Interactions Between Cassava Mosaic Geminiviruses and Their Vector, Bemisia tabaci (Hemiptera: Aleyrodidae).

The sweetpotato whitefly, Bemisia tabaci (Gennadius) is the vector of the cassava mosaic geminiviruses (CMGs) that cause cassava mosaic disease (CMD). Synergistic interactions between B. tabaci and CMGs have been hypothesized as a cause of whitefly "super-abundance," which has been a key factor behind the spread of the severe CMD pandemic through East and Central Africa. The current study investigated this hypothesis by conducting experiments with CMD-susceptible cassava varieties infected with different CMGs in both the north-western Lake Zone region (pandemic affected) and the eastern Coast Zone where CMD is less severe. Male and female pairs of B. tabaci were placed in clip cages for 48 h on plants of three cassava varieties at each of the two locations. There were significantly more eggs laid on CMG-infected than on CMG-free plants in the Lake Zone, whereas in Coast Zone, there were no significant differences. There were no significant differences in proportions, mortality, and development duration of immature stages of B. tabaci among virus states and cassava variety in the two locations. The overall number of eggs was significantly higher with longer development duration of the immature stages in the Lake than in the Coast Zone, whereas mortality was significantly higher in the Coast than in the Lake Zone. Based on these results, it is concluded that there was no net positive synergistic interaction between CMGs and B. tabaci for either lowland coastal or mid-altitude inland populations. Consequently, other factors seem more likely to be the cause of the "super-abundance," and require further investigation.

Whiteflies stabilize their take-off with closed wings.

The transition from ground to air in flying animals is often assisted by the legs pushing against the ground as the wings start to flap. Here, we show that when tiny whiteflies (Bemisia tabaci, body length ca. 1 mm) perform take-off jumps with closed wings, the abrupt push against the ground sends the insect into the air rotating forward in the sagittal (pitch) plane. However, in the air, B. tabaci can recover from this rotation remarkably fast (less than 11 ms), even before spreading its wings and flapping. The timing of body rotation in air, a simplified biomechanical model and take-off in insects with removed wings all suggest that the wings, resting backwards alongside the body, stabilize motion through air to prevent somersaulting. The increased aerodynamic force at the posterior tip of the body results in a pitching moment that stops body rotation. Wing deployment increases the pitching moment further, returning the body to a suitable angle for flight. This inherent stabilizing mechanism is made possible by the wing shape and size, in which half of the wing area is located behind the posterior tip of the abdomen.

Control of the Tomato Leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), in Open-Field Tomatoes by Indigenous Natural Enemies Occurring in Israel.

The tomato leafminer, Tuta absoluta (Meyrick), had established in Israel by 2010, attacking both open-field tomatoes and greenhouse crops.We searched for its natural enemies in open-field tomatoes, and tried to determine their potential for controlling this pest. We surveyed the local natural enemies in open tomato fields and measured their impact on pest populations in an unsprayed field. We assessed the suppressive ability of the dominant hemipteran predator, Nesidiocoris tenuis Reuter, against T. absoluta under controlled laboratory conditions and evaluated the impact of its augmentation on T. absoluta control in open-field tomatoes. We found five natural enemy species:the predator, N. tenuis, two braconids, and two eulophids. Predation accounted for 64.5±9.2% (mean ± SE) of T. absoluta larval mortality, whereas parasitism accounted for 20.96±7.5%. Together, they eliminated the pest population at tomato harvest time. Under controlled conditions, predation by N. tenuis rose from 58 to 72% with increased density of T. absoluta, suggesting positive density dependence. The reduction of T. absoluta (83%) by N. tenuis was higher than that of Bemisia tabaci (32%), suggesting a preference of N. tenuis for T. absoluta. Augmentation of N.tenuis was as effective as conventional treatment insecticide treatment, and plant damage was low and did not seem to affect yield. Results indicate that reduced pesticide use enables indigenous natural enemies, particularly N.tenuis, to successfully control T. absoluta and prevent crop damage in open-field tomatoes.

Whitefly parasitoids: distribution, life history, bionomics, and utilization.

Whiteflies are small hemipterans numbering more than 1,550 described species, of which about 50 are agricultural pests. Adults are free-living, whereas late first to fourth instars are sessile on the plant. All known species of whitefly parasitoids belong to Hymenoptera; two genera, Encarsia and Eretmocerus, occur worldwide, and others are mostly specific to different continents. All parasitoid eggs are laid in-or in Eretmocerus, under-the host. They develop within whitefly nymphs and emerge from the fourth instar, and in Cales, from either the third or fourth instar. Parasitized hosts are recognized by conspecifics, but super- and hyperparasitism occur. Dispersal flights are influenced by gender and mating status, but no long-range attraction to whitefly presence on leaves is known. Studies on En. formosa have laid the foundation for behavioral studies and biological control in general. We review past and ongoing studies of whitefly parasitoids worldwide, updating available information on species diversity, biology, behavior, tritrophic interactions, and utilization in pest management.

Immature development of Eretmocerus mundus (Hymenoptera: Aphelinidae).

The development from egg to pupation is followed for the wasp Eretmocerus mundus, parasitizing the whitefly Bemisia tabaci. We elucidate and describe structural details, histological developments and changes that the different parasitoid and host tissues have undergone during parasitism. These include the presence and apparent function of very large salivary glands, which probably produce substances that help to regulate the host's decomposition and parasitoid nutrition. Moreover, the gut of all instars is devoid of both peritrophic membrane and microvilli and, in the early instars, it has squamous rather than columnar epithelial cells. Differing from many other parasitoids, the E. mundus larva usually does not come into contact with the host tissues and does not devour the entire host during its development. The possible reasons for the developmental mechanisms, as well as the functions of the host capsule that envelopes the parasitoid, are discussed.

Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci.

BACKGROUND: The whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), and the viruses it transmits, are a major constraint to growing vegetable crops worldwide. Although the whitefly is often controlled using chemical pesticides, biological control agents constitute an important component in integrated pest management programs, especially in protected agriculture. One of these agents is the wasp Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae). E. mundus lays its egg on the leaf underneath the second-third instar nymph of B. tabaci. First instars of the wasp hatch and penetrate the whitefly nymphs. Initiation of parasitization induces the host to form a capsule composed of epidermal cells around the parasitoid. The physiological and molecular processes underlying B. tabaci-E. mundus interactions have never been investigated. RESULTS: We used a cDNA microarray containing 6,000 expressed sequence tags (ESTs) from the whitefly genome to study the parasitoid-whitefly interaction. We compared RNA samples collected at two time points of the parasitization process: when the parasitoid first instar starts the penetration process and once it has fully penetrated the host. The results clearly indicated that genes known to be part of the defense pathways described in other insects are also involved in the response of B. tabaci to parasitization by E. mundus. Some of these responses included repression of a serine protease inhibitor (serpin) and induction of a melanization cascade. A second set of genes that responded strongly to parasitization were bacterial, encoded by whitefly symbionts. Quantitative real-time PCR and FISH analyses showed that proliferation of Rickettsia, a facultative secondary symbiont, is strongly induced upon initiation of the parasitization process, a result that supported previous reports suggesting that endosymbionts might be involved in the insect host's resistance to various environmental stresses. CONCLUSION: This is the first study to examine the transcriptional response of a hemipteran insect to attack by a biological control agent (hymenopterous parasitoid), using a new genomic approach developed for this insect pest. The defense response in B. tabaci involves genes related to the immune response as described in model organisms such as Drosophila melanogaster. Moreover, endosymbionts of B. tabaci appear to play a role in the response to parasitization, as supported by previously published results from aphids.

Plant-mediated interactions between whiteflies, herbivores, and natural enemies.

Whiteflies (Homoptera: Aleyrodidae) comprise tiny phloem-sucking insects. The sessile development of their immatures and their phloem-feeding habits (with minimal physical plant damage) often lead to plant-mediated interactions with other organisms. The main data come from the polyphagous pest species Bemisia tabaci (Gennadius) and Trialeurodes vaporariorum (Westwood), which are intricately associated with their host plants. Although these associations might not represent aleyrodids in general, we rely on them to highlight the fundamental role of host plants in numerous ecological interactions between whiteflies, other herbivores, and their natural enemies. Plant traits often affect the activity, preference, and performance of the whiteflies, as well as their entomopathogens, predators, and parasitoids. Leaf structure (primarily pubescence) and constitutive and induced chemical profiles (defensive and nutritional elements) are critically important determinants of whitefly fitness. Pest management-related and evolutionary biology studies could benefit from future research that will consider whiteflies in a multitrophic-level framework.

Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae).

Whiteflies (Homoptera: Aleyrodidae) are sap-sucking insects that harbor "Candidatus Portiera aleyrodidarum," an obligatory symbiotic bacterium which is housed in a special organ called the bacteriome. These insects are also home for a diverse facultative microbial community which may include Hamiltonella, Arsenophonus, Fritchea, Wolbachia, and Cardinium spp. In this study, the bacteria associated with a B biotype of the sweet potato whitefly Bemisia tabaci were characterized using molecular fingerprinting techniques, and a Rickettsia sp. was detected for the first time in this insect family. Rickettsia sp. distribution, transmission and localization were studied using PCR and fluorescence in situ hybridizations (FISH). Rickettsia was found in all 20 Israeli B. tabaci populations screened but not in all individuals within each population. A FISH analysis of B. tabaci eggs, nymphs, and adults revealed a unique concentration of Rickettsia around the gut and follicle cells, as well as a random distribution in the hemolymph. We postulate that the Rickettsia enters the oocyte together with the bacteriocytes, leaves these symbiont-housing cells when the egg is laid, multiplies and spreads throughout the egg during embryogenesis and, subsequently, disperses throughout the body of the hatching nymph, excluding the bacteriomes. Although the role Rickettsia plays in the biology of the whitefly is currently unknown, the vertical transmission on the one hand and the partial within-population infection on the other suggest a phenotype that is advantageous under certain conditions but may be deleterious enough to prevent fixation under others.

Host-parasite interactions between whiteflies and their parasitoids.

There is relatively little information available concerning the physiological and biochemical interactions between whiteflies and their parasitoids. In this report, we describe interactions between aphelinid parasitoids and their aleyrodid hosts that we have observed in four host-parasite systems: Bemisia tabaci/Encarsia formosa, Trialeurodes vaporariorum/E. formosa, B. tabaci/Eretmocerus mundus, and T. lauri/Encarsia scapeata. In the absence of reported polydnavirus and teratocytes, these parasitoids probably inject and/or produce compounds that interfere with the host immune response and also manipulate host development to suit their own needs. In addition, parasitoids must coordinate their own development with that of their host. Although eggs are deposited under all four instars of B. tabaci, Eretmocerus larvae only penetrate 4th instar B. tabaci nymphs. A pre-penetrating E. mundus first instar was capable of inducing permanent developmental arrest in its host, and upon penetration stimulated its host to produce a capsule (epidermal in origin) in which the parasitoid larva developed. T. vaporariorum and B. tabaci parasitized by E. formosa initiated adult development, and, on occasion, produced abnormal adult wings and eyes. In these systems, the site of parasitoid oviposition depended on the host species, occurring within or pressing into the ventral ganglion in T. vaporariorum and at various locations in B. tabaci. E. formosa's final larval molt is cued by the initiation of adult development in its host. In the T. lauri-E. scapeata system, both the host whitefly and the female parasitoid diapause during most of the year, i.e., from June until the middle of February (T. lauri) or from May until the end of December (E. scapeata). It appears that the growth and development of the insects are directed by the appearance of new, young foliage on Arbutus andrachne, the host tree. When adult female parasitoids emerged in the spring, they laid unfertilized male-producing eggs in whiteflies containing a female parasitoid [autoparasitism (development of male larvae utilizing female parasitoid immatures for nutrition)]. Upon hatching, these male larvae did not diapause, but initiated development, and the adult males that emerged several weeks later mated with available females to produce the next generation of parasitoid females. Thus, the interactions that exist between whiteflies and their parasitoids are complex and can be quite diverse in the various host-parasitoid systems.

Host-parasitoid interactions relating to penetration of the whitefly, Bemisia tabaci, by the parasitoid wasp, Eretmocerus mundus.

It has been reported that the aphelinid wasp Eertmocerus mundus parasitizes all four nymphal instars of the sweet potato whitefly, Bemisia tabaci (Biotype B), with 3rd instars being the preferred hosts. The parasitoid lays its egg on the leaf underneath the host nymph. First instars hatch and later penetrate the whitefly. Previous studies have shown that the initiation of parasitoid penetration induces the host to form a cellular capsule around the parasitoid. As described here, females never oviposited once the 4th instar whitefly nymph had initiated adult development. First instar E. mundus larvae were observed under 2nd, 3rd and 4th instar whitefly nymphs, however, penetration did not occur until the whitefly had reached the 4th instar. The non-penetrating E. mundus larva almost always induced permanent developmental arrest in its 4th instar whitefly host and also caused a reduction in whole body host ecdysteroid titers. Therefore, unless there is a peak in molting hormone titer in the area local to penetration, it appears that the induction of capsule formation is not due to an increase in ecdysteroid titer. As the capsule formed around the penetrating parasitoid, host epidermal cells multiplied and became cuboidal and columnar, and relatively thick layers of new cuticle were deposited within the developing capsule, particularly near its ventral opening. The newly formed host cuticle was thinner in the dorsal part of the capsule and appeared to be absent at its apex. These results provide new information regarding the timing and dynamics of parasitoid oviposition and egg hatch as related to larval penetration, parasitoid-induced changes in whitefly development, molting hormone titers and the process of capsule formation.

Host plant pubescence: effect on silverleaf whitefly, Bemisia argentifolii, fourth instar and pharate adult dimensions and ecdysteroid titer fluctuations.

The ability to generate physiologically synchronous groups of insects is vital to the performance of investigations designed to test insect responses to intrinsic and extrinsic stimuli. During a given instar, the silverleaf whitefly, Bemisia argentifolii, increase in depth but not in length or width. A staging system to identify physiologically synchronous 4th instar and pharate adult silverleaf whiteflies based on increasing body depth and the development of the adult eye has been described previously. This study determined the effect of host plant identity on ecdysteroid fluctuations during the 4th instar and pharate adult stages, and on the depth, length and width dimensions of 4th instar/pharate adult whiteflies. When grown on the pubescent-leafed green bean, tomato and poinsettia plants, these stages were significantly shorter and narrower, but attained greater depth than when grown on the glabrous-leafed cotton, collard and sweet potato plants. Thus, leaf pubescence is associated with reduced length and width dimensions, but increased depth dimensions in 4(th) instars and pharate adults. For all host plants, nymphal ecdysteroid titers peaked just prior to the initiation of adult development. However, when reared on pubescent-leafed plants, the initiation of adult development typically occurred in nymphs that had attained a depth of 0.2 to 0.25 mm (Stage 3 - 4). When reared on glabrous-leafed plants, the initiation of adult development typically occurred earlier, in nymphs that had attained a depth of only 0.15-0.18 mm (Stage 2 Old - early 3). Therefore, based on ecdysteroid concentration, it appears that Stage-2, -3 and -4/5 nymphs reared on pubescent-leafed plants are physiologically equivalent to Stage-1, -2 Young and -2 Old/3, respectively, nymphs reared on glabrous-leafed plants. The host plant affected the width but not the height of the nymphal-adult premolt ecdysteroid peak. However, leaf pubescence was not the determining factor. Thus, host plant identity affects physiological events as well as structural characteristics during whitefly nymphal and adult development.

The nymphal-adult molt of the silverleaf whitefly (Bemisia argentifolii): Timing, regulation, and progress.

The developmental progress of silverleaf whitefly (Bemisia argentifolii) 3rd instars and 4th instar/pharate adults was monitored using a tracking system that had been designed to identify synchronous individuals in another species of whitefly, the greenhouse whitefly, Trialeurodes vaporariorum. When reared on greenbean under conditions of LD 16:8 and a temperature of 26 +/- 2 degrees C, the body depth of 3rd instar SLWFs increased from approximately 0.04 mm (Stage 2) to 0.175-0.2 mm (Stage 7-8) and the body depth of the 4th instar increased from approximately 0.1 mm (Stage 1) to 0.25-0.30 mm (Stage 4-5). The durations of the 3rd instar and the 4th instar/pharate adult were approximately 3 and 7 days, respectively. Examination of coronal sections of 4th instars revealed that adult eye and wing development are initiated during Stage 6, the stage in which an external examination showed that the eye has begun to undergo pigment diffusion. Ecdysteroid titers peaked at approximately 400 fg/ micro g protein during stages 4 through 6A of the 4th instar, i.e., just prior to and upon the initiation of the pharate adult stage. Although adult development is initiated later in the SLWF than in the GHWF (adult eye and wing development begin in Stages 4 and 5, respectively, in GHWFs), the same rapidity of metamorphosis is observed in both species. Within approximately 24 h, the simple bi-layered wing bud developed into a deeply folded wing of nearly adult proportions and within an additional 12-24 h, the nymphal eye and wing bud had been replaced by the well-differentiated eye and wing of the adult whitefly. Our study is the first to describe the regulation, timing, and progress of the nymphal-adult molt and of the structural changes that accompany nymphal-adult metamorphosis in the SLWF.