The parasitoids of the aleyrodid Bemisia tabaci in Israel: development, host preference and discrimination of the aphelinid wasp Eretmocerus mundus

Developmental history and behavior of Eretmocerus mundus Mercet, a parasitoid of Bemisia tabaci was studied at 25°C. The eggs may be laid under all four nymphal instars but not under the pupa. Yet the second and third instars are preferred. The egg hatches only under the fourth instar or the pupa. Developmental medians at 25°C are: Instar I-2.5, II-4, II-4, prepupa-2 and pupa 8 days. When ovipositing, the female stands at an angle of 90° to the host, with wings raised and inserts the ovipositor under the whitefly nymph. The egg is laid close to the insertion point of the whitefly's proboscis into the leaf. After oviposition, the female apparently marks the host while drumming on it with her hind legs. She distinguishes already parasitized hosts from unparasitized ones and refrains from laying under the former. Discrimination is accomplished after antennal drumming only.

---

Les parasitoïdes de Bemisia tabaci (aleyrodidae) en Israel: développement, ponte et sélection des hôtes ches Eretmocerus mundus (aphelinidae)

Résumé Le développment et le comportement de E. mundus, parasitoïde de B. tabaci, ont été étudiés à 25°C. Les oeufs sont pondus sous les quatre stades larvaires (les deuxième et troizième sont préférés) mais pas sous les nymphes. Les oeufs n'éclosent que sous les larves du quatrième stade ou les nymphes. Les temps de développement médiaux sont à 25°, les suivants: stade I: 2,5j; stade II: 4j; stade III: 4j et nymphe 8j. Pendant la ponte, la femelle est à 90° sur son hôte, les ailes dressées, et insère sa tarière sous la larve d'aleurode. L'oeuf est déposé près du point d'insertion de la trompe dans la feuille. Après l'émission, la femelle marque apparemment son hôte pendant qu'elle tambourine avec ses pattes postérieures. Elle distingue les hôtes parasités ou non, et limite sa ponte dans les premiers. La sélection est effectuée seulement après tambourinage antennaire.

     

桑白蚧的重要寄生蜂——桑白蚧恩蚜小蜂的鉴别与利用

桑白蚧恩蚜小蜂Encarsia(=Prospaltella)berlesel(Howard)是寄生桑白蚧Pseudaulacaspls pentagona(Targioni-Tozzctti)的重要寄生蜂,许多国家进行了引进移植,对控制桑白蚧的为害取得明显的成效．本记述了桑白蚧恩蚜小蜂形态特征的鉴别。以及各国引进利用的概况．并讨论了利用寄生蜂防治桑白蚧的重要性．     

Invasion and Displacement of Experimental Populations of a Conventional Parasitoid by a Heteronomous Hyperparasitoid

Aphelinid parasitoids have an outstanding record of success in programmes of classical biocontrol against whiteflies and scale insects. Heteronomous hyperparasitoids are aphelinids in which the sexes develop on or in different hosts. The female always develops as a primary endoparasitoid of Homoptera. The male develops as a secondary parasitoid hyperparasitoid of his own or another species of homopteran endoparasitoid. Caged experiments were performed with the cabbage whitefly, Aleyrodes proletella, to examine the invasion of a population of a conventional parasitoid, Encarsia inaron both sexes primary endoparasitoids by a heteronomous hyperparasitoid, E. tricolor. In all cages the heteronomous hyperparasitoid successfully invaded an established population of the conventional parasitoid and the conventional species population declined to very low levels within 8 weeks of the introduction of the heteronomous hyperparasitoid. The patterns of invasion were different in each cage. In two cages, high levels of male production by E. tricolor were observed, indicating that hyperparasitism of the conventional species was probably an important factor in causing the decline in the E. inaron population. In a reciprocal experiment in which E. inaron was introduced to an established population of E. tricolor the conventional species failed to invade or persist. A survey of published references to complexes of parasitoids containing a heteronomous hyperparasitoid and one or more conventional species indicated that, in the majority of cases, the heteronomous hyperparasitoid was the most important species in the complex. There are clear implications for the use of these parasitoids in programmes of classical biocontrol. This is because high competitive ability against other parasitoids is not necessarily a good indicator of the ability of a species to maintain high levels of pest control, especially when hyperparasitic behaviour is involved.     

Egg laying and host stage preference at constant temperatures inEncarsia tricolor [Hym.: Aphelinidae]

Encarsia tricolor Foërster is a facultative autoparasitoid that develops on the important pestTrialeurodes vaporariorum (Westwood) in outdoor crop conditions, which makes this aphelinid species promising for biological control programs in regions where field and protected crops coexist. In this paper we report the results obtained in the study of daily and totalE. tricolor egg laying and of adult female preference for different host stages in which to lay eggs at constant temperatures in the range 10 to 32 °C. Only whitefly nymphs were present in the searching arena (tomato leaflets). The mean number of eggs laid per female in one day ranged from 4.0 (10 °C and 32 °C) to 15.2 (24 °C). The mean total number of eggs increased with temperature from 10 to 28 °C, reaching a maximum of 123 eggs per female at 28 °C, and decreased sharply from 28 to 32 °C. The relation between the intrinsic rate of increase (r_m) and temperature in the range 10 to 28 °C followed a straight line whose equation was r_m=?0.076+0.011*T (R²=0.99). The r_m ofE. tricolor was greater than the r_m ofT. vaporariorum when temperature was higher than 9.2 °C. The preference for any particular host instar in which to lay eggs was not always significant. However, N4 was the host instar preferred whenever preference was statistically significant.     

Growth and development of Encarsia formosa (Hymenoptera: Aphelinidae) in the greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae): effect of host age

The tiny parasitoid wasp, Encarsia formosa, has been used successfully to control greenhouse whiteflies (GHWFs) in greenhouses in many countries throughout the world. Therefore, there has been considerable interest in developing methods for artificially rearing this wasp. However, little information is available concerning the regulation of its development including the host-parasitoid interactions that are required for the parasitoid to complete its life cycle. Here we confirm that parasitoid developmental rates differ significantly based upon the host instar parasitized. Development was faster when 3rd and 4th instar GHWFs were offered for parasitization than when 1st or 2nd instars were used. Our results show that it is primarily the embryo and the first two parasitoid instars that exhibit prolonged developmental times when 1st and 2nd instar whiteflies are parasitized. Although percent emergence was not affected by host age at the time of parasitization, adult longevity as well as adult emergence pattern varied greatly depending upon the instar parasitized. When 3rd and 4th instar GHWFs were selected for oviposition, adult wasps lived significantly longer than when 1st or 2nd instars were used; also, there was a sharp emergence peak on the 2nd day after emergence was first observed (reduced or absent when 1st or 2nd instar GHWFs were parasitized) and the emergence period was reduced from between 8 and 11 days to 5 days. In general, the younger the host instar parasitized, the less synchronous was parasitoid development. Previous reports that E. formosa will not molt to the 2nd instar until the host has reached its 4th instar were not confirmed. When 1st instar host nymphs were parasitized, 2nd instar parasitoids were detected in 3rd instar hosts. Importantly, however, no matter which instar was parasitized, the parasitoid never molted to its last instar until the host had reached Stage 5 of its last instar, a stage in which host pharate adult formation has been initiated. It appears, then, that a condition(s) associated with host pharate adult formation is required for the parasitoid's final larval molt. Results reported here should facilitate the development of in vitro rearing systems for E. formosa.     

Suitability of Bemisia tabaci (Hemiptera: Aleyrodidae) instars for the parasitization by Encarsia bimaculata and Eretmocerus sp. nr. furuhashii (Hymenoptera: Aphelinidae) on glabrous and hirsute host plants

The host instar preferences of Encarsia bimaculata and Eretmocerus sp. nr. furuhashii parasitizing Bemisia tabaci and their development on four host plants, collard, eggplant, cucumber and tomato, were studied in the laboratory. Both of the parasitoids accepted all nymphal stages of B. tabaci, but E. bimaculata preferred third and fourth instars while Er. sp. nr. furuhashii preferred second and third instars under both choice and no choice conditions. Regardless of host stage parasitized, adults of parasitoids emerged only from fourth instars. When given the simultaneous choice of all instars, E. bimaculata reduced parasitization of first and second instars (3.73 and 4.76%, respectively) while increasing parasitization of third and fourth instars (5.44 and 6.93%, respectively), in contrast Er. sp. nr. furuhashii increased its parasitization of second and third instar nymphs (1.27 and 3.17%, respectively) and decreased that of first and fourth instars (7.0 and 3.06%, respectively). Host plants did not significantly influence instar preference for either parasitoid. Developmental periods of both the parasitoids from egg to adult emergence were longest when first instars were parasitized and shortest when fourth instars were selected. Parasitoid developmental time was generally shorter on glabrous plants than on hirsute plants.     

两种蚜小蜂对烟粉虱寄主的产卵选择性（英文）

双斑恩蚜小蜂和桨角蚜小蜂是华南地区烟粉虱的两种优势种寄生蜂。本文研究了两种寄生蜂对不同龄期烟粉虱寄主的产卵选择特性。结果表明: 两种寄生蜂均可寄生烟粉虱的1～4龄若虫。当只有1个龄期的烟粉虱若虫存在时,双斑恩蚜小蜂更多地寄生3龄和4龄若虫,较少寄生1龄和2龄若虫;而桨角蚜小蜂则更多地寄生3龄和2龄若虫,较少寄生1龄和4龄若虫。在4个龄期若虫同时存在时,双斑恩蚜小蜂会明显增加对3龄和4龄若虫的产卵寄生,降低对1龄和2龄若虫的寄生;而桨角蚜小蜂则增加对2龄和3龄若虫的寄生,减少对1龄和4龄若虫的寄生。寄主植物的差异不影响这二种蚜小蜂对各龄期烟粉虱若虫的产卵选择倾向。结果提示,烟粉虱若虫3龄和4龄是双斑恩蚜小蜂最适宜的寄主,而桨角蚜小蜂最适宜的寄主是烟粉虱2龄和3龄若虫。     

Biological Control of <Emphasis Type="Italic">Melanaspis Obscura</Emphasis> on Oaks in Northern California

In 1988, Encarsia aurantii (Howard) (Hymenoptera: Aphelinidae) was introduced into northern California to control an isolated infestation of obscure scale, Melanaspis obscura (Comstock) (Coccoidea: Diaspididae), on native and exotic oaks (Quercus spp.) in Sacramento’s Capitol Park. By 2002, there was no longer any need for chemical control of the scale (i.e., complete biological control). Both parasite and host are univoltine; peak emergence of adult parasites coincides with the peak of newly settled, first-instar scales. Increase of the parasite and concomitant decline of the scale from 1992 to 2004 are documented for one native and one exotic oak tree. During spring of 2004, mean density of female scales (based on 100 twigs per tree) on 12 previously infested oak trees was generally low, ranging from <1 (eight trees) to ∼15 (single tree) scales/twig. Mean percentage parasitization (per twig) ranged from ∼30 to ∼85%, and was density independent (spatial context) for each of five trees. Two refuges for the scale population were noted: some scale crawlers settled and developed under the parental scale cover (spatial refuge) and some female scales continued to produce crawlers into late summer and early fall, when adult parasites were no longer available (temporal refuge). This case illustrates how an introduction strategy (i.e., single-species release of E. aurantii), which was derived from an analysis of the parasite guild of the pest, was executed in the field and ultimately led to successful biological control.     

松突圆蚧及友恩蚜小蜂空间分布型和种群消长动态研究

通过对广东省试验林区内松突圆蚧Hemiberlesia pitysophila Takagi及其本地种寄生蜂友恩蚜小蜂Encarsia amicula Viggiani et Ren林间空间分布型和种群消长动态的调查研究发现:两者空间分布型相吻合,都为均匀分布;两者在林间全年种群消长曲线均呈"S"型变化。松突圆蚧种群密度高峰期出现在3月下旬至4月下旬,友恩蚜小蜂种群密度高峰期则分别出现在2月下旬和4月下旬至5月中旬。另外友恩蚜小蜂对松突圆蚧的寄生率全年共出现2个高峰期,分别是2月下旬和4月下旬至6月上旬。结果表明,友恩蚜小蜂和寄主松突圆蚧在林间时空发生规律具有高度一致性。     

Functional response and progeny production of the Madeira mealybug parasitoid, Anagyrus sp. nov. nr. sinope: The effects of host and parasitoid densities

We tested the hypothesis that control of an herbivorous pest would be improved by providing floral resources for adult natural enemies. The herbivore was euonymus scale, Unaspis euonymi (Comstock) (Homoptera: Diaspididae), a serious pest of woody ornamental plants. The experimental landscape consisted of 3 × 3 m plots, each containing a central bed of Euonymus fortunei (Turcz.) that was infested with the scale. Floral resource plants were cultivars of four species that overlapped in bloom periods to provide a continuous supply of floral resources during summer: Trifolium repens L., Euphorbia epithymoides L., Coreopsis verticillata L. var. ‘Moonbeam,’ and Solidago canadensis L. var. ‘Golden Baby.’ Plots contained either low or high densities of all four species, or no resource plants. Densities of euonymus scale were typically lower in plots containing resource plants than in plots without them. Parasitism by Encarsia citrina (Craw.) (Hymenoptera: Aphelinidae) was rarely influenced by the experimental treatments, flower biomass, whole-plant biomass, or scale density, but in some cases was inversely correlated with density of scales within a generation and in the subsequent generation. Parasitism occasionally reduced densities of scales in plots containing resource plants, but this effect apparently was related to vegetative, not floral qualities of plants. A steady increase in parasitism rate over the three-year course of the experiment across the entire landscape was associated with decreasing density of scales, suggesting a numerical response by the parasitoid population. These findings suggest that the parasitoid is capable of effectively controlling euonymus scale in ornamental landscapes where environmental conditions are favorable.