Intraguild interactions between the predator Macrolophus pygmaeus and the parasitoid Eretmocerus mundus,natural enemies of Bemisia tabaci

The native parasitoid Eretmocerus mundus Mercet and the predator Macrolophus pygmaeus Rambur are widely used to control Bemisia tabaci (Gennadius) in Mediterranean tomato greenhouses. An optimal biological control strategy for B. tabaci should take into account intraguild interactions between these natural enemies. In this study, predator's prey preferences and prey consumption were studied when offered different parasitoid and whitefly stages. The effect of the host plant on the adults of both natural enemies was also examined. M. pygmaeus preferred to consume B. tabaci over E. mundus when immature stages and adults of B. tabaci and E. mundus were offered. They consumed a larger amount of healthy B. tabaci nymphs and adults than of parasitised nymphs or E. mundus adults. The predator M. pygmaeus interfered with the reproduction of E. mundus females on cotton but not on tomato. However, B. tabaci nymphal mortality on tomato associated with parasitoid host feeding was also lower when the adult parasitoids coexisted with the predators. The joint release of M. pygmaeus and E. mundus adults did not increase the control of the whitefly B. tabaci.     

Efficacy of multiple biocontrol agents against the sweet potato whitefly Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on tomato

Abstract: Biological control provides an environmentally harmonious and potentially stable management tactic to combat noxious pests such as Bemisia tabaci, notorious for its resistance to synthetic pesticides. Bioassays conducted under control chamber conditions integrating applications of the parasitoid Encarsia formosa, reared for 20 years on Trialeurodes vaporariorum, and the fungus Verticillium lecanii on the third‐fourth instar nymphs of B. tabaci on tomato, showed a comparable effect between the parasitoid‐fungus combined treatment and the fungus treatment alone (70.7% vs. 70.4%). Analysis of our results indicates antagonism between the two biocontrol agents related to the parasitoids’ ability to discriminate between infected and healthy B. tabaci nymphs. The parasitoid treatment alone produced 36.3% mortality, with no mortality in the distilled water controls. The behavioural performance of the parasitoid could have either genetic or environmental causes. Bioassays studying the feeding habit of the imported mirid predator Macrolophus caliginosus (adults) and the indigenous mirid Camptotylus reuteri (nymphs and adults) on eggs, or early second instar nymphs of B. tabaci, and choice preference tests indicated a significant difference in feeding between M. caliginosus and C. reuteri. There was no significant difference in percentage feeding of M. caliginosus on eggs (2.2%) or second instar nymphs (8.0%). There was a significant difference in feeding of M. caliginosus adults (18.6%) when offered eggs and second instars in the same arena compared with eggs or second instars offered separately. These results could be attributed to the biological behaviour of the predator having a type III functional response. Studies with the local C. reuteri species showed no significant difference in adult and nymphal consumption on second instars of B. tabaci compared with nymphs on eggs. However, C. reuteri adults fed less on eggs compared with nymphs. This local predatory species appears to be more efficient than M. caliginosus in feeding on particular stages of B. tabaci without depending on prey density. This is further supported by the low consumption of both adults and nymphs in the choice test (4% and 2.3%, respectively) compared with M. caliginosus adults (18.6%).     

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.     

Population suppression of Bemisia tabaci (Hemiptera: Aleyrodidae) using yellow sticky traps and Eretmocerus nr. rajasthanicus (Hymenoptera: Aphelinidae) on tomato plants in greenhouses

We conducted three experiments for management of Bemisia tabaci (Gennadius) biotype ‘B’ on tomatoes under greenhouse conditions: (i) vertically placing yellow sticky cards either parallel or perpendicular to tomato rows at a rate of 1 per 3‐m row; (ii) releasing Eretmocerus sp. nr. rajasthanicus once at 30 adults/m² in the high whitefly density greenhouses (> 10 adults/plant), or twice at 15 adults/m² at a 5‐day interval in the low whitefly density greenhouses (< 10 adults/plant); and (iii) using combinations of yellow sticky cards that were placed vertically parallel to tomato rows and parasitoids released once at 30/m² in high whitefly density greenhouses or twice at 15/m² at a 5‐day interval in low whitefly density greenhouses. Our data show that yellow sticky cards trapped B. tabaci adults and significantly reduced whitefly populations on tomato. The yellow sticky cards that were placed parallel to tomato rows caught significantly more whitefly adults than those placed perpendicular to tomato rows on every sampling date. In the treatment where parasitoids were released once at 30/m² in high whitefly density greenhouses, the number of live whitefly nymphs were reduced from 4.6/leaf to 2.9/leaf in 40 days as compared with those on untreated plants on which live whitefly nymphs increased from 4.4/leaf to 8.9/leaf. In the treatment where parasitoids were released twice at 15/m² in low whitefly density greenhouses, the numbers of live nymphs of B. tabaci on tomato leaves were reduced from 2.1/leaf to 1.7/leaf in 20 days as compared with those on untreated plants on which numbers of live nymphs of B. tabaci increased from 2.2/leaf to 4.5/leaf. In the treatment of yellow sticky cards and parasitoid release once at 30/m² in high whitefly density greenhouses, the numbers of live nymphs of B. tabaci on tomato leaves were reduced from 7.2/leaf to 1.9/leaf, and in the treatment of yellow sticky cards and parasitoid release twice at 15/m² at a 5‐day interval at low whitefly density, the numbers of live nymphs of B. tabaci on tomato leaves were reduced from 2.5/leaf to 0.8/leaf; whereas the numbers of live nymphs of B. tabaci on untreated plants increased from 4.4/leaf to 8.9/leaf. An integrated program for management of B. tabaci on greenhouse vegetables by using yellow sticky cards, parasitoids and biorational insecticides is discussed.     

Evaluation of the local population of Eretmocerus mundus (Hymenoptera: Aphelinidae) for biological control of Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) in greenhouse peppers in Argentina

Bemisia tabaci biotype B is a key pest in pepper crops in Argentina. The parasitoid Eretmocerus mundus is frequently found parasitizing this whitefly in greenhouses without pesticide applications. The present studies were carried out with the objective of evaluating control obtained with different rate and number of parasitoid releases under experimental conditions. Release rate: cages with pepper pots were positioned in an experimental greenhouse and randomly assigned to the release rate treatments (0, 1 and 3 pairs of E. mundus/plant/week with a total of three introductions). Number of releases: similar cages were assigned to the number of parasitoid introduction treatments (0, 1, 2 and 3) with the best release rate obtained in the previous trial. In both assays whitefly (adults and nymphs) and parasitoid (parasitized nymphs) population sizes in each cage were monitored weekly for a period of 10 weeks. Results suggested that the introduction of 2 E. mundus/plant/week was enough to suppress host population compared to control treatment (peaks of 7.75 adults and 58.75 nymphs/cage and 643.75 adults and 1598 nymphs/cage, respectively) (p < 0.05), with 85% of parasitism. E. mundus had to be introduced three times to achieve the best pest control (peaks of 1.17 adults and 20.33 nymphs/cage vs. 55.67 adults and 75 nymphs/cage in control treatment) with 84% of parasitism (p < 0.05). These results were then validated in a pepper crop under experimental greenhouse conditions. Whitefly population was lower in those greenhouses where E. mundus was released compared to control greenhouses (0.15 adults and 0.71 nymphs/4 leaves and 0.73 adults and 1.64 nymphs/4 leaves, respectively), with a peak of 54% of parasitism (p < 0.05). We concluded that good suppression of B. tabaci could be achieved using E. mundus under spring conditions in Argentina.     

Predation,oviposition and conversion rates of the predacious mite,Neoseiulus californicus (McGregor) consuming different densities of Tetranychus urticae Koch,Bemisia tabaci (Genn.) and Thrips tabaci Lind.

Rates of prey consumption, egg production and prey conversion by the predacious mite, Neoseiulus californicus (McGregor) were estimated at different densities of Tetranychus urticae Koch, Bemisia tabaci (Genn.) and Thrips tabaci Lind. in the laboratory. N. californicus females functionally and numerically responded to the increasing densities of T. urticae nymphs, B. tabaci nymphs and T. tabaci larvae showing Holling’s type II. The maximum mean predation and oviposition rates by the predator females devouring T. urticae, B. tabaci and T. tabaci occurred at 15, 10 and 10 prey individuals/day, respectively, followed by the plateau levels at higher prey densities. N. californicus females exhibited the highest feeding and oviposition on T. urticae nymphs, followed by T. tabaci larvae and B. tabaci nymphs. The predator females showed the highest efficiency in converting the prey into egg progeny at 5 individuals/day of the previous prey species, respectively. T. urticae was the most favourable for N. californicus females, followed by T. tabaci and B. tabaci.     

Functional response of Neoseiulus cucumeris (Oudemans) (Acari: Phytoseiidae) to Bemisia tabaci (Gennadius) on tomato leaves

Bemisia tabaci (Gennadius) is an important invasive pest of vegetables and other horticultural plants worldwide. In this study, the functional response of Neoseiulus cucumeris (Oudemans) to different stages of immature B. tabaci was evaluated under laboratory conditions. Predation experiments were conducted on tomato leaf discs (2.5?cm diameter) over a 24-h period at 26?±?1°C and 65?±?5% relative humidity with a L16:D8 photoperiod. The prey densities ranged from 5 to 90 immature stages (eggs and first- to fourth-instar nymphs) of B. tabaci per leaf disc. The results showed that the egg stage of B. tabaci was the most susceptible prey stage and that the mated female adult mite (3-day-old) was a more effective predator than the male adult mite. The functional response of adult N. cucumeris followed a Type II trend curve as shown in a logistic regression model. Adult N. cucumeris exhibited different predation tendencies towards prey in different stages of immaturity. The daily maximum number of eggs, first-, second- and third-instar nymphs of B. tabaci killed by a single female over a 24-h period (26?±?1°C, 65?±?5% RH and L16:D8 photoperiod) were 8.5, 5.2, 3.0 and 2.1, respectively, whereas the number killed by a single male was 6.0, 4.0, 2.3 and 1.8, respectively. The results of this study could help determine an effective B. tabaci biocontrol measure that employs a natural predator.     

Development of Encarsia bimaculata (Heraty and Polaszek) (Hymenoptera: Aphelinidae) in Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) nymphs

Encarsia bimaculata was recently described from India as a potentially useful parasitoid of Bemisia tabaci. Its developmental biology was studied in the laboratory at 25–30 °C and 70–75% RH. Results showed that E. bimaculata is a solitary, arrhenotokous, heteronomous, autoparasitoid. Mated females laid eggs internally in B. tabaci nymphs that developed as primary parasitoids. Males developed as hyperparasitoids, either in females of their own species or in other primary aphelinid parasitoids. Superparasitism was common under cage conditions. Both sexes have an egg, three larval instars, prepupal, and pupal stages. Development from egg to adult took 12.70 ± 2.10 days for females and 14.48 ± 2.60 days for males. Individual B. tabaci nymphs were examined for E. bimaculata parasitization using three isozymes: esterase, malate dehydrogenase, and xanthine dehydrogenase. All three isozymes showed differential banding patterns that identified E. bimaculata parasitized or unparasitized B. tabaci nymphs.     

Biological studies of the predacious miteTyphlodromus pelargonicus a predator of the two spotted spider miteTetranychus urticae on cucumber plants [Acari: Phytoseiidae; Tetranychidae]

The predacious miteTyphlodromus pelargonicus El-Badry preyed on the different developmental stages of the two spotted spider miteTetranychus urticae Koch. The development was quickest and the number of prey consumed was highest when individuals were maintained on eggs compared with nymphs or adult female stages. The predator was able to develop and reproduce on the eriophyid miteEriophyes dioscoridis. Soliman & Abou-Awad, nymphs of the tobacco whiteflyBemisia tabaci (Genn.) and pollen grains ofPhoenix dactylifera andRicinus communis. The average number of eggs/♀/day was 1.4, 0.7, 1.2 and 0.9 on eriophyid, whitefly,Ph. dactylifera andR. communis respectively.      

Microbial control of cotton pests: use of the naturally occurring entomopathogenic fungus Aspergillus sp. (BC 639) in the management of Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) and beneficial insects on transgenic cotton crops

The commercial adoption of transgenic Bacillus thuringiensis (Bt) cotton (Bollgard II®) reduced the use of insecticides to control Helicoverpa spp. However, the ineffectiveness of the Bt toxin against sucking pests such as silverleaf whiteflies (Bemisia tabaci) resulted in a marked increase in B. tabaci populations and in the use of insecticides to control this pest. The effect of the entomopathogenic fungus Aspergillus sp. BC 639 on B. tabaci and beneficial insects (predominantly predatory insects) was studied in commercial cotton field trials. The results showed that oil-based extracts of the entomopathogenic fungus BC 639 control the number of B. tabaci adults and nymphs in commercial transgenic cotton crops. The BC 639 fungus caused 60.0%, 67.2%, and 68.8% mortality in adults, and 54.6%, 62.3%, and 51.7% in nymphs at 7, 14, and 21 days after treatment, respectively, relative to the unsprayed controls. The effect of BC 639 at concentrations of 125, 250, and 500?ml/ha on low-density B. tabaci (～10 nymphs/leaf) did not differ significantly from that of the commercial insecticide (pyriproxifen). However, at higher densities (>50 nymphs per leaf), low concentrations of BC 639 (125 and 250?ml/ha) were not as effective as 500?ml/ha BC 639 in successfully controlling the pest. A simple graphic analysis suggested that the more B. tabaci nymphs per leaf, the fewer adults per leaf, and that once the number of nymphs increased to ～70 per leaf, a negative feedback regulatory effect reduced the survivorship of the nymphs and adults and/or caused the emigration of the adults from the contaminated leaves in search of new resources. Therefore, the ability of BC 639 to control B. tabaci adults and nymphs with minimal effects on predatory insects indicates its potential utility in supplementing integrated pest management programmes for cotton crops.     

Impacts of elevated CO2 on Bemisia tabaci infesting Bt cotton and its parasitoid Encarsia formosa

Atmospheric carbon dioxide concentration is expected to rise in the coming decades. Rising atmospheric CO₂ levels may alter plant‐insect‐parasitoid associations due to the indirect effects of CO₂ enrichment on phytochemicals important for herbivore and parasitoid nutrition. Tritrophic effects of elevated CO₂ on Bt cotton (GK‐12) and non‐transgenic (Simian‐3, or S3) cotton [Gossypium hirsutum L. (Malvaceae)], Bemisia tabaci (Gennadius) biotype B (Hemiptera: Aleyrodidae), and its parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae), were examined in open‐top chambers. Significantly, longer egg‐adult developmental duration and higher mortality of nymphs were observed under elevated CO₂ concentrations on both cotton cultivars during three successive generations. However, no significant differences were found in adult longevity, offspring sex ratio, and the number of eggs laid per female adult of B. tabaci fed on transgenic (GK‐12) or non‐transgenic cotton (S3) grown under elevated CO₂. Abundance of B. tabaci adults increased from 10 to 120 per plant and then decreased to 40 per plant through the growing season, but no significant differences in density occurred between CO₂ treatments and between cultivar treatments. Similarly, no significant differences were found in the developmental duration, parasitization rate, and adult emergence rate of E. formosa after parasitizing B. tabaci for three successive generations. Our results showed that the effects of transgenic Bt cotton did not significantly affect the development, survivorship, life span, or fecundity of B. tabaci and its parasitoids. Moreover, interactions between B. tabaci and E. formosa were not significantly affected by elevated CO₂. These results suggest that the biological control of B. tabaci by E. formosa would not be influenced by transgenic Bt cotton and/or elevated CO₂, indicating that the current risk management strategy regarding B. tabaci outbreaks and biocontrol by E. formosa will remain effective if the atmospheric CO₂ level continues to rise.     

Inactivation of Wolbachia Reveals Its Biological Roles in Whitefly Host

Background

The whitefly Bemisia tabaci is cryptic species complex composed of numerous species. Individual species from the complex harbor a diversity of bacterial endosymbionts including Wolbachia. However, while Wolbachia is known to have a number of different roles, its role in B. tabaci is unclear. Here, the antibiotic rifampicin is used to selectively eliminate Wolbachia from B. tabaci so as to enable its roles in whitefly development and reproduction to be explored. The indirect effects of Wolbachia elimination on the biology of Encarsia bimaculata, a dominant parasitoid of B. tabaci in South China, were also investigated.

Methodology/Principal Finding

qRT-PCR and FISH were used to show that after 48 h exposure to 1.0 mg/ml rifampicin, Wolbachia was completely inactivated from B. tabaci Mediterranean (MED) without any significant impact on either the primary symbiont, Portiera aleyrodidarum or any of the other secondary endosymbionts present. For B. tabaci MED, Wolbachia was shown to be associated with decreased juvenile development time, increased likelihood that nymphs completed development, increased adult life span and increased percentage of female progeny. Inactivation was associated with a significant decrease in the body size of the 4^th instar which leads us to speculate as to whether Wolbachia may have a nutrient supplementation role. The reduction in nymph body size has consequences for its parasitoid, E. bimaculata. The elimination of Wolbachia lead to a marked increase in the proportion of parasitoid eggs that completed their development, but the reduced size of the whitefly host was also associated with a significant reduction in the size of the emerging parasitoid adult and this was in turn associated with a marked reduction in adult parasitoid longevity.

Conclusions/Significance

Wolbachia increases the fitness of the whitefly host and provides some protection against parasitization. These observations add to our understanding of the roles played by bacterial endosymbionts.     

Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae)

Peristenus spretus Chen & van Achterberg (Hymenoptera: Braconidae) is a solitary endoparasitoid, which is considered for augmentative biological control of Apolygus lucorum Meyer-Dür (Heteroptera: Miridae) in Chinese cotton fields. Since the association of P. spretus with A. lucorum was only recently discovered, the biology of the parasitoid remains unknown. In order to understand its reproductive biology, the mutual interference and functional response of P. spretus were investigated by altering either the parasitoid or the host density while keeping the other constant. In both experiments, the effects of parasitoid and host densities on parasitism, superparasitism, progeny production and sex ratio were assessed. P. spretus exhibited a Holling type II functional response to changing host densities, indicating that parasitism increases with increasing host density until the parasitoid reaches its maximum reproductive capacity. The model suggested that a single P. spretus female could parasitise a maximum of 88 nymphs per day or four nymphs per hour. Increasing the wasp-nymph ratio from 1:10 to 1:80 significantly increased the offspring production more than fivefold from ±5.8 to ±35.6; further increasing the host densities (above 80 nymphs) did not significantly increase offspring production. Strong mutual interference of foraging P. spretus females occurred only at high parasitoid densities. Parasitoids foraging alone produced an average progeny of 33.4, whereas parasitoids foraging in groups of 16 produced only 2.6. The optimal wasp-nymph ratio for mass-rearing P. spretus is 4:100, given that resources of parasitoids and nymphs are unlimited.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

Host-feeding of three parasitoid species on Bemisia tabaci biotype B and implications for whitefly biological control

Parasitoids in the genera Encarsia and Eretmocerus (Hymenoptera: Aphelinidae) are important biological control agents of whiteflies through their reproductive as well as host‐feeding activities. The feeding capacities of female parasitoids of three species with different reproductive strategies [Encarsia sophia (Girault & Dodd), Encarsia formosa Gahan, and Eretmocerus melanoscutus Zolnerowich & Rose] on their host, sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype B (Homoptera: Aleyrodidae), were evaluated on cabbage in a single‐instar no‐choice experiment in the laboratory and a mixed‐instar choice experiment in the greenhouse. In both single‐ and mixed‐instar experiments, significant differences in host‐feeding capacities were found among the three parasitoid species. Encarsia sophia exhibited superior capacity of host‐feeding compared to E. formosa and E. melanoscutus. In the single‐instar experiment, parasitoids fed more on younger (smaller) hosts than older (larger) hosts. In the mixed‐instar experiments, all three parasitoid species exhibited a clear preference for feeding on older hosts compared to younger hosts. Total number of whitefly nymphs fed on by E. sophia was approximately three times that of the other two parasitoid species. Whitefly mortality accounted for by host‐feeding by E. sophia was up to 59.7%, and, thus, equivalent to parasitization. The significance of host‐feeding of E. sophia for biological control of B. tabaci is discussed.     

Evaluation of the indigenous parasitoid Encarsia transvena (Hymenoptera: Aphelinidae) for biological control of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) in greenhouses in India

The efficiency of the native parasitoid, Encarsia transvena Timberlake for the management of greenhouse whitefly, Bemisia tabaci (Gennadius) was studied in cages and a greenhouse in India. Parasitism by Enc. transvena of B. tabaci on Lycopersicon esculentum L. (tomato), Solanum melongena L. (eggplant) and Nicotiana tabacum L. (tobacco) was evaluated in cages to compare the utility of each species as potential banker plants. B. tabaci populations were consistently present on all three host plant species for almost two months providing sufficient hosts for parasitoid multiplication. Significantly more B. tabaci nymphs/unit leaf area were found on N. tabacum (77.7) and on S. melongena (76.5) than L. esculentum (45.9) in the initial growing period of the plants, that increased more on L. esculentum as the crops grew older. A greater proportion of B. tabaci were parasitised by Enc. transvena on L. esculentum than on N. tabacum and S. melongena. Rate of parasitism on L. esculentum was 25.19 and on N. tabacum was 24.70 in greenhouse. Parasitism, although occurring throughout greenhouses, was greatest on plants within 3 metres of introduced banker plants. The results suggest the utility of the three plant species as potential banker plants for the management of whiteflies in greenhouses.     

Mating and host density affect host feeding and parasitism in two species of whitefly parasitoids

Abstract The parasitoids in the genera of Encarsia and Eretmocerus (Hymenoptera: Aphelinidae) are important biological control agents of whiteflies, and some of them not only parasitize hosts but also kill them with strong host‐feeding capacity. Two whitefly parasitoid species, Encarsia sophia and Eretmocerus melanoscutus were examined to determine if mating and host density affected their host feeding and parasitism. The whitefly host, Bemisia tabaci, was presented to these two wasp species in densities of 10, 20, 30, 40, 50 and 60 third‐instar nymphs per clip cage. Mated whitefly parasitoid females fed on more hosts than unmated females under a range of host densities (under all six host densities for En. sophia; under the densities of 40 nymphs or more for Er. melanoscutus). Meanwhile, mated females parasitized more whitefly nymphs than unmated females under all host densities for both species. With increase of host density, mated or unmated Er. melanoscutus females killed more hosts by host feeding and parasitism. Mated En. sophia females killed more hosts by host feeding with increase of host density, whereas unmated females did not parasitze whitefly nymphs at all. Our results suggest that only mated female parasitoids with host‐feeding behavior should be released in crop systems to increase their bio‐control efficiency.     

Parasitism,host feeding and immature development of Encarsia formosa reared from Trialeurodes vaporariorum and Bemisia tabaci on Trialeurodes ricini

Encarsia formosa Gahan (Hymenoptera: Aphelinidae), a thelytokous parasitoid, is an important biological control agent of whiteflies because of its outstanding reproduction and host‐feeding ability. In this study, we evaluated the parasitism, host feeding and developmental time of E. formosa populations reared on Trialeurodes vaporariorum (Westwood) (EFT) or on Bemisia tabaci (Gennadius) (EFB) when different nymphal instars of the castor whitefly, Trialeurodes ricini (Misra), were offered as hosts, with an aim to understand the preference of the parasitoid on nymphal instars of T. ricini. Experiments were conducted on castor bean plants at 26 ± 2°C, 50–60% RH and 16 : 8 (L : D) photoperiod. The results showed that E. formosa successfully oviposited and fed on all nymphal instars of T. ricini. However, numbers of the first instars fed on by the E. formosa populations reared on T. vaporariorum (EFT) and B. tabaci (EFB) were significantly greater (45.9 and 31.3, respectively) than those of the second (EFT: 30.4 and EFB: 15.8), the third (EFT: 22.4 and EFB: 13.2) and the fourth nymphal instars (EFT: 6.0 and EFB: 3.8). The number of T. ricini nymphs parasitized by E. formosa varied significantly among different instars, and the parasitism rates on the first instar (EFT: 15.2; EFB: 7.7) and fourth instar (EFT: 19.3; EFB: 4.9) were greater than those on the second and third instars. Encarsia formosa reared on T. vaporariorum had a significantly higher host feeding and ovipositing potential on T. ricini than EFB. When parasitizing the fourth instar nymphs, E. formosa completed development in a significantly shorter time (12.9 day) than when ovipositing in other instars (17.8–19.1 day). These results showed that EFT had a better host adaption than EFB. The information from this study should be useful for us to better understand the performance and nymphal preference of E. formosa from T. vaporariorum and B. tabaci when they parasitized and fed on T. ricini, and the interactions of parasitoids with different host whitefly species.     

Distribution of Bemisia tabaci within soybean plants and on individual leaflets

To control whiteflies on soybean crops in an effective and economically viable way, it is necessary to quantify the occurrence and density of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) on the leaflets. Estimating the number of B. tabaci cm^‐2 on leaflets is difficult, because its distribution pattern on the various parts of the plant canopy and on the leaflet surface is unknown. The aim of this study was to evaluate the distribution of B. tabaci nymphs on soybean plants and leaflets, under greenhouse and field conditions. One hundred soybean plants infested with all nymph stages were randomly selected in a greenhouse, and 25 in a field. Of each plant, a trifoliate leaf of the middle third of the plant’s height was selected and its central leaflet was collected (greenhouse experiment), or a trifoliate leaf of each third layer (upper, middle, and lower), of which the left, central, and right leaflets were collected (field experiment). The collected leaflets were divided into 32 sections (1 cm² per section), arranged in an array of eight rows and four columns to count whitefly nymphs. The Morisita index (I_δ), the negative binomial parameter k, and the dispersion index (I) were calculated for each leaflet, using the number of nymphs as variable. The highest population densities of whitefly nymphs were found in the middle third of the soybean plants. In leaflets from the middle third, the nymphs concentrated in the middle and bottom parts of the leaflets, whereas in the upper and lower thirds of the plant, they were randomly distributed on the leaflets.     

Delayed development of the whitefly (Bemisia tabaci) and increased parasitism by Encarsia bimaculata in response to sublethal doses of piperonyl butoxide

Abstract Effects of sublethal piperonyl butoxide (PB) on parasitization of Bemisia tabaci (Gennadius ) (Hemiptera: Aleyrodidae) by Encarsia bimaculata Heraty et Polaszek (Hymenoptera: Aphelinidae) were evaluated both in cage and greenhouse experiments. When first, second and third instar B. tabaci nymphs were treated with PB, all but the first instar were significantly prolonged. Data indicated that sublethal PB could improve E. bimaculata parasitism rates without influencing parasitoid eclosion rates. Prolonged development increased rates of parasitism by E. bimaculata, from 17.6% to 24.7% in cages, presumably by increasing the duration of host exposure. Sublethal PB combined with E. bimaculata as an integrated approach to control B. tabaci was evaluated using life table parameters under greenhouse conditions. Indices of population trend (I) calculated from life tables were estimated at 4.6 for B. tabaci exposed to PB and parasitoids compared to 14.1 with parasitoids alone and 23.5 in untreated controls. The results showed that after PB was sprayed and parasitoids introduced, development of B. tabaci was delayed and the peak of each stage was postponed. The older nymphal stage had highest mortality, primarily due to mortality caused by parasitism by E. bimaculata.