Ovicide in the whitefly parasitoid, Encarsia formosa

The oviposition decisions made by insect parasitoids when encountering hosts of variable quality have been the subject of extensive theoretical and experimental investigation. For parasitoids that lay their eggs inside the host, the possible outcomes of encounters with parasitized hosts have been assumed to include only oviposition (superparasitism), rejection, or in some cases feeding on host haemolymph. We document another outcome in Encarsia formosa Gahan (Hymenoptera: Aphelinidae), a species that has been a model system for the study of oviposition behaviour. In E. formosa, females may kill eggs previously laid within the host by jabbing them with their ovipositor before ovipositing themselves. (1) Our observations indicated that jabbed eggs were indeed killed. (2) In experimental arenas in the laboratory, ovicide occurred in the majority of encounters with parasitized hosts and at highest frequency in encounters resulting in oviposition. (3) There was no significant difference in the handling time associated with oviposition+ovicide in parasitized hosts in comparison with oviposition alone, suggesting that there is no time cost to ovicide. (4) Ovicide did not appear to be incidental to normal probing within a host. Radial analysis of the direction of ovipositor movement with respect to the centre of the previously laid egg within the host showed that females engaged in ovicidal bouts probed most often in the direction of the egg. This is the first well-documented study of ovicide in an endoparasitoid. We suggest ovicide may be under-reported in other endoparasitoid species due to the difficulty of observing it. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Pre- and post-landing response of the parasitoid Encarsia formosa to whitefly hosts on Gerbera jamesonii

One of the factors that may complicate biological control of the greenhouse whitefly on Gerbera jamesonii by Encarsia formosa is the rosette shape of this ornamental, which differs from the vertical shape of most vegetable plants (cucumber, egg plant, tomato, etc.). Therefore, host-habitat location and the behaviour prior to landing on uninfested and infested leaves was studied. Attraction of E. formosa from a short distance by infested leaves could not be detected: the parasitoid females landed at random on uninfested and infested leaves. After the first landing, a redistribution of the wasps occurred on the leaves. After 24 h three times as many wasps were found on the infested leaves than on uninfested ones. In a dispersal experiment with four plants, E. formosa appeared to have no preference for landing on leaves of the medium age class, which is the age class on which most of the whiteflies in a suitable stage for parasitism occur. Twenty percent of the parasitoids were found on the plants 20 min after releasing them. These results were independent of the plant cultivar and the host density on the plants. In the course of 8 h, the number of E. formosa females recovered from plants increased linearly, and this increase was greater on plants where hosts were present and also greater on the plant cultivar with the lowest trichome density. After 24 h, the percentage of females was highest (56%) on plants with the highest host density. E. formosa females were arrested on leaves where hosts were present. Contrary to our expectation, the results from the two G. jamesonii cultivars that differed strongly in leaf hairiness were not significantly different in most experiments. Only at the high host density was parasitism found to be lower on the cultivar with the higher hair density. Parasitoids may walk on top of the `hair coverlet' of cultivars with high trichome density and, therefore, be hampered less than expected.     

Temporal and spatial analysis of greenhouse whitefly and its parasitoid Encarsia formosa in two types of greenhouse ecosystems

Temporal and spatial relationships between greenhouse whitefly and its parasitoid Encarsia formosa were analysed at different levels by using Rook's neighbourhood model, and for two types of greenhouses: a small greenhouse in China (15.1 m²) and a large greenhouse in the Netherlands (6480 m²). For whitefly eggs and larvae, there was no difference in their spatial relationship occurring within- and between-plot in the two types of greenhouses. Eggs and larvae occurrence aggregated with no special directional distributions. Whitefly adults exhibited nonlinear spatial density dependence within-plot, and moved randomly between-plot. Whitefly adults preferred to fly away in a N–S directions and to settle down at a NW–SE directions with an increase in the number of their neighbouring infected plants within-plot. The parasitoid E. formosa showed a strong relationship with the temporal and spatial distribution of the host, but influenced the spatial distribution of whitefly.     

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.     

Intraguild predation by the generalist predator Dicyphus hesperus on the parasitoid Encarsia formosa

Predation was measured in the laboratory by Dicyphus hesperus females on patches of greenhouse whitefly (Trialeurodes vaporariorum) pupae. The patches contained different proportions of unparasitized pupae and those parastisized as nymphs by Encarsia formosa. Dicyphus hesperus fed readily on parasitized pupae and the number of parasitized pupae consumed increased with the proportion available indicating a capacity for intraguild predation. However, D. hesperus females did not display a preference for feeding on parasitized pupae versus unparasitized pupae. Dicyphus hesperus adults were released at three densities into greenhouse enclosures containing tomato plants harbouring greenhouse whitefly and immature E. formosa. Numbers of killed and parasitized whitefly nymphs and pupae and the total number of healthy whitefly were compared among Dicyphus density treatments. On upper leaves, the amount of predation on whitefly nymphs was higher at the highest predator density than at the lower density or in enclosures where D. hesperus was not released. On lower leaves, the number of parasitized pupae was lowest with the highest predator density indicating a negative effect of intraguild predation by D. hesperus on E. formosa. Despite this, Dicyphus density did not affect the density of whitefly in the presence of E. formosa. The results are discussed as they relate to concurrent use of D. hesperus and E. formosa for regulation of greenhouse whitefly populations.     

Non-consumptive effects of Encarsia formosa on the reproduction and metabolism of the whitefly Bemisia tabaci

BioControl - The impact of predatory or parasitic natural enemies on their pest prey or hosts arises not only through consumption but also through non-consumptive effects. Multiple studies have...     

Influence of antibiotics on the offspring production of the Wolbachia-infected parthenogenetic parasitoid Encarsia formosa

Three different concentrations of the antibiotic tetracycline in honey were tested for their influence on the offspring production and longevity of the parasitoid wasp Encarsia formosa. Several earlier publications did not provide a conclusive answer on the effect that the Wolbachia have on these wasps. The results of our experiments show that at high tetracycline hydrochloride concentrations in honey (50mg/ml) the antibiotic is toxic to the females, all females died within three days after the antibiotic treatment. The concentration 5mg/ml was less toxic although the treated females also lived shorter and produced less offspring than the control females. At the lowest tested concentration of 1mg/ml there was no significant difference either in offspring production or in longevity between the control and the treated females. The antibiotic treatment at both 5 and 1mg/ml resulted in exclusively male progeny after the first two days of oviposition. These results are consistent with the theory that in species in which all individuals are infected the Wolbachia should not impose a large fitness cost.     

Role of the aphelinid parasitoid Encarsia guadeloupae in the suppression of the exotic spiralling whitefly Aleurodicus dispersus on banana in India

A field study conducted during 2000-2001 on banana plantation located at Bangalore Rural district revealed that the population of the spiralling whitefly Aleurodicus dispersus Russell declined from 116.85 per 25-cm² leaf area in March 2000 to 1.10 per 25-cm² leaf area in December 2001. During the study period, a total of seven natural enemies were observed. The aphelinid parasitoid Encarsia guadeloupae Viggiani was the only major natural enemy encountered on the spiralling whitefly causing 20.70% parasitism in January 2000, which had increased to 95.68% by December 2001. The density of the spiralling whitefly was positively correlated with maximum temperature and negatively correlated with relative humidity and the parasitism by E. guadeloupae. The multiple regression model showed that about 67.94% of the variation in the whitefly density could be accounted for by parasitism only.     

Root and shoot jasmonic acid induced plants differently affect the performance of Bemisia tabaci and its parasitoid Encarsia formosa

Plants employ both direct and indirect defenses to protect themselves from attacks by herbivores and pathogens. To date most aboveground and belowground interaction studies have focused on interactions between plants and leaf-chewing herbivores, while the plant defence on the performance of phloem-feeding insects, induced by above- and belowground interaction, has been less explored. Here, jasmonic acid (JA) was used to mimic herbivore-induced responses in Chinese broccoli (Brassica oleracea var. alboglabra) roots (RJA) and shoots (SJA). The effects of JA-induced plant defenses on the performance of the phloem-feeding whitefly, Bemisia tabaci, and its aphelinid parasitoid Encarsia formosa were investigated. The results indicated that SJA induction has a much larger negative effect on B. tabaci than RJA: nymphs develop slower and have a lower survivorship. Also, females live shorter and have a lower fecundity on SJA plants compared to those on RJA and untreated control (CON) plants. The intrinsic rate of increase (r_m) of B. tabaci on SJA plants was 0.089, which was significantly lower than those on CON and RJA plants (0.115 and 0.104, respectively). The parasitoid E. formosa, on the other hand, shows a significantly faster development when parasitizing whitefly hosts feeding on SJA plants, whereas parasitism rate, longevity and fecundity were similar to those on RJA and CON plants. The current study reveals that plants induced with exogenous JA vary in both their resistance to whitefly and suitability for parasitoids, depending on the organ to which the JA was applied. Root and shoot JA applications also have contrasting effects on the phloem-feeding insect B. tabaci and its parasitoid, that is, SJA induction leads to more negative effects on whitefly performance than RJA induction, but its parasitoid performs better on hosts reared on SJA plants. These results show that top-down and bottom-up processes governing herbivore populations on Chinese broccoli are working in concert to increase plant resistance when plants are induced by SJA application.     

Vitellogenin of the parasitoid wasp, Encarsia formosa (Hymenoptera: Aphelinidae): gene organization and differential use by members of the genus

The vitellogenin (Vg) gene of the parasitoid wasp, Encarsia formosa (Hymenoptera: Aphelinidae), has been cloned and sequenced. The gene codes for a protein consisting of 1814 amino acids in seven exons. The position of the six introns in the E. formosa gene align with those inferred for the Vg gene of the honeybee, Apis mellifera. The position of two introns in the hymenopteran sequences are shared with every full-length insect Vg gene characterized to date. The deduced amino acid sequence of the E. formosa Vg gene most closely resembles that of the ichneumonid parasitoid, Pimpla nipponica (38% identity). The gene product, less the putative signal peptide, contains large quantities of serine (11.3% of total residues) but lacks the extensive polyserine tracts found in the Vgs of insects outside the apocritan Hymenoptera. The gene also codes for the highest level of lysine (9.5%), and lowest levels of phenylalanine (2.6%) and tyrosine (2.3%), observed in any insect Vg characterized to date. The mature gene product retains 12 cysteine residues in positions conserved in other insect Vgs. Ovary homogenates suggest that processed Vg is stored in the egg as an uncleaved molecule of approximately 200 kDa. Vg expression was examined in three additional Encarsia species. The protein was found in female E. sophia and E. luteola, but not in male E. luteola or female E. pergandiella. Despite extensive screening of a phage library prepared from E. pergandiella genomic DNA, a Vg gene was not detected in this species.     

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.     

Oviposition mechanisms in the whitefly parasitoids Encarsia transvena and Eretmocerus mundus

The ovipositors of two whitefly parasitoids, Encarsia transvena and Eretmocerus mundus were examined using scanning and transmission electron microscopy. That of Encarsia is straight, has an apparently hard and sharply pointed upper valve, and appears well-suited to penetrating a hard substrate. That of Eretmocerus is curved, thick-walled, but has a blunt and apparently flexible tip. These features correlate well with what is known of the mode of oviposition and host feeding in the two taxa, with Encarsia and Eretmocerus ovipositing internally and externally respectively.     

Foraging Behavior of the Parasitoid Encarsia formosa on Gerbera jamesonii Leaves

Insight into the foraging behavior of the parasitoid Encarsia formosa Gahan for whitefly hosts was gained by continuous observation of individual parasitoids on leaves of the ornamental plant Gerbera jamesonii, until females left the leaf. Comparison of the parasitoid behavior on three cultivars gave similar results. Mean searching time on uninfested G. jamesonii leaves of three cultivars was 1 h 30 min and the mean percentage of walking activity of the total observation time on those cultivars was 61%. Both parameters were not influenced by different leaf structures of Gerbera cultivars. Encounters with hosts arrested the parasitoids on the leaves. The walking activity and the percentage of host encounters that resulted in an oviposition decreased with decreasing egg load of the parasitoid. In comparison with tomato, where biological control of whiteflies is successful, only minor differences in the foraging behavior occur, except for the residence time of females, which was about three to four times longer on G. jamesonii leaves, but these leaves are about seven times larger than tomato leaves. The facts that (1) the foraging behavior of E. formosa on G. jamesonii is independant of the cultivar and (2) the foraging behavior is, in many aspects, similar to that on tomato suggest that biological control of whitefly on this ornamental plant is a potential option.     

Effects of sublethal doses of pesticides on the oviposition behaviour of Encarsia formosa

Female Encarsia formosa were enclosed in artificial arenas containing twenty-five Trialeurodes vaporariorum scales on a Cellophane substrate. Either the substrate or the scales were previously treated with chemicals. The number of oviposition wound marks on the scales was used as a measure of effect on parasite behaviour. The insecticides, tetradifon and γ-BHC, had their greatest effect when applied to scales. The fungicides, benomyl and dichlofluanid, were more active on the Cellophane. Pirimicarb applied to the scales decreased oviposition, but greatly increased it when applied to the substrate. It is concluded that even sublethal amounts of pesticides may seriously impair the effectiveness of this parasite in commercial biological control.     

Developmental rates of two congeneric parasitoids,Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), utilizing different egg provisioning strategies

Endoparasitic Hymenoptera vary in the extent to which they provision their eggs and thus in the degree to which they appear to rely on their hosts for resources during embryonic development. In this study, developmental rates were examined in two congeneric parasitoid species, Encarsia formosa and E. pergandiella, that provision their eggs to different degrees. E. formosa eggs are much larger than E. pergandiella eggs. E. formosa eggs hatch significantly earlier than the eggs of E. pergandiella when deposited in 1st or 4th instar nymphs of a common whitefly host, Bemisia tabaci. Both species hatch earlier in 4th instar nymphs, but the delay in hatching in hosts parasitized as 1st instars is much greater in E. pergandiella. While E. formosa develops more rapidly to the 1st larval instar, E. pergandiella emerge as adults significantly earlier, though smaller, than E. formosa adults regardless of the host instar parasitized. These findings show that the extent of provisioning in the eggs of these wasps does not strictly determine their order of progression through different stages of development.     

A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella

Vertically transmitted symbionts of arthropods have been implicated in several reproductive manipulations of their hosts. These include cytoplasmic incompatibility (CI), parthenogenesis induction in haplodiploid species (PI), feminization and male killing. One symbiont lineage in the alpha-Proteobacteria, Wolbachia, is the only bacterium known to cause all of these effects, and has been thought to be unique in causing CI, in which the fecundity of uninfected females is reduced after mating with infected males. Here, we provide evidence that an undescribed symbiont in the Bacteroidetes group causes CI in a sexual population of the parasitic wasp Encarsia pergandiella. Wasps were crossed in all four possible combinations of infected and uninfected individuals. In the cross predicted to be incompatible, infected (I) males x uninfected (U) females, progeny production was severely reduced, with these females producing only 12.6% of the number of progeny in other crosses. The incompatibility observed in this haplodiploid species was the female mortality type; dissections showed that most progeny from the incompatible cross died as eggs. The 16S rDNA sequence of this symbiont is 99% identical to a parthenogenesis-inducing symbiont in other Encarsia, and 96% identical to a feminizing symbiont in haplodiploid Brevipalpus mites. Thus, this recently discovered symbiont lineage is capable of inducing three of the four principal manipulations of host reproduction known to be caused by Wolbachia.     

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.     

Some effects of insecticide deposit patterns on the parasitism of Trialeurodes vaporariorum by Encarsia formosa

The functional response of Encarsia formosa parasitising Trialeurodes vaporariorum on Phaseolus vulgaris was a typical type II functional response (Holling, 1959) where, with increasing host density, the numbers of hosts parasitised by a single parasitoid show a negatively accelerating rise to an upper plateau. A mean maximum parasitism of 6.6 per female per 24 h reached at host densities near 80 larvae per leaf was observed. When presented with insecticide (‘Pynosect 30 ULV’) deposits, the parasite's search pattern changed, conforming to a typical Sigmoid functional response curve. With a uniform cover spray deposit of 27.6 × 10^-7 ml/cm² searching began only at host densities of c. 80 larvae per leaf and the mean maximum parasitism was only 1.5 per female per 24 h. When the insecticide deposit of 27.6 × 10^-7 ml/cm² was in the form of discrete groups of 100 μm droplets, searching began at host densities of c. 40 larvae per leaf but the mean maximum parasitism was low at 2.2. However by using the same discrete deposit pattern but reducing the deposit level to 2.65 × 10^-7 ml/cm² it was possible to obtain the same high mean maximum parasitism as with the untreated control.