Harnessing natural enemies for sustainable management of Bemisia tabaci: a review of the role of predators, parasitoids and entomopathogens

Bemisia tabaci (Gennadius) biotype B and the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), have become serious pests of cotton and vegetable crops in China since the early 1990s. In recent years, however, B. tabaci have broken out more frequently and widely than have T. vaporariorum. The B. tabaci biotype B has also developed higher resistance to several insecticides. Here, the effects of four different host plants on the insecticide susceptibility of B. tabaci biotype B and T. vaporariorum have been compared. The LC(50) values of imidacloprid, abamectin, deltamethrin and omethoate in T. vaporariorum reared on cucumber were significantly higher than those in B. tabaci (the LC(50) values in T. vaporariorum were respectively 3.13, 2.63, 2.78 and 6.67 times higher than those in B. tabaci). On the other hand, the B. tabaci population reared on cotton was more tolerant to all four insecticides tested than the T. vaporariorum population from the same host, especially to abamectin (up to 8.4-fold). The effects of the four host plants on the activity of carboxylesterase (CarE) in B. tabaci biotype B and T. vaporariorum were also compared. The results showed that, although the CarE activity of B. tabaci and T. vaporariorum varied depending on the host plants, the B. tabaci population possessed significantly higher CarE activity than the T. vaporariorum population reared on the same host plant. This was especially so on cucumber and cotton, where the CarE activities of the B. tabaci population were over 1.6 times higher than those of T. varporariorum. The frequency profiles for this activity in B. tabaci and T. vaporariorum populations reared on same host plant were apparently different.

<i>Tomato chlorosis crinivirus</i>

Historians are keen to remind us that history tends to rhyme, even if it does not repeat itself. In a historical context, the story of today’s genetically modified (GM) crops resembles that of the synthetic organic insecticides beginning circa the second half of the last century. In practice, GM crops include crop cultivars that have been modified by incorporating one or more genes (using genetic engineering techniques) originating from species other than the crop species itself. Presently available GM crops include crop cultivars expressing tolerance to particular herbicides, or resistance to insect pests or diseases (or combinations). Beginning in the late 1940s, synthetic organic insecticides became widely available for agricultural use, were received by farmers and agricultural scientists with excitement and little scepticism, and soon became indispensable if farmers were to remain competitive (Perkins 1982). Synthetic insecticides were rapidly used indiscriminately and the environmental consequences of such indiscriminate use became clearly evident within three decades, including impacts on communities of nontarget organisms (NTO) (Perkins 1982). The human-health consequences were evident sooner, but were largely ignored. Such consequences remain easily seen today, for example in the public’s attitude toward pesticide use in agriculture (due in good measure to Rachel Carson’s Silent Spring), in the ways we attempt to manage agricultural pests (e.g., Integrated Pest Management) and in some of our environmental and agricultural policies (e.g., creation

A 2-year demonstration study was conducted to compare the effectiveness of two sources of Encarsia formosa (EF) on the biological control of the sweetpotato whitefly (SPWF) (Bemisia tabaci Gennadius) on poinsettias (Euphorbia pulcherrima Wild.). Commercially produced EF were raised on the greenhouse whitefly (GHWF) (Trialuerodes vaporariorum Westwood), while the locally produced EF were raised on the SPWF. Results showed that SPWF populations were reduced considerably both years, and maximum nymph parasitism ranged from 60% to &gt;80%. No large differences were observed in the ability of EF to control SPWF populations whether raised on SPWF or GHWF nymphs. This study suggests that there is potential for controlling SPWF populations on poinsettia by EF in conjunction with an integrated pest management (IPM) program.

The ladybeetle, Delphastus catalinae (Horn), is one of the most commonly used predacious natural enemies being commercially reared for controlling whiteflies, including Bemisia tabaci (Gennadius) biotype B (=B. argentifolii Bellows & Perring), on various ornamental and vegetable crops under greenhouse conditions. The development, survivorship, and fecundity of D. catalinae feeding on B. tabaci biotype B on collard plants were determined in the laboratory, and the age-specific life table parameters were analyzed based on the life history data. Developmental time was 4.0, 1.9, 1.1, 1.4, 5.2, and 5.3 days for eggs, first, second, third, fourth instars, and pupae, respectively, with an average of 18.9 days from oviposition to adult emergence for both sexes, 19.0 days for females, and 18.8 days for males. Adult longevities averaged 146.6 days for both sexes, 122.6 days for females, and 170.5 days for males. After an average 4.9 days preoviposition period, females laid a mean of 5.6 eggs per day over a 97.0-day period. Net reproductive rate (R0) and gross reproductive rate (ΣMmx) were estimated by life table analysis at 276.8 and 325.1, respectively. Generation time (T) and doubling time (DT) were 35.6 and 4.8 days respectively, and the intrinsic rate of natural population increase (rm) was estimated at 0.158, or l= 1.171 for the finite rate of increase. The rm value of D. catalinae is similar to or higher than those of the whitefly feeding on most vegetable and ornamental crops, indicating that the ladybeetle is capable of regulating populations of B. tabaci biotype B and other whiteflies under greenhouse conditions.

Infection of tomato by Tomato Yellow Leaf Curl Virus alters the foraging behavior and parasitism of the parasitoid Encarsia formosa on Bemisia tabaci

Zucchini squash, Cucurbita pepo L., is an important vegetable crop in Florida. Physiological disorders and insect-transmitted diseases are major problems for squash growers in semi-tropical regions around the world. Bemisia tabaci (Gennadius) biotype B is a significant whitefly pest and is largely responsible for transmitting viruses and causing physiological disorders in squash. Several studies have shown that whitefly populations are reduced when crops are interplanted with non-host cover crops or mulches. The aim of the present study was to determine how the presence of buckwheat, Fagopyrum esculentum Moench, and a key predator, Delphastus catalinae (Horn), affect whitefly colonization on squash. Whitefly densities were higher on squash than on buckwheat. The introduction of D. catalinae on squash significantly reduced whitefly populations. Overall, there were higher densities of D. catalinae on squash where the whitefly pest was more concentrated compared with buckwheat. The study provided preliminary evidence that D. catalinae, when used in conjunction with buckwheat as a living mulch, may aid in reducing whiteflies in squash. This greenhouse experiment highlights the need to investigate a multitactic approach of intercropping buckwheat with squash and the incorporation of D. catalinae in the field to manage populations of whiteflies and whitefly-transmitted diseases. © 2015 Society of Chemical Industry.

Populations of the whitefly, Bemisia tabaci collected from the Americas and the Caribbean Basin were examined for non-specific esterases and for the ability to induce characteristic phytotoxic disorders in key assay species as a means of investigating biogeographic diversity. Esterase markers were used to detect polymorphisms among regional B. tabaci populations and to establish the present distribution of B. tabaci biotypes in the region. The A biotype occurred only in contiguous locales in northern Mexico and the southwestern US, while the B biotype was present throughout much of the Caribbean Basin and the US, and in Brazil. Distinct C and D type esterase markers were observed for Costa Rican and Nicaraguan B. tabaci populations, respectively. The 0 or null type population was collected only from Jatropha gossypifolia (L.) in Puerto Rico. Laboratory colonies of the A and the B biotypes were almost equally sensitive to an organophosphate, profenofos. The B biotype was more resistant to a pyrethroid, permethrin, suggesting the existence of a biotype of fi. tabaci, with a history of exposure to pesticides with a pyrethroid-based chemistry. In mating studies involving reciprocal crosses between the A and the B biotypes, very few F, female progeny were produced, indicating either minimal or non-existent reproductive compatibility between these haplo-diploid B. tabaci populations, presently considered to be the same species. Evidence is presented for the recent and widespread introduction, and subsequent spread of the B biotype throughout the US, the Caribbean Basin, and other proximal locations.

Characterization of the ryanodine receptor gene in Encarsia formosa (Gahan) and its expression profile in response to diamide insecticides

Bemisia tabaci (Gennadius) biotype B, called a "superbug", is one of the most harmful biotypes of this species complex worldwide. In this report, the invasive mechanism and management of B. tabaci biotype B, based on our 5-year studies, are presented. Six B. tabaci biotypes, B, Q, ZHJ1, ZHJ2, ZHJ3 and FJ1, have been identified in China. Biotype B dominates the other biotypes in many regions of the country. Genetic diversity in biotype B might be induced by host plant, geographical conditions, and/or insecticidal application. The activities of CarE (carboxylesterase) and GSTs (glutathione-S-transferase) in biotype B reared on cucumber and squash were greater than on other host plants, which might have increased its resistance to insecticides. The higher activities of detoxification enzymes in biotype B might be induced by the secondary metabolites in host plants. Higher adaptive ability of biotype B adults to adverse conditions might be linked to the expression of heat shock protein genes. The indigenous B. tabaci biotypes were displaced by the biotype B within 225 d. The asymmetric mating interactions and mutualism between biotype B and begomoviruses via its host plants speed up widespread invasion and displacement of other biotypes. B. tabaci biotype B displaced Trialeurodes vaporariorum (Westwood) after 4-7 generations under glasshouse conditions. Greater adaptive ability of the biotype B to adverse conditions and its rapid population increase might be the reasons of its successful displacement of T. vaporariorum. Greater ability of the biotype B to switch to different host plants may enrich its host plants, which might enable it to better compete with T. vaporariorum. Native predatory natural enemies possess greater ability to suppress B. tabaci under field conditions. The kairomones in the 3rd and 4th instars of biotype B may provide an important stimulus in host searching and location by its parasitoids. The present results provide useful information in explaining the mechanisms of genetic diversity, evolution and molecular eco-adaptation of biotype B. Furthermore, it provides a base for sustainable management of B. tabaci using biological and ecological measures.

Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B is one of the most limiting pests of tomato crops in the world. Tomato yield is currently dependent on the use of pesticides, which are problematic to farmers, consumers and the environment. A promising alternative to reduce the harmful effects caused by the indiscriminated use of synthetic insecticides is the use of insecticides of botanical origin. This study aimed to evaluate the effect of 3% (w/v) aqueous extracts from different structures of thirteen botanical species on the behavior of B. tabaci biotype B adults, as well as insecticidal activity of such aqueous extracts on B. tabaci eggs, nymphs, and adults infesting tomato plants. A distilled water solution was used as a negative control, and thiamethoxam insecticide (18 g/100 L of water) as a positive control. Leaf extract of Toona ciliata was observed to have the most efficient inhibitory effect in tests of extracts on whitefly behavior. Furthermore, the use of leaf extract of Toona ciliata led to the most drastic reduction in the number of adults and eggs on tomato leaflets. Leaf extract of Piper aduncum led to the greatest observed ovicidal effect (78.00% of non-hatched nymphs); however it was not effective against nymphs and adults. The leaf extracts of Trichilia pallida, Trichilia casaretti, and Toona ciliata showed the highest control indexes (67.9, 60.3, and 55.1%, respectively). For adults mortality, T. pallida was the most effective (72.8%). Our results indicate that application of extracts of T. pallida, T. ciliata, and T. casaretti are promising strategies to manage B. tabaci biotype B on tomato.

This chapter focuses on greenhouse whitefly (Trialeurodes vaporariorum) and sweet potato whitefly (Bemisia tabaci) attacking greenhouse vegetables (e.g. Lycopersicon esculentum, Capsicum annuum, Cucumis sativus and Lactuca sativa) and ornamental crops in Canada, and provides an overview of the parasitoids (Encarsia formosa and Eretmocerus eremicus) and predators (Delphastus catalinae, Dicyphus hesperus and Macrolophus caliginosus) that have been used for its management, and the evaluation of effectiveness of these biological control agents. Future research prospects are recommended.

Bemisia tabaci (Genn.) was considered a secondary pest in Brazil until 1990, despite being an efficient geminivirus vector in beans and soybean. In 1991, a new biotype, known as B. tabaci B biotype (=B. argentifolii) was detected attacking weed plants and causing phytotoxic problems in Cucurbitaceae. Nowadays, B. tabaci is considered one of the most damaging whitefly pests in agricultural systems worldwide that transmits more than 60 different plant viruses. Little is known about the genetic variability of these populations in Brazil. Knowledge of the genetic variation within whitefly populations is necessary for their efficient control and management. The objectives of the present study were to use RAPD markers (1) to estimate the genetic diversity of B. tabaci populations, (2) to study the genetic relationships among B. tabaci biotypes and two other whitefly species and (3) to discriminate between B. tabaci biotypes. A sample of 109 B. tabaci female individuals obtained from 12 populations in Brazil were analyzed and compared to the A biotype from Arizona (USA) and B biotype from California (USA) and Paraguay. Trialeurodes vaporariorum and Aleurodicus cocois samples were also included. A total of 72 markers were generated by five RAPD primers and used in the analysis. All primers produced RAPD patterns that clearly distinguished the Bemisia biotypes and the two other whitefly species. Results also showed that populations of the B biotype have considerable genetic variability. An average Jaccard similarity of 0.73 was observed among the B biotype individuals analyzed. Cluster analysis demonstrated that, in general, Brazilian biotype B individuals are scattered independently in the localities where samples were collected. Nevertheless, some clusters were evident, joining individuals according to the host plants. AMOVA showed that most of the total genetic variation is found within populations (56.70%), but a significant portion of the variation is found between crops (22.73%). The present study showed that the B biotype is disseminated throughout the sampled areas, infesting several host plants and predominates over the A biotype.

Insects represent the most diverse group of organisms on our planet with approximately one million described species. While some of them have beneficial effects in ecosystem services through plant pollination and natural pest control, there are numerous quarantine insect pests causing considerable damage to crop production and storage. Consequently, in crop pest management, the application of effective insecticides is extremely needed, and at selection of appropriate active compounds, the effects of insecticides or their residues on non-target organisms should be considered. The application of synthetic insecticides could result in the resistance of the target insect against the applied insecticide. Therefore, recently, a great attention has been devoted to insecticide formulations using active compounds of natural origin that are less toxic than conventional synthetic insecticides, exert the effects exclusively on the target insect and closely related organisms, are very effective in very small doses, are characterized with rapid decomposition, and, due to short exposure, practically do not contribute to environmental pollution. Using a nanotechnology approach, insecticide formulations with the enhanced bioavailability of active ingredients enabling their targeted delivery, controlled release, protection against degradation, and higher effectiveness could be prepared. In this manner, the overuse of these toxic compounds could be avoided resulting in the reduced contamination of the environment and representing an economically favorable solution. This chapter gives a comprehensive overview of recent findings related to the bioactivity of nanoformulations of synthetic and natural insecticides against harmful insects causing severe damage to economically important crops or deteriorating stored food products. The impact of nanoinsecticides on the environment, including potential deleterious effects on non-target organisms, is discussed as well.

Seven spot ladybird beetle, (Coccinella septempunctata) is a widely distributed natural enemy of soft-bodied insect pests especially aphids worldwide. Both the adult and larvae of this coccinellid beetle are voracious feeders and serve as a commercially available biological control agent around the globe. Different techniques are adopted to enhance the mass rearing and storage of this natural enemy by taking advantage of its natural ability to withstand under extremely low temperatures and entering diapause under unfavorable low temperature conditions. The key objective of this study was to develop a cost effective technique for enhancing the storage life and predatory potential of the larvae of C. septempunctata through cold storage in conjunction with the use of nuclear techniques, gamma radiations. Results showed that the host eating potential of larvae was enhanced as the cold storage duration was increased. Gamma irradiation further enhanced the feeding potential of larvae that were kept under cold storage. Different irradiation doses also affected the development time of C. septempuntata larvae significantly. Without cold storage, the lower radiation doses (10 and 25 GY) prolonged the developmental time as compared to un-irradiated larvae. Furthermore, the higher dose of radiation (50GY) increased the developmental time after removal from cold storage. This study first time paves the way to use radiation in conjunction with cold storage as an effective technique in implementation of different biological control approaches as a part of any IPM programs