Comparison of Foraging Behavior, Interspecific Host Discrimination, and Competition of Encarsia formosa and Amitus fuscipennis

The foraging behavior of Amitus fuscipennis MacGown & Nebeker and Encarsia formosa Gahan was studied on tomato leaflets with 20 Trialeurodes vaporariorum (Westwood) larvae in the first or third stage. Ten of the whitefly larvae were previously parasitized and contained a conspecific or a heterospecific parasitoid egg or larva. The host type (host stage and/or previous parasitization) did not influence the foraging behavior of either parasitoid species. The residence time on these tomato leaflets was about 0.9 h for A. fuscipennis and 1.9 h for E. formosa. Amitus fuscipennis hardly stood still and fed little, while E. formosa showed extensive standing still and feeding. As a result, the time walking while drumming was similar for both parasitoid species. The numbers of host encounters and ovipositions per leaflet were similar for both parasitoid species. However, the residence time of A. fuscipennis was half as long as that of E. formosa so the rate of encounters and ovipositions was higher for A. fuscipennis. Amitus fuscipennis is more efficient in finding and parasitizing hosts under these conditions. The walking activity and host acceptance of the synovigenic E. formosa diminished with the number of ovipositions, but not those of the proovigenic A. fuscipennis. Encarsia formosa is egg limited, while A. fuscipennis is time limited because of its short life span and high egg load. Both parasitoid species discriminated well between unparasitized larvae and self-parasitized larvae, but discriminated poorly those larvae parasitized by a conspecific and did not discriminate larvae parasitized by a heterospecific. Self-superparasitism, conspecific superparasitism, and multiparasitism were observed for both parasitoid species. Superparasitism always resulted in the emergence of one parasitoid and multiparasitism resulted in a higher emergence of one parasitoid of the species that had parasitized first. The data suggest that A. fuscipennis is a good candidate for use in biological control of high-density spots of T. vaporariorum when we consider its high encounter and oviposition rate.     

寄主植物对双斑恩蚜小蜂的发育、存活和繁殖的影响

研究了茄子和扶桑两种不同寄主植物对烟粉虱寄生性天敌双斑恩蚜小蜂Encarsia bimaculata发育、存活和繁殖等特性的影响。在26±0.5℃的条件下,在扶桑上,双斑恩蚜小蜂卵至成虫的发育历期为13.6天,2龄幼虫至成虫的存活率为93.2%;而在茄子上双斑恩蚜小蜂卵至成虫的发育历期和2龄幼虫至成虫的存活率分别为12.1天和91.1％。扶桑上双斑恩蚜小蜂雌性成虫的平均寿命为8.0天,平均单雌产卵量为35.9粒;而在茄子上雌性成虫的平均寿命为6.6天,平均单雌产卵量为27.6粒。双斑恩蚜小蜂在扶桑和茄子植物上的种群内禀增长率分别为0.2081和0.892。两种不同寄主植物对双斑恩蚜小蜂在若虫发育历期和存活率、成虫寿命和平均产卵量以及内禀增长率等方面均存在着显著差异。研究结果表明,寄主植物对双斑恩蚜小蜂的发育、存活和繁殖有较大的影响。     

Whitefly control in cut gerbera: is it possible to control Trialeurodes vaporariorum with Encarsia formosa?

We investigated the impact of inundative releases of the parasitoid, Encarsia formosa Gahan (Hymenoptera: Aphelinidae), for control of greenhouse whitefly, Trialeurodes vaporariorum (Westwood), on cut gerbera (Gerbera jamesonii L.) under controlled greenhouse conditions. Experimental units consisted of ten plants covered and separated from other units by gauze tents. We assessed three release rates of the aphelinid parasitoid: a 7-week experiment with a standard release rate (10 m⁻²/14 days), and a subsequent 3-month trial with high (100 m⁻²/week) and very high (1,000 m⁻²/week) release rates. Experimental units without release of parasitoids served as control treatment. Gerbera plants were infested initially with 50–100 juvenile and 50–70 adult whiteflies in the first experiment, and in the second experiment with less than 50 juveniles per plant and 50–70 adults. Whitefly and parasitoid population density were assessed in weekly intervals using infestation and activity categories. Results show that parasitized whiteflies were present in all treatments within 2 weeks after initial release. Unfortunately, it was not possible to control whiteflies with standard release rates of E. formosa. Although parasitism rates slightly increased, the effect on whitefly populations was negligible. Large amounts of honeydew and growth of sooty mold fungi caused the termination of the first experiment. In a second experiment, E. formosa was tested at 10–100 times higher release densities. In contrast to the first experiment, whitefly densities increased steadily during the first 8 weeks, but remained constant until the end of the experiment in both treatments. Parasitism by E. formosa reached its maximum after 8 weeks. We discuss possible reasons for the low efficiency of E. formosa as a whitefly antagonist in greenhouse production of gerbera.     

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。     

The influence of parthenogenesis-inducing Wolbachia on the oviposition behaviour and sex-specific developmental requirements of autoparasitoid wasps

Parthenogenesis-inducing (PI) Wolbachia are bacteria that cause incipient male eggs of parasitoid wasps to develop as females. These microbes may invade populations and lead to fixation of parthenogenesis. In this study, the consequences of fixation of PI Wolbachia on evolution of behaviour and development were addressed in three species of whitefly parasitoids in the genus Encarsia. Most sexual Encarsia are obligate autoparasitoids. In these haplodiploid wasps, fertilized, female-producing eggs are laid in whitefly or scale insect nymphs, while unfertilized, male-producing eggs are laid in immature parasitoids within the homopteran integument. The oviposition behaviour and progeny developmental requirements of unmated females of a sexual autoparasitoid species were compared with two species that were fixed for PI Wolbachia. All species were treated with antibiotics, effectively ‘curing’ the asexual species of Wolbachia infection. As expected, unmated females of the sexual species, E. pergandiella, laid few eggs in whiteflies relative to immature parasitoids, and males emerged exclusively from parasitoids. In contrast, females of one of the parthenogenetic species, E. formosa, laid few eggs in parasitoids relative to whiteflies, and male progeny emerged exclusively from whiteflies. Females of the second parthenogenetic species, E. hispida, were intermediate in their oviposition behaviour. Females laid eggs in both wasps and whiteflies. However, all of the males except one emerged from the whiteflies. The results suggest that the association of autoparasitoids and PI Wolbachia may result in dramatic evolutionary change of both host selection behaviour and developmental requirements of the infected wasps.     

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.     

Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii

Colonization of tomato greenhouses by native predatory mirid bugs at the end of the spring cycle is common in the western Mediterranean area when no broad-spectrum insecticides are applied. Due to their polyphagy, these predators interact with pest populations and also with other natural enemies present in the crop. In this work we evaluate the abundance and timing of greenhouse colonization by these predators and their interaction with the greenhouse whitefly Trialeurodes vaporariorum, a key crop pest, and its introduced parasitoid Encarsia formosa. Although quite unpredictable, natural colonization of greenhouses by Macrolophus caliginosus and Dicyphus tamaninii, the two predominant species in our location, usually leads to the establishment of predator populations in the crop that subsequently prey on greenhouse whitefly. No preference for parasitized pupae was observed in greenhouse samples, while laboratory experiments revealed a marked tendency to avoid parasitoid pupae. In our area, IPM programs for greenhouse tomatoes and other vegetables should take advantage of the presence of this predator complex by allowing the immigration and establishment of its populations without disturbing them with highly toxic and non-selective insecticides.     

Effects of three insecticides on adult bionomics of the parasitoid Encarsia formosa

Pesticides can negatively affect many life history traits of natural enemies. In this study, we studied the effects of three insecticides with different modes of action on the bionomics of Encarsia formosa, a parasitoid of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Buprofezin (800 mg (a.i.)/L) and pyriproxyfen (50 mg (a.i.)/L) were selected among IGRs, while fenpropathrin (250 mg (a.i.)/L) was selected from the Pyrotheroids. Adults of E. formosa were treated via exposure to residues of insecticides on leaf discs. Our results revealed that buprofezin and pyriproxyfen did not affect longevity and fecundity, while fenpropathrin significantly reduced the longevity and fecundity of treated wasps. Results of logistic regression revealed that control, buprofezin- and pryproxyphen-treated E. formosa was a function of host density and followed a type II functional response. In contrast, E. formosa treated by fenpropathrin showed a type III functional response. Estimated attack rate for buprofezin and pyriproxyfen did not differ significantly from the control, whereas fenpropathrin-treated wasps showed a lower attack rate than the control. According to the obtained results, handling time of fenpropathrin-treated wasps was significantly higher (4.57 ± 0.5) than the control (2.83 ± 0.35). Our results showed that the maximum parasitism rate achieved by control wasps was 8.39, while the rate for buprofezin-, pyriproxyfen- and fenpropathrin-treated wasps was 6.99, 7.69 and 5.25, respectively. Overall, results suggest that buprofezin and pyriproxyfen can be used in an integrated pest management programme or biological control programme without destructive effects on the efficiency of this natural enemy in green houses.     

Impacts of two conventional insecticides on different stages of Encarsia inaron Walker parasitizing the whitefly,Trialeurodes vaporariorum Westwood under greenhouse condition

In this research, for the first time, compatibility of imidacloprid and pyriproxyfen was assayed with both pupa and adult stages of Encarsia inaron Walker parasitizing Trialeurodes vaporariorum Westwood. First, the insecticides were sprayed on bean plants containing the parasitoid pupae, thenceforth, survival of the adult parasitoid was evaluated 24 h post-exposure to fresh, 1-, 4-, 7-, 14-, and 21-day-old residues of them on bean leaflets in Petri dishes. Both insecticides significantly reduce E. inaron adult emergence. Mortality of the parasitoid pupa in treatment with imidacloprid (69.7%) was significantly higher than mortality with pyriproxyfen (28.6%). Pyriproxyfen was non-toxic to the adult parasitoid when residues were dried in fresh and aged through the experiment, while in the same condition, imidacloprid significantly killed the adult parasitoids up to 7 days after application. Results have been discussed on the potential compatibility of the insecticides with E. inaron in an integrated pest management (IPM) approach.     

Natural history of whitefly in Costa Rica: an evolutionary starting point

Abstract.  1. To understand evolution of foraging behaviour in the whitefly parasitoid Encarsia formosa (Hymenoptera, Aphelinidae), natural densities and distributions of whitefly (Homoptera, Aleyrodidae) were quantified in E. formosa 's presumed area of origin, the Neotropics.
2. Leaves were collected in Costa Rican nature areas along long transects (2–4 km), short transects (100 m), within 3-D plots (50 dm³−2.3 m³) and along suspension bridges within the canopy, and checked for presence of whitefly nymphs.
3. Generalised linear mixed modelling revealed that the number of hosts on the lower side of a leaflet of an average plant within an average spot of an average transect could be described by a Poisson distribution with mean and variance equal to 0.241, in a ratio of I1:I2:I3:I4 = 0.14:0.23:0.26:0.37. The Poisson mean was affected largely by the plant and less by the spot or transect. Variation in leaf area explained little of the variation between plants. Based on the shape of the opening in vacated puparia, the probability that a whitefly became parasitised eventually was 12% on an average leaflet. Whitefly density was much lower in the canopy than at the forest floor in the same area.
4. Semivariance analyses showed that in one of the three short transects, the numbers of whiteflies on leaves were spatially dependent. In four of seven 3-D plots at least one level of spatial dependence could be detected.
5. Results are discussed in the context of understanding evolution of foraging behaviour by E. formosa .