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.     

Pathogenicity of Aschersonia spp. against whiteflies Bemisia argentifolii and Trialeurodes vaporariorum

Entomopathogenic fungi of the genus Aschersonia are specific for whitefly and scale insects. They can be used as biological control agents against silverleaf whitefly, Bemisia argentifolii and greenhouse whitefly, Trialeurodes vaporariorum. Forty-four isolates of Aschersonia spp. were tested for their ability to sporulate and germinate on semi-artificial media and to infect insect hosts. Seven isolates sporulated poorly (less than 1x10(7) conidia/dry weight) and 10 were not able to infect either of the whitefly species. Several isolates were able to produce capilliconidia. Infection level was not correlated with germination on water agar. After a selection based on spore production and infection, virulence of 31 isolates was evaluated on third instar nymphs of both whitefly species on poinsettia (Euphorbia pulcherrima). Whitefly infection levels varied between 2 and 70%, and infection percentages of B. argentifolii correlated with that of T. vaporariorum. However, mortality was higher for T. vaporariorum than for B. argentifolii, as a result of a higher 'mortality due to unknown causes.' Several isolates, among which unidentified species of Aschersonia originating from Thailand and Malaysia, A. aleyrodis from Colombia, and A. placenta from India showed high spore production on semi-artificial medium and high infection levels of both whitefly species.     

Identification of the molting hormone of the sweet potato (Bemisia tabaci) and greenhouse (Trialeurodes vaporariorum) whitefly

In order to identify the whitefly molting hormone, whole body extracts of mature 4th instar and newly formed pharate adult Bemisia tabaci (Biotype B) and Trialeurodes vaporariorum were prepared and subjected to reverse phase high performance liquid chromatography (RPHPLC). Ecdysteroid content of fractions was determined by enzymeimmunoassay (EIA). The only detectable ecdysteroids that were present in significant amounts in whitefly extracts were ecdysone and 20-hydroxyecdysone. The concentrations of 20-hydroxyecdysone in B. tabaci and T. vaporariorum extracts, respectively, were 40 and 15 times greater than the concentrations of ecdysone. The identity of the two ecdysteroids was confirmed by normal phase high performance liquid chromatography (NPHPLC). When ecdysteroid content of RPHPLC fractions was assayed by radioimmunoassay (RIA), small amounts of polar ecdysteroids were also detected indicating that these ecdysteroids have a very low affinity for the antiserum used in the EIA. Ecdysteroid at 10.4 mM administered by feeding stimulated 2nd instar whitefly nymphs to molt. Based on our results, it appears that 20-hydroxyecdysone is the whitefly molting hormone.     

Germination of the entomopathogenic fungus Verticillium lecanii on scales of the glasshouse whitefly Trialeurodes vaporariorum

In a series of laboratory experiments, tobacco leaf discs infested with scales of the glasshouse whitefly Trialeurodes vaporariorum, were immersed in suspensions of conidia of three strains of the entomopathogenic fungus Verticillium lecanii. The germination of conidia on the insect was recorded and compared with the germination of conidia applied to Czapek—Dox Complete Medium. Laboratory bioassays were performed to record the mortality of whitefly scales exposed to conidia of all three fungal strains. The rate of germination of conidia on the whitefly scales was much reduced compared to that oh complete medium. Differences were recorded in the rate of germination of the three strains on complete medium, but not on the whitefly scales. There was no correlation between the pathogenicity of the strains to whitefly scales in laboratory bioassays and the rate of germination on the host.     

微小花蝽对温室白粉虱的捕食作用

研究微小花蝽Orius minutus(L.)对温室白粉虱Trialeurodes vaporariorum(Westwood)的捕食作用。结果表明,微小花蝽成虫对温室白粉虱各虫态的功能反应呈HollingⅡ型。微小花蝽成虫对温室白粉虱卵、1龄和2龄混合若虫及其3龄若虫的理论最大捕食量分别为123,74和52头/d。微小花蝽成虫对温室白粉虱卵的捕食效应随捕食者个体间干扰作用的增加而下降,符合Hassel-Varley方程,捕食作用率(E)随着微小花蝽数(P)增加而呈幂指数下降,模拟模型E=0.1021P-0.3189,干扰系数为0.3189。在15～40℃的温度范围内,随着温度的升高微小花蝽成虫对温室白粉虱卵的寻找效率提高,最高达1.1990,处置时间缩短,最低达到0.0035d。     

Inheritance of dicrotophos resistance in greenhouse whitefly

We studied inheritance of resistance to dicrotophos in greenhouse whitefly,Trialeurodes vaporariorum Westwood (Homoptera, Aleyrodidae). Compared with females from a field-collected susceptible strains (S), females from a resistant strain (R) ofT. vaporariorum derived from heavily treated cotton fields had a 28-fold greater LC₅₀ to dicrotophos in laboratory bioassays. Concentration-mortality lines obtained from female progeny of reciprocal F₁ crosses (R_♀ XS_♂ and S_♀ XR_♂) were similar, suggesting that inheritance of dicrotophos resistance was autosomal and not influenced by maternal effects. Responses of F₁ female progeny were similar to those of the parental S strain, indicating that the resistance was partially recessive (degree of dominance, D, was −0.61). Mortality observed in female progeny obtained from a backcross (F_1♀ XR_♂) corresponded more closely to expectations derived from polygenic models than to expectations from a monogenic model. The estimated number of effective factors (sensu Lande, 1981) contributing equally to resistance was three.     

In vitro bioassay for the effect of Ajuga reptans phytoecdysteroids on Trialeurodes vaporariorum larval development

A rapid and reliable in vitro bioassay method to test the effects of synthetic and natural compounds on the development of greenhouse whitefly Trialeurodes vaporariorum Westwood (Homoptera Aleyrodidae) is described.Leaf fragments of Nicotiana glauca Graham infested with eggs of whitefly were cultured under aseptic conditions on half-strength Murashige-Skoog medium. The development of the insect in vitro and in vivo were comparable except for a higher mortality rate in the first larval instar.Ecdysteroids from Ajuga reptans L. were applied to leaf fragments by immersion in aqueous solution of the compounds or by addition to the culture medium. A high mortality rate of first larval instars was detected with 29-norsengosterone and ajugalactone treatments. This effect was specially pronounced when the products were incorporated in the medium. A significant increase in mortality was also recorded in the pupal state with a 20-hydroxyecdysone treatment. This effect was never observed before, because all whitefly larvae on A. reptans leaves die in the first larval instar.     

Survival of the parasitoidEncarsia formosa after treatment of parasitized greenhouse whitefly larvae with fungal spores ofAschersonia aleyrodis

The interaction between the entomopathogenic fungusAschersonia aleyrodis and the parasitoidEncarsia formosa on greenhouse whitefly as a host organism was studied, in particular, the survival of the parasitoid after treatment of parasitized hosts with fungal spores. The mean number of parasitized black pupae per parasitoid produced at 25°C was significantly reduced after spore treatment in the first three days following parasitization. Spore treatment four, seven or ten days after parasitization resulted in a mean number of parasitized pupae not significantly different from the number of black pupae in the control. The rather sudden change from low to high survival of parasitized hosts when treated with spores four days after parasitization in spite of high numbers of infected unparasitized larvae, coincided with the hatching of the parasitoid larva from the egg inside the host. Possible reasons for this decrease in susceptibility to infection after parasitoid egg hatch, such as induced changes in host cuticle or haemolymph, are discussed. Parasitoids emerged from treated hosts did not show differences in reproduction compared with parasitoids emerging from untreated hosts. Both natural enemeies of whitefly are compatible to a great extent.     

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.     

Realized heritability of resistance to dicrotophos in greenhouse whitefly

Realized heritability (h ²) of resistance to dicrotophos in greenhouse whitefly,Trialeurodes vaporariorum Westwood, was estimated from a laboratory selection experiment. Five generations of selection increased the LC₅₀ approximately 13-fold. Estimatedh ² of resistance to dicrotophos was 0.40 when calculated with the method of Tabashnik (1992) and 0.35 with the method of Tanaka & Noppun (1989). These results suggest that 35 to 40% of the total phenotypic variation in resistance was caused by additive genetic variation. For thirteen previously reported estimates ofh ² of insecticide resistance in other insect pests, the mean was 0.29. The relatively highh ² of dicrotophos resistance forT. vaporariorum is consistent with rapid resistance development in field populations.     

Unbiased estimation of greenhouse whitefly, Trialeurodes vaporariorum, mean density using yellow sticky trap in cherry tomato greenhouses

The spatial distribution of the count of adult greenhouse whiteflies, Trialeurodes vaporariorum (Westwood), on yellow sticky traps was analyzed using Taylor's power law and spatial autocorrelation statistics in the cherry tomato greenhouses from 1998–1999. Samples were collected weekly using a cylindrically shaped yellow sticky trap placed in a 5 by 8 grid covering 0.10–0.15 ha in each of five cherry tomato greenhouses. Taylor's (1961) power law indicated that counts of T. vaporariorum on traps were aggregated within greenhouses. Spatial autocorrelation analysis showed that trap catches were similar (positively autocorrelated) to a distance of 12.5 m, and then dissimilar (negatively autocorrelated) at >12.5 m. Autocorrelation-lag plots showed a globally significant spatial relation in 34 of 57 sample-weeks according to Bonferroni's approximation. The presence of this spatial relation was not related to the changes of mean density. Trap counts at the second lag distance (12.5–25 m) showed little spatial autocorrelation and tended to be the most spatially independent. A fixed-precision-level sequential sampling plan was developed using the parameters from Taylor's power law. The presence of spatial dependency in data sets degraded the sampling plan's precision relative to performance in data sets lacking significant spatial autocorrelation. Therefore, to obtain an unbiased mean density of T. vaporariorum per greenhouse, sticky traps should be placed at least >12.5 m apart to ensure that they are spatially independent.     

The status ofBemisia tabaci (Hom.: Aleyrodidae),Trialeurodes vaporariorum (Hom.: Aleyrodidae) and their natural enemies in Crete

The non «B» biotype ofBemisia tabaci (Gennadius) is recorded for the first time in Crete in 1992, in the north east and south east of the island.Trialeurodes vaporariorum (Westwood) is the predominant whitefly on plants in the north and west of the island. Three surveys of Crete were made in 1992 and 1993 for natural enemies ofB. tabaci andT. vaporariorum and resulted in the collection of 4 species ofEncarsia, (plus a number of species that are unidentifiable at this time), anEretmocerus sp. (unidentifiable at this time) and a fungal pathogen,Paecilomyces farinosus (Dickson Ex Fries) Brown &; Smith.Encarsia adrianae was identified fromT. vaporariorum; which constitutes its most westerly distribution point and a new host record respectively.B. tabaci andT. vaporariorum were found on horticultural crops, ornamentals and weeds. Populations of both whitefly species were severely depleted on field hosts throughout the island during the winter of 1992/93. Climatic constraints, competition withT. vaporariorum in otherwise suitable niches, effective natural enemies and an observed low level of polyphagy may explain the present limited distribution of the non «B» biotype ofB. tabaci in Crete.     

Design and use of a simulation model to evaluate germplasm for antibiotic resistance to the greenhouse whitefly (Trialeurodes vaporariorum) and the sweetpotato whitefly (Bemisia tabaci)

SARAH (Software for theAssessment of antibioticResistance toAleyrodidae inHost plants) is a deterministic simulation model of whitefly population growth based on whitefly life-history components determined on individual plants. The life-history components recorded were oviposition rate, adult survival, pre-adult survival, developmental period, and sex ratio. The simulation model serves as a tool to combine these components and to obtain a single criterion for (antibiotic) resistance. The criterion used was the decrease in simulated intrinsic population growth rate, r _s , relative the r _s value determined on a susceptible control genotype. This model-based evaluation method was tested using the greenhouse whitefly,Trialeurodes vaporariorum Westwood, on tomato and the sweetpotato whitefly,Bemisia tabaci Gennadius, on tomato, eggplant, collard, and pepper. To study its consistency over time, the evaluation method was repeated six times forT. vaporariorum on a susceptible and a resistant tomato cultivar. Simulated intrinsic population growth rate was more consistent in indicating resistance than any of the individual life-history components. Of tenL. hirsutum accessions tested for resistance toT. vaporariorum, three exhibited r _s values that were significantly lower than those for the susceptible control. In addition, on these tenL. hirsutum accessions, a significant positive correlation was observed between r _s and sex ratio (# females/# males). Four host plant species (tomato, collard, eggplant, and pepper) were evaluated for resistance toB. tabaci. All life-history components and r _s values varied among host species, while a negative r _s value was observed forB. tabaci on pepper. A high correlation was found between results from a sensitivity analysis of SARAH and results from a sensitivity analysis of a validated whitefly population simulation model by Yanoet al. (1989a). Significant correlations were found for the relationships between oviposition rate, adult survival, or pre-adult survival and r _s , indicating that none of these life-history components can be omitted from the test procedure. This model-based evaluation method offers a standardized way to quantify levels of antibiotic resistance to whiteflies and will enhance efficiency in breeding programs.     

Repellent effects of pongam oil on settlement and oviposition of the common greenhouse whitefly Trialeurodes vaporariorum on chrysanthemum

The repellent activities, including host deterrence and anti-oviposion, of pongam oil against the adults of the common greenhouse whitefly Trialeurodes vaporariorum Westwood in greenhouses were tested. Chrysanthemum plants treated with different concentrations （0.5%-2.0%） of water-suspended pongam oil showed relatively long-lasting host deterrent and anti-oviposition effects on the adults of greenhouse whitefly. Although the repellent effect declined in time and concentration, strong effects on the reduction of oviposition were found, which lasts, dependent on concentration at least 12 days after application.     

Variation between laboratory populations in the performance of the parasitoid Encarsia formosa on two host species, Bemisia tabaci and Trialeurodes vaporariorum

We tested the hypothesis that populations of the parthenogenetic parasitic wasp Encarsia formosa Gahan (Hymenoptera: Aphelinidae) differed in their ability to use two different host species, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) and Trialeurodes vaporariorum Westwood (Homoptera: Aleyrodidae). Of the three wasp populations tested, two populations had been reared for many generations on B. tabaci and one population had been reared for many years on T. vaporariorum. Performance was measured by the number of whitefly nymphs that were successfully parasitized by individual wasps, and performance on either host was measured in separate experiments. There was variation between wasp populations in their performance on the host B. tabaci, with one wasp population reared for many years on this host performing considerably better than the other two populations. There were no significant differences between populations in their use of the preferred host, T. vaporariorum. The experiments were conducted in such a way that we could distinguish heritable differences between populations from environmentally-induced conditioning differences due to the immediate host from which an individual wasp enclosed. In either experiment there were no significant effects of conditioning, although there was a trend within each population for wasps conditioned on T. vaporariorum to have higher performance than those conditioned on B. tabaci. Thirdly, we conducted a selection experiment, initiated with wasps from a single population historically reared on T. vaporariorum, to measure the effect of laboratory rearing on different hosts for 17 generations. We did not see any difference in the performance of wasps on B. tabaci after this period of rearing on either of the two hosts. In summary, populations of E. formosa do differ in their relative performance on B. tabaci. The one population that was tested further did not show any response to selection by rearing, but the ability to respond to selection on performance may not be equal for all populations. The possibility that wasp populations have differential performance on particular hosts may affect the use of this species as a biological control agent.     

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.     

Timing and ecdysteroid regulation of the molt in last instar greenhouse whiteflies (Trialeurodes vaporariorum)

A system of markers has been devised to track the development of 3rd and 4th instar/pharate adult greenhouse whiteflies. Instars were identified based on measurements of body width and body length. Depending upon the host plant, the product of the two measurements was exceptionally useful in distinguishing between instars. Body depth was used to divide the 3rd instar into eight stages and body depth and color and appearance of the developing adult eye were used to divide the 4th instar/pharate adult into nine stages. Under conditions of L:D 16:8 and a temperature of 26±2°C, the body depth of 3rd instars reared on greenbean increased from 0.025 (stage 1) to 0.2 mm (stage 8) and the instar duration was approximately 3 days. The body depth of 4th instars increased from approximately 0.1±0.02 (Stage 1) to 0.3±0.03 mm (Stage 5) and then remained constant or decreased slightly during adult development. Ecdysteroid titers peaked at approximately 120 fg/μg protein during Stages 3 through 6 of the 4th instar. Based on an external examination of developing 4th instars and the fluctuations in ecdysteroid titer, it appears that adult development is initiated in Stage 4 or 5 4th instars. Results from histological studies support this view. In Stage 4 nymphs, a subtle change was observed in the corneagenous cells of the eye. However, most Stage 4 4th instars possessed wing development characteristic of earlier, immature stages. In all Stage 5 insects, wing development had been initiated and the corneagenous cells had become quite distinct. In Stage 6 whiteflies, the wing buds were deeply folded and by Stage 7, spines were observed on the new cuticle, indicating that the adult cuticle was well-formed by this stage. Our study is the first to investigate the timing and regulation of the molt, to monitor ecdysteroid titers in precisely staged 4th instar whiteflies and to examine the internal anatomical changes associated with metamorphosis in these tiny homopteran insects.     

Stylet penetration by larvae of the greenhouse whitefly on cucumber

Probing behaviour of Trialeurodes vaporariorum (Westwood) larvae was monitored using the DC electrical penetration graph (EPG) technique on the host plant cucumber. EPGs were recorded for 16 h, simultaneously with honeydew excretion using a honeydew clock. Three waveforms were distinguished: a pathway waveform (C), and two phloem waveforms, one with a high (H), and one with a low frequency (L) signal. The C waveform mainly occurred in the crawler stage of the 1st instar larvae. EPGs recorded from larvae during and after moulting indicated that the process involves stylet withdrawal; hence the stylets of each new instar need to penetrate again from the leaf surface to the phloem.All sessile stages, from L1 to pre-pupa, spent almost their entire time in waveforms H and L. These waveforms alternated more frequently in the early instars than during the later ones, in which the H waveform became predominant. The H waveform was highly correlated with honeydew excretion and thus phloem sap ingestion. The L waveform was not related to honeydew excretion but EPGs indicated that the stylet tips remain in a sieve element during both waveforms. Periods of honeydew production demonstrated a delay of 30–40 min in relation to the onset and end of H and L waveforms. This delay is presumably related to the time needed for food passing through, or emptying of, the insect's gut. From the 1st instar to the pre-pupa, the frequency of excreted honeydew droplets decreased but their size increased, causing a net increase of the excretion rate.     

Comparison of Searching Behaviour of Two Aphelinid Parasitoids of the Greenhouse Whitefly, Trialeurodes vaporariorum under Summer vs. Winter Conditions in a Temperate Climate

Searching behaviour of two aphelinid parasitoids, Encarsia formosa Gahan and Eretmocerus eremicus Rose and Zolnerowich, was compared in a controlled environment under simulated summer [high light intensity (83 ± 1 W/m²), and 24 ± 1°C] and winter [low light intensity (11 ± 0.5 W/m²), and 20 ± 1°C] greenhouse conditions on tomato leaflets, with and without a single 3rd instar whitefly host, Trialeurodes vaporariorum (Westwood), within a 4-cm tomato leaflet arena. Residence time of both parasitoid species was longer on infested leaflets vs. clean leaflets, and longer under winter than summer conditions. When parasitoids encountered a host on infested leaflets, residence time increased. In all cases, residence time of E. formosa was longer that of E. eremicus. Proportion of time spent searching (i.e. antennating leaf surface while walking or standing still) was longer on clean vs. infested leaflets for both E. formosa and E. eremicus. Walking speed by E. eremicus on clean leaflets was faster than E. formosa under both summer and winter conditions. Host handling time and proportion of host acceptance did not vary among parasitoids. These findings suggest that E. eremicus could be more efficient in host finding on tomato leaflets than E. formosa over all seasons, especially in the winter when natural light is limiting and where daylight temperatures are ≥20°C.