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The whitefly, Bemisia tabaci (Gennadius) is a polyphagous pest causing considerable yield loss to many crops around the globe. It is a phloem feeder and transmits several viral diseases as well. It has great genetic diversity and is considered a complex of biotypes. Despite the adoption of several available control strategies, management by chemical pesticides has still been the first choice for the farmers to protect their crops. However, prolonged use of chemical pesticides has ultimately accelerated the development of multifold resistance against various groups of insecticides in different parts of the world. The status of development of insecticide resistance against different groups of insecticides by this pest, mechanisms of resistance, cross-resistance, role of detoxifying enzymes, and management issues have been discussed in this chapter.
Regional Research Station (Hill Zone), Uttar Banga Krishi Viswavidyalaya, India
Tapan Kumar Hath*
Department of Agricultural Entomology, Uttar Banga Krishi Viswavidyalaya, India
*Address all correspondence to: tapanhath@gmail.com
1. Introduction
Whitefly, B. tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae) is a pest of global significance. It is a serious pest of vegetable, field, and ornamental crops [1, 2, 3]. This notorious pest shares global distribution as an important pest in field as well as in greenhouse production systems [2, 4]. Both the nymph and adult cause severe economic loss to the growers by direct sucking sap from the phloem and thereby reducing the yield. They also cause indirect damage by transmitting the virus [5] and excreting honeydew on leaves. As a result of honeydew secretion, black sooty mold develops that impairs photosynthesis ability of the infested plants. B. tabaci is considered as complex of biotypes [4, 6, 7] and composed of at least 40 morphologically indistinguishable species [8, 9, 10, 11]. These biotypes/species are mainly differentiated based on biochemical or molecular polymorphism markers. There are mainly two types of biotypes viz., biotype B and biotype Q. Biotype B is considered to be originated from the Middle East–Asia Minor region (Middle East Asia Minor 1—MEAM1 group) [9] whereas biotype Q possibly originated in the Iberian Peninsula Mediterranean—MED group) [12, 13].
The various biotype of this tiny fly causes significant economic loss. Henneberry and Faust [14] reported approximately 10 billion US dollars (USD) economic loss during the years 1980 to 2000 due to whitefly infestation. They also revealed that there were about 300 USD economic losses due to the infestation of whitefly in different bean crops during 1991. Cotton growers in Arizona, California, and Texas spent 154 million USD during 1994–1998 to control the whitefly [15]. This pest is listed as one of the top 100 invasive species of the world by IUCN. Due to the severity of infestation and polyphagous in nature, farmers largely depend on the chemical management of this pest. As a result of the extensive application of synthetic insecticides, B. tabaci has developed multifold resistance to a wide range of insecticides.
Insecticide resistance is one of the important threats in the changing agricultural scenario. It has been increasing at an alarming rate since the introduction of synthetic insecticides. The first case of insecticide resistance was documented by A.L. Melander in 1914. He reported that the San Jose scale was resistant to lime sulfur. Since then many pests have developed various degrees of resistance against various insecticides. The list is ever-growing.
In Turkey, the whitefly population (Biotype B) showed 20–310-fold resistance to OPs [16]. In India, Asia 1 whiteflies showed high resistance to OPs such as acephate and triazophos [17]. The population from China showed a low level of resistance to chlorpyriphos, dichlorvos, and carbosulfan (carbamate) [18, 19].
This pest has also developed various degrees of resistance against synthetic pyrethroids and neonicotinoids. The magnitude of resistance varies from region to region, and it mainly depends on the frequency of insecticide use. B biotype population from northwestern China [20] and Cyprus [21] showed very high resistance against cypermethrin and bifenthrin. Neonicotinoids were introduced as one of the most important chemicals against whitefly and they also performed well due to their systemic and translaminar properties and high residual activity [22, 23, 24]. However, due to their frequent and extensive use, resistance against these chemicals has been reported from different corners of the world. The first report of neonicotinoid resistance was published in 1996, describing the low efficacy of imidacloprid against B. tabaci [25]. Low-to-moderate levels of resistance to imidacloprid and thiamethoxam were reported from Brazil [26], whereas high levels of resistance were detected from Florida [27]. The same biotype of the pest showed different degrees of resistance to the same class of insecticide. Biotype Q in Israel showed a high level of resistance to thiamethoxam but a moderate level of resistance against imidacloprid and acetamiprid [28]. Control failure of whitefly with neonicotinoid has been reported from Pakistan also. It is due to neonicotinoid resistance in B. tabaci [29]. Naveen et al. [30] reported a high degree of resistance against neonicotinoids from India (Asia I and Asia II-1). Neonicotinoid resistance has also been reported from different parts of China both in biotype B and Q [18, 19, 31]. Biotype Q population of southeastern Spain showed 1–7-fold resistance (low level) against spiromesifen [32] whereas 8–32-fold resistance has been reported from India [17]. Astonishingly, several field populations from Spain showed more than 10,000-fold resistance against spiromesifen [33]. Insect growth regulators (pyriproxyfen and buprofezin) are also proving vulnerable to resistance by B. tabaci [17, 34, 35, 36]. These two chemicals, that is, pyriproxyfen and buprofezin act primarily against immature stages of whiteflies. They have distinct modes of action. Therefore, the chance of cross-resistance is very low. Buprofezin is a chitin synthesis inhibitor and results in nymphal death during ecdysis [37], whereas pyriproxyfen is a juvenile hormone mimic inter-rupting nymphal and pupal development. It also suppresses egg hatching by direct exposure of eggs or transovarially via the treatment of adult females [38]. Resistance to buprofezin was first detected in the Netherlands and thereafter from Spain and Israel [39, 40]. Commercial introduction of pyriproxyfen for management of whitefly was done in the year 1991 in Israel. Within 1 year of its introduction, whitefly developed about 550-fold resistance at LC50 and it was reported from a rose greenhouse that had previously been sprayed only three times with this chemical [40, 41].
Resistance in B. tabaci is known to be multi-factorial based on multiple mechanisms. Enhanced detoxification and modifications to acteyl-cholinesterase (AChE), GABA-gated chloride-ion channel, and voltage-sensitive sodium channel are important mechanisms. Pesticide detoxifying enzymes play an important role in reducing the susceptibility of insecticides. Insecticides are generally hydrophobic in nature. Metabolism converts water-insoluble (apolar) or fat-soluble (lipophilic) insecticides into polar compounds or less lipophilic compounds. Conversion of apolar substances to less lipophilic or polar metabolites takes place by two reactions, that is, phase I (primary) and phase II (secondary) reactions. The phase I metabolites are sometimes polar enough to be excreted but are usually further converted to water-soluble conjugates by phase II reactions. A general insecticide detoxification pathway is as follows (Figure 1).
Several standard methods are there to detect resistance development. At the field level, resistance development is suspected when control failure occurs. There are various reasons for the control failure of pests at the field level. Pesticide resistance is one of the important reasons for control failure. Once control failure is observed in the field, the population is collected and tested in the laboratory for confirmation. In the laboratory leaf-dip bioassays, biochemical assays, or molecular assays are conducted to know the susceptibility status of the population.
3.1 Leaf-dip bioassays
Several bioassay procedures are there to detect the resistance status but the leaf-dip bioassays are usually followed in the case of whitefly. In leaf-dip bioassay serial dilution of the tested insecticides are prepared from the commercial formulation of insecticide. Leaves are collected from the unsprayed field and washed under tap water. Then the washed leaves are air-dried under normal room temperature. Leaf discs of appropriate diameter are prepared and dipped in the insecticidal solution and agitated slightly for 5 to 10 seconds for complete wetting. Sometimes whole leaves are dipped in the insecticidal solution. Then the treated leaves or discs are dried for a few minutes until the surface liquid gets dried. In case of control, leaves or discs are dipped in distilled water. The leaves are kept on a Petri plate or in an appropriate container with a perforated lid or covered with a muslin cloth. Then 20 to 30 adult whiteflies are released in the Petri plates. The tests were carried out and maintained at 24 to 25°C temperature. Mortality is observed 48–72 hours after the treatment depending on the type of insecticides tested. Adults showing no signs of movement are considered as dead. Three replicates are usually carried out for each concentration of each insecticide and also for controls. Percentage of mortality of nymph for each concentration of test insecticide and control was calculated using the following formula:
Percent mortality=Number of dead whitefliesTotal number of whiteflies treated×100E1
Then corrected percent mortality was calculated using Abbott’s formula [42] based on the control mortality, if any. The corrected mortality data of each test insecticide of each location were subjected to probit analysis based on Finney [43]. Now, the resistance ratio (RR) or resistance factor (RF) is calculated using the following formula:
Resistance RatioRR=LC50ofafield populationLC50of the most susceptible populationE2
3.2 Biochemical assays
Biochemical assays are frequently used to characterize resistance mechanisms but they can also be used to detect resistance status. In biochemical assays, the activity of detoxifying enzymes viz., general esterases (GEs), glutathione S-transferases (GSTs), and cytochrome P-450 dependent mixed-function oxidases are estimated using spectrophotometer or microplate reader and compared in different populations. In resistant populations, the activity of pesticide-degrading enzymes is overproduced resulting in efficient degradation of the pesticides.
3.3 Molecular assays
Molecular assays detect genes or mutations involved in resistance. There are different types of nucleic acid-based assays for resistance study. Quantitative PCR, reverse transcription plus quantitative PCR, whole transcriptome sequencing, etc., are some of the important molecular assay techniques. These techniques require highly sophisticated and costly instruments and reagents.
4. Geographical distribution of insecticide resistance in whitefly
The whitefly has developed multifold resistance against various groups of insecticides. Approximately 650 cases of insecticide resistance have been reported in the genus Bemisia, and it has developed resistance against more than 60 active ingredients [44]. Among two biotypes, MED (biotype Q) is considered to be more resistant to insecticides than MEAM1 (biotype B) [28, 35, 45, 46]. In the case of India, the species Asia II-7 has developed more resistance to insecticides than Asia I and Asia II-1 (Table 1) [30].
Control failure of a pest is a very common phenomenon in the case of resistance development. As a result of the control failure, farmers usually increase the frequency of application along with the higher dose of the chemical. Sometimes farmers reduce the interval between two consecutive sprays. All these incidences ultimately worsen the resistance scenario. When the chemical is no more effective to control the pest, then the ineffective pesticide is replaced with a new one provided that a suitable one is available. Initially, the new one also gives good efficacy. However, after repeated and prolonged use, the new one also becomes ineffective. This cycle continues and the pests develop multiple resistance. This scenario has been repeated in various agroecosystems of the world and the effect is enormous. Moreover, under the present scenario, it will be increasingly difficult to design, develop, and introduce new pesticides to solve the problems. Even there is a chance of development of resistance prior to the introduction of a new chemical. Hence, every care should be taken to delay and combat the resistance issue.
The development of pesticide resistance leads to control failure of the pests and thereby increases the cost of production due to higher requirements of the chemicals and frequent application costs. Control failure resulting from the resistance development leads to more use of the chemicals that ultimately deteriorates the quality of the produces. The pesticide residues in the product may be harmful to the health of the consumers and thereby society as a whole. In addition to that pest, resurgence may occur due to disruption of the pest-defender ratio. The secondary pests may attain the status of major pest due to harmful effects on the available natural enemies. As whitefly acts as a vector of various virus diseases of plants, the viral diseases of the plants may increase that may result in huge economic loss to the farmers.
The biological characteristics like migratory ability and polyphagous nature of whitefly promote resistance development. These characteristics cannot be controlled directly. Therefore, multipronged strategies need to be adopted to manage the problem. Insecticide resistance management (IRM) strategies need to be followed to delay and combat the problem. Excessive use of chemical insecticide for the management of whitefly is the main cause of insecticide resistance development. So, we need to use insecticide as last resort. The frequency of insecticide use and thereby the degree of selection pressure is the main driving force for the development of insecticide resistance. Emphasis has to be given in the rotation of insecticides having different modes of action (MOA) based on IRAC’s MoA classification scheme [69]. Insecticides having similar modes of action should not be used frequently. Moreover, the information on the cross-resistance phenomenon needs to be considered. The chance of multiple resistance development is also there in case of extreme selection pressure [50]. Chemicals having different modes of action are enlisted in Table 2. These insecticides may be used in rotation programs for the management of whitefly. The availability and use of an insecticide in a specific crop vary in different countries and it is regulated by law. Hence, it is important to check whether an insecticide is approved for use in a particular crop or not before recommending it. The mode of action, dose, and waiting period of chemicals that are approved for management of whitefly in India are as follows [70]. The cross-resistance information needs to be taken into account before recommendation. The insecticides should be used as per the label claim and should be selected based on the local recommendation or local efficacy and selectivity.
Mitochondrial electron transport inhibitor (complex –I)
150
3
Buprofezin 15.00% + Acephate 35.00% w/w WP
Inhibitor chitin biosynthesis, type 1 + Acetylcholinesterase (AChE) inhibitor
187.5 + 437.5
7
Table 2.
Insecticides with different modes of action for rotation program in whitefly management.
Spraying of mixture formulation of insecticides is also an important tactic for the management of whitefly. The basis of this approach is that individual insecticides in the mixture formulation have different modes of action and they lack cross-resistance [71, 72]. However, it has been found that the frequent and injudicious use of synergized insecticides lead to the development of high degree of resistance to both the chemicals. Despite several controversies over the use of mixture formulation of insecticide, the insecticide mixtures are still popular among farmers.
The chemical insecticide should be used as a last resort for the management of whitefly. Insecticides’ use may be regulated in such a way that the full diversity of available chemicals is exploited instead of over-reliance on a single chemical for a long time. The Israeli strategy introduced in 1987 to preserve susceptibility to insecticides by optimizing and restricting their use to a single treatment per year [40, 41, 72] may be followed. The use of broad-spectrum insecticides should be avoided to minimize nontarget toxicity. This will conserve the natural enemies. The status of resistance should be monitored at regular intervals.
IPM strategies must be emphasized to combat the resistance problem. Some of the IPM strategies for management of whitefly are mass trapping and monitoring of whitefly using yellow sticky traps, use of entomopathogenic fungi (EPF), augmentative release of natural enemies, etc.
7. Biological control of whitefly using natural enemies
About 115 species of whitefly parasitoid belonging to 23 genera in five families (Aphelinidae, Azotidae, Signiphoridae, Encrytidae, and Platygastridae) have been reported [73]. The two most important genera of whitefly parasitoid are Encarsia and Eretmocerus. These two parasitoids significantly reduced the population of whitefly [74, 75, 76]. Apart from these two parasitoids, about 150 predators of whitefly have been reported from different parts of the world. Some of the important predators are ladybird beetles, predaceous bugs, lacewings, and spiders. It has also been reported that Euseious scutalis and Typhlodromips swirskii can significantly reduce the whitefly population on a single plant.
Entomopathogenic fungi or EPF are an important group of biological control agents that play a key role in the natural mortality of whitefly populations. They infect directly through the cuticle. Beauveria bassiana and Metarhizium anisopliae are some of the most commonly used microbial insecticides for the management of whitefly [77, 78]. In addition to these two microbials, Aschersonia, Isaria (Paecilomyces), and Lecanicillium (Verticillium) are also used for the management of whitefly. Moreover, it has recently been reported that Clonostachys rosea has a pathogenic effect on the fourth instar nymphal and adult stages of the whitefly [79].
Modern agriculture is highly dependent on pesticide-based pest control and resistance development is inevitable. Therefore, resistance management strategies need to be adopted to maintain the efficacy of pesticides for successful pest management. For this, resistance diagnosis of whitefly populations needs to be done at regular intervals. Resistance is an evolutionary process. Hence, it needs to be managed wisely. The main reason for resistance development is over-reliance on pesticides. Therefore, pesticides should be used as a last resort and other nonchemical methods of pest management need to be emphasized. These will reduce the selection pressure on whitefly and thereby delay the resistance development.
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Written By
Biswajit Patra and Tapan Kumar Hath
Submitted: 20 September 2021Reviewed: 09 December 2021Published: 02 May 2022
Open access peer-reviewed chapter
