Prey selection by Dicyphus hesperus of infected or parasitized greenhouse whitefly

The development of effective biological control programs in which predators are integrated with other natural enemies such as parasitoids and entomopathogens requires an understanding of their interactions. In this study we examined the extent to which the omnivorous mirid bug Dicyphus hesperus, an effective biological control agent of greenhouse whiteflies, accepts prey that are either parasitized by the specialist whitefly parasitoid, Encarsia formosa or infected by the generalist fungal entomopathogen, Beauveria bassiana. In non-choice laboratory experiments, we measured how parasitism and infection of greenhouse whitefly, Trialeurodes vaporariorum, as related to parasitoid age and course of fungal infection, might alter the probability of feeding by second instar or adult female predators. Predation by D. hesperus was similar for parasitized and unparasitized whiteflies, regardless of parasitoid age. However, predators generally avoided feeding on infected whiteflies, particularly when infection was manifested through the presence of oosporein or hyphae on the surface of prey.     

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.     

Establishment of a silverleaf whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) population in western Sydney

A field survey in western Sydney found populations of Bemisia tabaci biotype B (silverleaf whitefly) that have the potential to damage greenhouse vegetable crops prevalent in the region. Adult whiteflies were collected from five farms at 2-week intervals and the proportion of silverleaf whitefly in the overall whitefly population was determined using polyacrylamide gel electrophoresis. High levels of silverleaf whitefly were detected at most sampling dates on two of the farms surveyed and a third farm exhibited lower but relatively continuous silverleaf whitefly abundance. The presence of permanent silverleaf whitefly populations must be considered by the greenhouse industry when formulating whitefly management plans for western Sydney.     

Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly

An ongoing debate in biological control consists of whether interference between biological agents can disrupt pest control. This study investigated the outcome of interactions between the entomopathogen Beauveria bassiana with the whitefly predator Dicyphus hesperus and the parasitoid Encarsia formosa, as well as their effect on the control of the greenhouse whitefly Trialeurodes vaporariorum on greenhouse tomato crops. Our objective was to determine whether the generalist B. bassiana would disrupt biological control by interfering with D. hesperus or E. formosa. In experimental greenhouses, whitefly, parasitoid and predator populations were established, and over 27 days, tomato plants were sprayed with three applications of the B. bassiana based product BotaniGard® (5.13×10³ conidia/mm²) or water (control). Populations of greenhouse whitefly and biological control organisms were regularly monitored in control and B. bassiana-treated compartments. Overall, 10.6% of all whiteflies in treated compartments were infected, and 0.98% were both infected and parasitized. There were 31.7 and 22.3% fewer immature and adult whiteflies, respectively, on B. bassiana-treated plants relative to controls. Parasitism by E. formosa and predation by D. hesperus occurred at rates of 7.5 and 2.5%, respectively, in B. bassiana-treated compartments, and 5 and 6%, respectively in control compartments. Our study suggests that applications of B. bassiana for short-term biological control of greenhouse whiteflies are compatible with the concurrent use of E. formosa and D. hesperus on greenhouse tomato crops.     

Searching behaviour of Encarsia formosa as mediated by colour and honeydew

The habitat- and host-searching behaviour of female Encarsia formosa Gahan (Hymenoptera: Aphelinidae) was assessed using an airflow olfactometer and a filter paper test. Responses to different odour cues, colours, host-produced honeydew, non-host honeydew and single carbohydrates were determined. The parasitoid was not attracted to or arrested by odours emanating from clean tobacco leaves, tobacco leaves heavily infested with the host Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) and covered with honeydew, or honeydew alone. However, E. formosa females showed a significant response to green light transmitted through a tobacco leaf. The yellow part of the spectrum was partly responsible for this response. Thus, the long-range orientation is random with respect to the presence of hosts. Filter paper tests showed that the short-range searching behaviour is influenced by water soluble, non-volatile contact-kairomones contained in the host-produced honeydew. Contact with honeydew excreted by L3/L4 T. vaporariorum resulted in longer searching times than honeydew from adult T. vaporariorum or L3/L4 Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). No difference was found between the response to honeydew excreted by adult and L3/L4 B. tabaci. The parasitoids' response to honeydew was unaffected by the host plant on which the whiteflies had fed. Non-host honeydew and single carbohydrates also affected the searching behaviour of E. formosa but to a lower extent than host honeydew. The possible differences in the carbohydrate and amino acid composition of the honeydew excreted by different life-stages of T. vaporariorum and B. tabaci are discussed.     

Host feeding in insect parasitoids: why destructively feed upon a host that excretes an alternative?

Host feeding is the consumption of host tissue by the adult female parasitoid. We studied the function of destructive host feeding and its advantage over non‐destructive feeding on host‐derived honeydew in the whitefly parasitoid Encarsia formosa Gahan (Hymenoptera: Aphelinidae). We allowed parasitoids to oviposit until they attempted to host feed. We either prevented or allowed host feeding. Parasitoids had access to sucrose solution, with or without additional access to honeydew. Parasitoids that were allowed to host feed did not have a higher egg load 20 or 48 h after host feeding than parasitoids prevented from host feeding. Host feeding did not increase the number of eggs matured within these periods, nor did the time spent host feeding positively affect any of these response variables. On the other hand, the presence of honeydew did have a positive effect on egg load 20 and 48 h after host feeding compared with parasitoids deprived of honeydew. Parasitoids with access to honeydew matured more eggs within these periods than honeydew‐deprived parasitoids. Host feeding increased life expectancy, but this effect was nullified when honeydew was supplied after the host‐feeding attempt. In conclusion, feeding on honeydew could be an advantageous alternative to host feeding in terms of egg quantity and longevity. This applies especially to parasitoids exploiting Homoptera, because these parasitoids can obtain honeydew from the host itself. It is possible that destructive host feeding has evolved to enable females to sustain the production of high‐quality anhydropic eggs, which may be important in the parasitoid's natural environment. We argue that future studies should take natural alternative food sources into more consideration.     

烟粉虱两种寄生蜂生物学特性及寄主竞争关系研究

室内比较了寄生烟粉虱Bemisia tabaci的两种寄生蜂——丽蚜小蜂Encarsia formosa和浅黄恩蚜小蜂En. sophia的生物学特性,并研究了以烟粉虱为寄主时两种寄生蜂间的竞争关系。结果表明：两者的后足胫节长度间无显著差异。浅黄恩蚜小蜂的产卵器及卵均长于丽蚜小蜂的,但浅黄恩蚜小蜂的待产卵量显著少于丽蚜小蜂。浅黄恩蚜小蜂检测寄主所花时间短于丽蚜小蜂,但检查圈数显著多于丽蚜小蜂,产卵时间以丽蚜小蜂所花时间为多。以4龄初期的烟粉虱为寄主时,丽蚜小蜂的卵期为48 h,而浅黄恩蚜小蜂24 h即完成卵期的发育。后者的蛹历期也显著短于丽蚜小蜂的蛹历期。丽蚜小蜂由卵到成虫的总发育历期比浅黄恩蚜小蜂的要长72 h左右。一头丽蚜小蜂与一头浅黄恩蚜小蜂组合后的总产卵量为14.0粒,略高于两头丽蚜小蜂组合的总产卵量（10.2粒）,显著高于两头浅黄恩蚜小蜂组合的产卵量（9.5粒）;两种蜂组合的处理中被寄生寄主体内的着卵量为1.73粒,显著高于单独一种蜂组合中被寄生寄主的着卵量,后两者分别为1.29和1.39粒。在寄主竞争情况下,在被两种蜂均寄生的寄主体内丽蚜小蜂和浅黄恩蚜小蜂产入的卵量分别为1.21和1.43粒,显著高于仅被一种蜂寄生的寄主体内的对应蜂种的卵量,后者分别为1.06和1.19粒。结果提示两种蜂均能识别对方的存在,且浅黄恩蚜小蜂表现出更强的竞争能力。     

Hyperparasitism by an exotic autoparasitoid: secondary host selection and the window of vulnerability of conspecific and native heterospecific hosts

Encarsia transvena is an 'autoparasitoid' in the hymenopteran family Aphelinidae. In this species, female eggs are laid in whitefly nymphs. Male eggs are laid externally on immature parasitoids enclosed within the whitefly integument, either their own species, or other primary parasitoids. We explored parasitism by E. transvena of conspecific female immatures and those of a native primary parasitoid, Eretmocerus eremicus, in laboratory experiments. In the first experiment, female E. transvena were offered different combinations of two stages of E. transvena (late larvae – prepupae (ET2), and early pupae (ET3)), and one stage of E. eremicus (prepupae – early pupae (EE2)) in paired choice tests. The results indicated very little parasitism of ET3 relative to the host it was paired with, either EE2 or ET2. However, when EE2 was offered with ET2, there was no statistically significant difference in parasitism. In a no-choice experiment in which oviposition patterns and male progeny development were examined in four stages of both species of wasp, clear differences were observed between the host species. Only one stage of E. transvena (ET2) was parasitized and supported development of male E. transvena to any significant degree. In contrast, in E. eremicus, EE2, EE3 (red-eyed pupae), and EE4 (late pupae) were all parasitized, and male E. transvena emerged from all three stages, although fewer males emerged from EE4. In both species, wasp larvae that were still enclosed within the wet whitefly remains (ET1 and EE1) were parasitized at a very low rate. Lastly, an experiment that determined the length of the later developmental stages of E. transvena and E. eremicus suggested that the duration of the period in which E. transvena is susceptible to parasitism by conspecific females is less than half the period of susceptibility of E. eremicus. These results taken together suggest the potential for interference of E. eremicus by E. transvena, but other factors not examined here may also influence the outcome of interactions in the field.     

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.     

Insecticides with novel modes of action: Mechanism, selectivity and cross-resistance

Efforts have been made during the past two decades to develop insecticides with selective properties that act specifically on biochemical sites present in particular insect groups, but whose properties differ from other insecticides. This approach has led to the discovery of compounds that affect the hormonal regulation of molting and developmental processes in insects; for example, ecdysone agonists, juvenile hormone mimics and chitin synthesis inhibitors. In addition, compounds that selectively interact with the insect nicotinic acetylcholine receptor, such as imidacloprid, acetamiprid and thiamethoxam, have been introduced for the control of aphids, whiteflies and other insect species. Natural products acting selectively on insect pests, such as avermectins, spinosad and azadirachtin, have been introduced for controlling selected groups of insect pests. Compounds acting on the nervous site that controls the sucking pump of aphids and whiteflies, such as pymetrozine, or respiration, such as diafenthiuron, have been introduced for controlling sucking pests. All the above compounds are important components in pest and resistance management programs.     

Sex allocation and egg distribution of an autoparasitoid, Encarsia pergandiella (Hymenoptera: Aphelinidae)

Abstract. 1. Encarsia pergandiella Howard females develop as primary parasitoids on immature whiteflies, and males develop as secondary parasitoids on females of their own or a related species. The hypothesis that the sex ratio reflects the relative abundance of the two host types was tested in the laboratory using petri dish arenas with varying proportions of early fourth instar greenhouse whitefly (Trialeurodes vaporariorum (West.)) (primary hosts) and pupal female E.pergandiella (secondary hosts). Egg distribution was analysed with respect to sex ratio, super-parasitism and host discrimination.
2. The proportion of primary and secondary hosts parasitized in each treatment reflected the relative availability of each host type. Thus females presented with 75% primary hosts laid more female eggs than male. However, in all treatments, a greater proportion of secondary hosts were parasitized than would be expected from the proportion of secondary hosts available. This indicates that more male eggs were laid than expected.
3. More secondary hosts than primary hosts were superparasitized.
4. Host discrimination analysis using a new test statistic showed that females generally laid eggs at random with regard to previous parasitism of primary or secondary hosts. However, females in one treatment with 50% of each host type appeared to preferentially oviposit in secondary hosts which did not contain any eggs.     

Pyriproxyfen controls silverleaf whitefly, Bemisia tabaci (Gennadius), biotype B (Homoptera: Aleyrodidae) (SLW) better than buprofezin in bitter melons Momordica charantia L. (Cucurbitaceae)

To improve compatibility between chemical and biological controls, the use of selective insecticides such as insect growth regulators (IGRs) is crucial. In cucurbits, the use of pyriproxyfen (an IGR) has been shown by others to be an effective method of reducing the number of sap-sucking insects, especially silverleaf whitefly, Bemisia tabaci (Gennadius) Biotype B (SLW). Therefore, we compared pyriproxyfen and buprofezin (an IGR) with that of no treatment (control) in a bitter melon crop for the control of populations of SLW and for their effects on fruit production. Pyriproxyfen controlled SLW and tended to have heavier fruits than the control treatment and reduced the abundance of nymphs and exuvia. Buprofezin showed no evidence in controlling SLW compared with the pyriproxyfen and control treatments. Neither pyriproxyfen nor buprofezin had any effect on the number of harvested fruit or overall fruit yield, but the average weight per fruit was higher than the control treatment. Pyriproxyfen was effective in controlling whitefly populations in bitter melons, and both pyriproxyfen and buprofezin may have the potential to increase yield. Their longer-term use may increase predation by natural enemies as they are species-specific and could favour build up of natural enemies of SLW. Thus, the judicious use of pyriproxyfen may provide an effective alternative to broad-spectrum insecticides in small-scale cucurbit production.     

环境因子对温室白粉虱携播侧多食跗线螨的影响

侧多食跗线螨Polyphagotarsonemus latus(Banks)能够附着在温室白粉虱Trialeurodes vaporariorum胫跗节上进行远距离扩散,即携播。笼罩试验表明：温室白粉虱对侧多食跗线螨的携播是它们在正常情况下普遍发生的一种现象,18～25℃,50%～75%RH是其发生的最适条件;高温(32～39℃)虽能加速携播,使得1～2 h达到携播高峰,但携播率低,白粉虱不易存活;光照强度对携播率没有显著影响。适温高湿有利于温室白粉虱携带多个跗线螨,随着螨密度的增加,温室白粉虱的携播率和携螨数明显增大。85%携播螨采取翘式附着(呈45°)。显微镜照片清晰显示,携播中侧多食跗线螨的口针插入温室白粉虱足内。