for their insecticidal activities against eggs, nymphs, and adults of Trialeurodes vaporariorum Westwood, using an impregnated filter paper bioassays without allowing direct contact. Responses varied according to oil type and dose, and developmental stage of the insect. Bay, caraway seed, clove leaf, lemon eucalyptus, lime dis 5 F, pennyroyal, peppermint, rosewood, spearmint, and tea tree oils were highly effective against T. vaporariorum adults, nymphs, and eggs at 0.0023, 0.0093, and 0.0047 microl/ml air, respectively. These results indicate that the mode of delivery of these essential oils was largely a result of action in the vapor phase. Significant correlations among adulticidal, nymphicidal, and ovicidal activities of the test oils were observed. The essential oils described herein merit further study as potential fumigants for T. vaporariorum control.     

Interspecific interference competition between Encarsia formosa and Encarsia sophia (Hymenoptera: Aphelinidae) in parasitizing Bemisia tabaci (Hemiptera: Aleyrodidae) on five tomato varieties

Abstract Interspecific competition between Encarsia formosa and Encarsia sophia, two major parasitoids of Bemisia tabaci, and the influence of five tomato varieties on competition outcome were investigated under laboratory conditions. E. formosa parasitized more B. tabaci than E. sophia when in single wasp assays on any of the tomato varieties investigated. When B. tabaci nymphs were exposed to both wasp species (either simultaneously or sequentially), the number of B. tabaci nymphs parasitized by either wasp species was significantly decreased compared to the sole access condition. Total mortality of B. tabaci was increased when B. tabaci nymphs were exposed to both wasp species compared to only one wasp species. Thus competition between E. formosa and E. sophia apparently reduced parasitoid offspring numbers, but not the efficiency of biological control. In fact, control efficiency was enhanced in some cases, particularly on tomato variety Huangtuoyuan (HTY). When wasps were allowed sequential access to hosts, interference occurred through host feeding by the second wasp, especially if it was E. sophia. The effect of different tomato varieties was not significant.     

基于SCAR标记技术的丽蚜小蜂快速识别

丽蚜小蜂Encarsia formosa Gahan作为温室粉虱Trialeurodes vaporariorum Westwood和烟粉虱Bemisia tabaci (Gennadius)等粉虱类害虫的优势寄生蜂而备受关注。针对丽蚜小蜂体型微小, 难以与其他同域近缘种寄生蜂快速、 准确区别的问题, 本研究采用SCAR (sequence characterized amplified region, 特异性扩增区域)标记技术, 筛选出一对丽蚜小蜂特征片段扩增引物(EFZZF/EFZZR), 其扩增片段的大小为287 bp。种特异性检验结果表明, 该对引物只对丽蚜小蜂的基因组DNA具有扩增能力, 对其近缘种属寄生蜂如浅黄恩蚜小蜂Encarsia sophia (Girault & Dodd)、 海氏桨角蚜小蜂Eretmocerus hayati Zolnerowich & Rose、 本地未知种桨角蚜小蜂Eretmocerus sp.、 蒙氏桨角蚜小蜂Eretmocerus mundus Mercet、 刺粉虱黑蜂Amitus hesperidum Silvertri不具有扩增效果, 对丽蚜小蜂的寄主包括不同生物型 (B型、 Q型、 ZHJ 1型和ZHJ 2型)的烟粉虱、 温室粉虱以及我国最常见的黑刺粉虱Aleurocanthus spiniferus (Quaintanca)等亦不具有扩增能力。同时, 该检测技术灵敏度高, 对成虫的最低检出阈值为7.812 ng/μL (相当于1/1 600头成虫)。研究结果对丽蚜小蜂的种类识别、 寄主谱的确定及其有效利用具有重要意义。     

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.     

The differential mortality at various life stages of the greenhouse whitefly,Trialeurodes vaporariorum (Homoptera: Aleyrodidae), by infection with the fungus Aschersonia aleyrodis (Deuteromycotina: Coelomycetes)

The parasitoid Encarsia formosa is commonly applied to control the greenhouse whitefly Trialeurodes vaporariorum in glasshouse tomatoes and cucumbers. Nevertheless, in some cases the control capacity of this natural enemy is insufficient and an additional selective pest-suppressing agent is desirable. The entomopathogenic fungus Aschersonia aleyrodis was applied to cucumber plants carrying whiteflies in different developmental stages. After spraying each leaf with 2 ml of spore suspension (4 × 10⁶ spores/ml) the plants were kept at 100% RH for 24 hr; thereafter the humidity was lowered to 70% RH at 20°C and the photoperiod was 16 hr. Treated eggs did not become infected, but larvae that hatched from these eggs and settled on the treated abaxial leaf surface were infected at the same rate and to the same degree as treated first instar larvae. This suggests that the spores persist for at least 7 days. The final percentages of infection over all instars when treated as young eggs, old eggs, and first larval instars were 94, 93, and 90%, respectively. The final percentages of infection when treated as third and fourth larval instars and prepupae were 76, 28, and 12%, respectively. The older instars were less susceptible and adults were seldom infected by the fungus. Several applications of A. aleyrodis as a microbial insecticide are needed to achieve sufficient control of whitefly populations in glasshouses.