Key message

  • Bemisia tabaci is globally considered one of the top agricultural pests.

  • Tremendous efforts are invested in developing new insecticides which are highly target-specific in B. tabaci.

  • Bemisia tabaci has evolved resistance to insecticides from most chemical classes including novel insecticides.

  • Advanced methods based on molecular and gene sequence data obtained from resistant and susceptible field-collected B. tabaci populations resulted in better understanding of resistance mechanisms in this pest.

  • There are several components of IPM-IRM programs such as selective and biorational insecticides, insecticide rotation with different modes of action and nonchemical control methods.

Introduction—the whitefly Bemisia tabaci

The sweet potato (cotton) whitefly, Bemisia tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae) is a global, serious pest of vegetable, field and ornamental crops (Byrne and Bellows 1991; Oliveira et al. 2001; Stansly and Naranjo 2010). This pest directly harms plants by feeding on phloem sap and excretes honeydew on leaves and fruits, which forms a substrate for the growth of black sooty mold that stains the leaves, impairs photosynthesis and reduces fruit quality. In cotton, the honeydew may cause fiber stickiness that interferes with the spinning process in the textile mills and greatly reduces the product’s value (Ellsworth et al. 1999; Hequet et al. 2007). Bemisia tabaci is a vector of more than 100 plant viruses (Jones 2003; Hogenhout et al. 2008), and in some cases, viral diseases are limiting growth factors and may cause total crop loss. Cotton leaf curl Virus (CLCV), which is transmitted by B. tabaci, is a major disease of cotton in Asia and Africa, and tomato yellow leaf curl virus (TYLCV) is among the most damaging viruses that harms tomato crops worldwide.

Economic losses due to B. tabaci are enormous; Henneberry and Faust (2008) summarized some reports related to economic losses, which estimated approximately 10 billion US dollars (USD) during the years 1980 to 2000. Perring et al. (1993) estimated the direct losses due to whiteflies outbreaks over a half billion USD in the USA during 1991, and in India they estimated the losses in 1991 to various bean crops to be approximately 300 USD (Henneberry and Faust 2008). In Arizona, California and Texas, cotton growers spent 154 million USD during 1994–1998 to control the whitefly and prevent cotton lint stickiness (Ellsworth et al. 1999). However, losses due to virus diseases transmitted by B. tabaci were considered the most damaging: Briddon (2003) reported that cotton leaf curl virus (CLCV) caused 5 billion USD losses to cotton in Pakistan from 1992 to 1997, and Legg et al. (2014) estimated that cassava mosaic disease (CMD) and cassava brown streak disease (CBSD) caused annual production losses of more than 1 billion USD in Africa.

Bemisia tabaci is known for its genetic diversity and is considered a complex of biotypes (Brown et al. 1995; Perring 2001; Xu et al. 2010) or, as suggested, a complex of distinct cryptic species (De Barro et al. 2011; Boykin et al. 2012; Liu et al. 2012; Boykin and De Barro 2014). The biotypes/species are largely differentiated based on biochemical or molecular polymorphism markers and differ in their biological characteristics such as host plant range, the capacity to cause plant disorders, attraction by natural enemies, expression of resistance and plant virus-transmission capabilities (e.g., Bedford et al. 1994; Sanchez-Campos et al. 1999; Horowitz et al. 2005; Kontsedalov et al. 2008; Watanabe et al. 2019). The B biotype is the most widespread biotype on a worldwide scale (belongs to the Middle East Asia Minor 1—MEAM1 group) and is proposed to be originated from the Middle East–Asia Minor region (De Barro et al. 2011). This biotype was identified in the late 1980s (Costa et al. 1993), following extensive outbreaks of B. tabaci in the southwest USA. An additional common biotype Q (belongs to the Mediterranean—MED group), which possibly originated in the Iberian Peninsula, has since spread globally (Horowitz et al. 2003; Boykin et al. 2007; Chu et al. 2010). So far, the genetic groups of B. tabaci are composed of at least 40 morphologically indistinguishable species (Dinsdale et al. 2010; De Barro et al. 2011; Boykin and De Barro 2014; Hu et al. 2017). In the current review, we will use both terminologies (biotype/species), depending on the cited literature.

Bemisia tabaci has evolved resistance to insecticides from most chemical classes; among the common cryptic species, MED (biotype Q) is considered more resistant than the MEAM1 (biotype B) to insecticides such as pyriproxyfen and neonicotinoids (e.g., Horowitz et al. 2005); however, in recent years, there are other species of Bemisia including MEAM1, Asia I and Asia II-1 that have developed high resistance levels to various groups of insecticides (e.g., Naveen et al. 2017; Dângelo et al. 2018).

The dynamics of B. tabaci species and their association with insecticide resistance

MEAM1 (B) is considered the most common B. tabaci species, and it has probably been dispersed throughout the world by international trade mainly with ornamentals. Early reports have indicated that an invasion of a new biotype resulted in the displacement of indigenous biotypes as a result of competition or possibly other reasons (B biotype displaced A biotype in the USA, Brown et al. 1995; the displacement of B by non-B populations such as Q, Guirao et al. 1997; Q biotype displaced B when insecticide selection occurred, Horowitz et al. 2005). Since then, many reports have shown similar changes in biotypes/species of B. tabaci elsewhere, apparently due to frequent use of insecticides and development of insecticide resistance. Since 2005, a shift of biotype B to Q occurred in many locations of China (e.g., Teng et al. 2010; Li et al. 2017). An opposite process has been observed in Israel, where since 2009, a significant shift in the biotype ratios has been observed: the B biotype replaced the Q biotype in most crops. At the same time, resistance to pyriproxyfen was reduced considerably. The reason for this phenomenon is not clear, but it may relate to using less pyriproxyfen and neonicotinoids (Crowder et al. 2011; Horowitz and Ishaaya 2014). In addition, biotype Q prefers protected crops (Kontsedalov et al. 2012) as also reported from the USA and Italy (Mckenzie et al. 2012; Parrella et al. 2012).

This paper reviews insecticide resistance and management issues among B. tabaci species with a focus on studies published mainly within the past decade.

Insecticide resistance in Bemisia tabaci species

Insecticide resistance in B. tabaci is widespread, and it has evolved to most of the insecticides used (Basit 2019). According to Mota-Sanchez and Wise (2019) (Arthropod Pesticide Resistance Database, Michigan State University), there are so far approximately 650 reported cases of insecticide resistance in the genus Bemisia, and resistance was detected to more than 60 active ingredients.

The mechanisms of resistance in B. tabaci are similar to those described for other pest species, i.e., metabolically driven by elevated levels of detoxification enzymes or by point mutations resulting in target-site resistance.

Table 1 summarizes the global distribution of resistance to insecticides in species/biotypes of B. tabaci according to recent reports from various countries. Both MED (Q) and MEAM1 (B) species have developed resistance to most insecticide classes; however, where both species are available side by side, MED has developed higher resistance to many insecticides than MEAM1 (e.g., Yao et al. 2017; Luo et al. 2010 in China; Kontsedalov et al. 2012; Horowitz and Ishaaya 2014 in Israel). In India, the species Asia I and Asia II-1 were found more resistant to insecticides than Asia II-7 (Naveen et al. 2017).

Table 1 Recent reports of resistance to insecticides in Bemisia tabaci species/biotypes
Full size table

Resistance to different chemical classes of insecticides

Organophosphates (OPs) and carbamates

Resistance to organophosphates (OPs) is well established in B. tabaci in many countries (Horowitz et al. 2007; Ahmad et al. 2010; Naveen et al. 2017). In some cases, levels of resistance to OPs and carbamates were unstable and fluctuated from very low to high (Ahmad et al. 2010). In Turkey, resistance in biotype B (MEAM1) to OPs ranged between 20- and 310-fold (Erdogan et al. 2008). In Greece, the resistance level to pirimiphos-methyl was reported to be higher in greenhouses compared with open fields (Roditakis et al. 2009). High resistance to OPs such as acephate and triazophos was detected in Asia 1 whiteflies from India (Roy et al. 2019). In China, relatively low level of resistance to an OP (chlorpyrifos) was detected; however, initial baseline-level toxicity was rather high (Wang et al. 2017). Similarly, in the Q biotype of B. tabaci, from eastern China, low resistance to another OP (dichlorvos) as well as to the carbamate carbosulfan was exhibited (Yuan et al. 2012).

Resistance levels to methomyl (a carbamate) were shown to be low to moderate in MED strains from Spain, probably due to less frequent use and the adoption of IPM strategies (Fernandez et al. 2009).

The mechanisms of resistance to OPs and carbamates in B. tabaci are known for many years and have been studied since the 1980s; however, no substantially new results have been published over the past decade. Altered sensitivity alleles of acetylcholinesterase, the target site for OPs, have been described, and several levels of resistance are attributed to varying numbers of such alleles (Byrne and Devonshire 1993, 1997; Byrne et al. 1994). The insensitivity to OPs has also been linked to additional mechanisms of resistance such as increased esterase activities (Byrne and Devonshire 1991; Denholm et al. 1998) and was correlated with the levels of resistance (Dittrich et al. 1990). Alon et al. (2008) have shown that altered AChE sensitivity to OPs is linked to a F392W mutation in acetylcholinesterase 1 of B. tabaci. However, in the same study, overexpression of the carboxylesterase 1 gene was also correlated with chlorpyrifos resistance, suggesting that both mechanisms are involved in resistance to OPs (Alon et al. 2008).

Pyrethroids

Pyrethroid resistance in whiteflies is widespread although the magnitude and pattern of resistance and cross-resistance vary considerably among countries and cropping systems (Cahill et al. 1995, 1996; Denholm et al. 1996; Erdogan et al. 2008; Roditakis et al. 2009; Naveen et al. 2017). In some cases, very high resistance was detected to pyrethroids such as cypermethrin and bifenthrin in populations of B biotype from northwestern China (Ma et al. 2007) and Cyprus (Vassiliou et al. 2011). In other regions of China, resistance levels to pyrethroids, e.g., lambda-cyhalothrin and cypermethrin, have been declined also in Biotype Q (Yuan et al. 2012; Yao et al. 2017).

Pyrethroids target the para-type voltage-gated sodium channel (vgsc) in the central nervous system, leading to paralysis and rapid death. The two mutations L925I and T929V in the IIS4-5 linker of vgsc in B. tabaci were linked to pyrethroid resistance (Schuler et al. 1998; Lee et al. 2000; Morin et al. 2002; Bass et al. 2004; Roditakis et al. 2006; Alon et al. 2008; Farghaly 2010a). DNA microarrays were later used for resistance monitoring of field-collected populations based on the mutations in vgsc as well as acetylcholinesterase (Chung et al. 2011). In this study, high correlation was obtained between the microarray and direct sequencing, providing a large-scale tool for resistance monitoring in B. tabaci. Such molecular monitoring of resistance in B. tabaci has been used by others to detect resistance to pyrethroids, carbamates and OPs (Farghaly 2010b). Based on the molecular data obtained from resistant and susceptible populations, and the fact that the previously described mutations are stable in field populations, a simple PCR–agarose gel visualization-based assay was developed for reliably monitoring the frequency of the mutations known to confer resistance to pyrethroids and OPs. Results from larger monitoring campaigns revealed that this method is accurate and robust to reliably diagnose the spread of the respective resistance alleles (Tsagkarakou et al. 2009).

Resistance to pyriproxyfen and buprofezin

Resistance in B. tabaci to the Insect Growth Regulators (IGRs), pyriproxyfen and buprofezin has been reported widely from many countries (e.g., Horowitz et al. 2005, 2007; Erdogan et al. 2008; Crowder et al. 2008; Fernandez et al. 2009; Li et al. 2012; Basit et al. 2013; Horowitz and Ishaaya 2014; Roy et al. 2019).

Pyriproxyfen is a potent juvenile hormone (JH) mimic affecting the hormonal balance in insects, suppressing embryogenesis, metamorphosis and adult formation. It has been considered a leading insecticide for controlling whiteflies (Ishaaya and Horowitz 1995; Horowitz et al. 2005; Crowder et al. 2008; Castle et al. 2010), especially against biotype B. Both pyriproxyfen and buprofezin were considered harmless to natural enemies as compared with conventional insecticides. Naranjo et al. (2004) suggested that these selective IGRs can be used in an effective integrated control system for B. tabaci. However, its widespread use has resulted in resistance development in Israel since the 1990s (Horowitz et al. 1994; Horowitz et al. 2002, 2005). To delay resistance in B. tabaci, the use of pyriproxyfen and buprofezin, especially in cotton fields, was restricted to one application per a cotton season in most Insecticide Resistance Management (IRM) programs, but resistance to these IGRs has evolved and in some cases the use of pyriproxyfen and buprofezin was decreased because of the resistance (ARH, personal communication). Cases of strong resistance to pyriproxyfen have been associated with the Q rather than the B biotype (Horowitz et al. 2002, 2005; Dennehy et al. 2005; Horowitz and Ishaaya 2014). In Israel, since 2009, a significant shift in the biotype ratios has been observed: the B biotype has become predominate over the Q. At the same time, resistance to pyriproxyfen declined considerably (Crowder et al. 2011; Horowitz and Ishaaya 2014). However, simulation models conducted with the B biotype have demonstrated that resistance to pyriproxyfen in this biotype can be managed through modification of operational and environmental factors that can be controlled by the growers (Crowder et al. 2008, 2013; Li et al. 2012).

A study conducted in Arizona, where pyriproxyfen served as a major compound for controlling B. tabaci in cotton for over a decade, showed that resistance to this compound increased steadily, and synergism bioassays demonstrated that the increasing resistance to pyriproxyfen was correlated with elevated levels of cytochrome P450 monooxygenases (P450s) and glutathione S-transferases (GSTs) (Ma et al. 2010).

A study conducted with B. tabaci MED species employed the DNA microarray technology to compare gene expression levels in pyriproxyfen-resistant and -susceptible populations showed that in the resistant strain many genes implicated in xenobiotic detoxification are upregulated, such as P450s (Ghanim and Kontsedalov 2007), indicating that the resistance to pyriproxyfen could be metabolic. Another study using a recombinantly expressed CYP6CM1, a P450 upregulated in neonicotinoid- and pymetrozine-resistant strains of B. tabaci, demonstrated oxidative metabolism by the hydroxylation of pyriproxyfen (Nauen et al. 2015b), thus confirming the potential involvement of P450s in pyriproxyfen resistance.

Resistance to neonicotinoids

Neonicotinoids are among the most effective groups of insecticides for whitefly control. They exhibit systemic and translaminar properties and high residual activity (Takahashi et al. 1992; Elbert et al. 1998; Horowitz et al. 1998). They act especially against sucking insects such as whiteflies, aphids, leafhoppers and various coleopteran pests.

There have been a few review papers summarizing the global aspects of resistance to neonicotinoids (e.g., Nauen and Denholm 2005; Bass et al. 2015); hence, just some important recent studies will be considered below.

In many cases, resistance to neonicotinoids was associated with the Q biotype (e.g., Nauen et al. 2002; Horowitz et al. 2004; Roditakis et al. 2009; Dennehy et al. 2010; Luo et al. 2010), although a few cases of neonicotinoid resistance have been described also in B-biotype strains (Byrne et al. 2003; Schuster et al. 2010; Wang et al. 2010).

Low to moderate levels of resistance to the neonicotinoids imidacloprid and thiamethoxam were detected in Brazil (Silva et al. 2009), whereas in Florida, USA, high levels of resistance to imidacloprid and thiamethoxam were detected in biotype B of B. tabaci (Schuster et al. 2010). In Israel, resistance level in Q biotype to thiamethoxam was high and to imidacloprid and acetamiprid was moderate; Q biotype populations have taken over B in crops grown in protected conditions, where resistance outbreaks usually develop after several insecticide applications (Kontsedalov et al. 2012). In Cyprus, moderate to high levels of resistance were detected to imidacloprid (77–392-fold) and thiamethoxam (50–164-fold), but low resistance levels were observed to acetamiprid (Vassiliou et al. 2011). In Crete, very high resistance levels were detected in various whitefly populations for imidacloprid (38–1958-fold). A strong correlation between resistance to imidacloprid and the number of applications with neonicotinoids was observed (Roditakis et al. 2009). Recently, most of the B. tabaci populations in Turkey were found to be resistant to neonicotinoids with resistance levels up to 2060-fold for imidacloprid, while resistance to thiamethoxam was low (Satar et al. 2018). In Pakistan, neonicotinoid resistance increased in B. tabaci (the biotype was not defined) following intensive use leading to field failures (Ahmad and Khan 2017). In India, high resistance to neonicotinoids in several field populations of B. tabaci was detected, especially in Asia I and Asia II-1 strains (Naveen et al. 2017). Reports from China pointed out that the increase in resistance to neonicotinoids was mainly in biotype Q. While biotype B remained susceptible to acetamiprid, imidacloprid and thiamethoxam, field strains of biotype Q expressed moderate to high resistance to these insecticides (Luo et al. 2010). In southeastern China, moderate to high levels of resistance were detected in both B and Q biotypes to two neonicotinoids (28–1900-fold to imidacloprid, 29–1200-fold to thiamethoxam) (Wang et al. 2010). In eastern China, some field strains (especially Q biotype) exhibited low to high resistance to two neonicotinoids (imidacloprid and nitenpyram) (Yuan et al. 2012). A recent study conducted in three regions of China with B. tabaci Q collected from vegetables in 2011–2013 revealed low to high resistance to neonicotinoid insecticides (Wang et al. 2017). In southeast coast of China, resistance to neonicotinoids in the Q biotype was unstable in open fields, but increased constantly in protected areas (Yao et al. 2017).

Neonicotinoids target the insect nicotinic acetylcholine receptor (nAChR) in the central nervous system and disrupt nerve transmission leading to paralysis and death within short time (Tomizawa and Casida 2005). As the affinity of these compounds to mammalian nAChRs is very low, and some could be applied and taken up systemically by plants such as imidacloprid, or can by directly treated to seeds, they became very popular, and management programs heavily relied on using neonicotinoids (Jeschke et al. 2011). Enhanced detoxification is reported as the main mechanism for conferring resistance against imidacloprid in strains of both B. tabaci MEAM1 and MED (Nauen et al. 2002; Rauch and Nauen 2003). Karunker et al. (2008) have shown by measuring the expression of 11 P450 genes that CYP6CM1 overexpression was tightly associated with imidacloprid resistance. It was also shown that heterologously expressed CYP6CM1 could metabolize imidacloprid and other neonicotinoids in vitro (Karunker et al. 2009) and that its expression and protein level is correlated with the degree of resistance in field-collected populations (Roditakis et al. 2011). A recent computational study suggested that lower levels of dinotefuran resistance in such whitefly strains are due to differences in binding to CYP6CM1 (Meng et al. 2016), a finding validated for the new butenolide insecticide flupyradifurone and the sulfoximine insecticide sulfoxaflor, both not belonging to the neonicotinoids, but targeting insect nAChRs (Jeschke et al. 2015; Nauen et al. 2015a). Nevertheless, this enzyme has the potential to be used for the screening of field populations for resistance against imidacloprid using diagnostic tools such as ELISA (Nauen et al. 2015a). A predominantly metabolic mechanism of resistance was also confirmed by work conducted by Feng et al. (2010) in China. In this study, a thiamethoxam-resistant population was cross-resistant to other neonicotinoids. Synergism assays revealed that the inhibition of P450s strongly synergized neonicotinoid efficacy, a finding supported by increased enzyme activity in resistant strains (Feng et al. 2010). Metabolically based neonicotinoid cross-resistance has also been reported from other parts of China (Wang et al. 2009). Similar results were reported from Turkey, where field-collected populations of B. tabaci showed high levels of resistance to different neonicotinoids driven by metabolic mechanisms (Satar et al. 2018).

Recently, B. tabaci resistance to insecticides, especially neonicotinoids, has been increasingly investigated by employing RNAseq analysis to screen for (less obvious) mechanisms of resistance. Such experiments also enrich the available datasets of genes, gene expression data and pathways involved in resistance. A study conducted on the MED species of B. tabaci used RNAseq analyses to profile the expression patterns of different detoxification genes including P450s, GSTs and carboxylesterases, as potential candidate genes contributing to insecticide resistance (Ilias et al. 2015). The study demonstrated the overexpression of P450s from the CYP2, CYP3 and CYP4 clades, with CYP6CM1 being the major player. Interestingly, in this study, ten unigenes-encoding nAChRs subunits were identified, but none of those showed polymorphism that could be linked to neonicotinoid resistance when compared to a susceptible reference strain (Ilias et al. 2015).

Ketoenols

Ketoenols are a relatively new class of insecticides and known as derivatives of tetronic acids (spiromesifen) and tetramic acids (spirotetramat). Both compounds are active against whiteflies and act as inhibitors of lipid biosynthesis by targeting acetyl-CoA carboxylase, thus being particularly active against juveniles, but also affecting female fecundity (Bretschneider et al. 2003; Nauen et al. 2005). Several reports have indicated the absence of cross-resistance between spiromesifen and other major commonly used insecticides from different chemical groups such as neonicotinoids and pyriproxyfen (Nauen and Konanz 2005; Prabhaker et al. 2008; Kontsedalov et al. 2009). Spirotetramat is a systemic insecticide with phloem and xylem mobility for the control of a broader spectrum of sucking insects, including aphids, whiteflies, psyllids and scales. Similar to spiromesifen, it is particularly effective against juvenile stages and it significantly reduces fecundity and fertility of B. tabaci females (Brück et al. 2009).

Fernandez et al. (2009) reported low resistance level to spiromesifen (1- to sevenfold) in populations of Q biotype collected in southeastern Spain, and Roy et al. (2019) found in India low to moderate resistance (8- to 32-fold) to this insecticide. However, recently, several field strains that were assayed in Spain for resistance to these two insecticides exhibited very high resistance to spiromesifen (> 10,000-fold) and cross-resistance to spirotetramat, but to a much lower extent (130-fold) (Bielza et al. 2019).

Diamides

Diamide insecticides represent the most recent class of chemistry introduced to the market approximately 13 years ago (Nauen and Steinbach 2016). Five diamide insecticides, i.e., the phthalic diamide, flubendiamide and the anthranilic diamides chlorantraniliprole, cyclaniliprole, tetraniliprole and cyantraniliprole, have so far been commercialized. Flubendiamide and chlorantraniliprole are potent against lepidopteran pests, while cyantraniliprole also targets sucking pests such as whiteflies and aphids (Sattelle et al. 2008; Lahm et al. 2009). These compounds act on insect ryanodine receptors, large tetrameric calcium release channels located in neuromuscular tissues.

Studies on the molecular mechanisms of diamide resistance in lepidopteran pests, especially the diamondback moth Plutella xylostella and the tomato leaf miner Tuta absoluta, have revealed RyR target-site mutations with strong functional implications for diamide binding, while metabolic mechanisms of resistance based on elevated levels of detoxification enzymes were not sufficiently studied (Nauen and Steinbach 2016).

In B. tabaci, a short time after cyantraniliprole use in China, low to moderate resistance has evolved to this diamide, especially in the Q biotype (MED) of B. tabaci (Yao et al. 2017; Wang et al. 2018), whereas in European countries such as Spain, Italy and Greece no variation in susceptibility to cyantraniliprole was detected yet (Gravalos et al. 2015).

Other insecticides

Other important insecticides frequently used to control B. tabaci include pymetrozine, a transient receptor protein vanillin (TRPV) channel modulator of chordotonal organs. However, pymetrozine cross-resistance has been described in neonicotinoid-resistant strains of both B and Q biotype whiteflies from different regions worldwide (Gorman et al. 2010). The cross-resistance is mainly driven by the overexpression of CYP6CM1 as shown by another study showing the hydroxylation of pymetrozine by functionally expressed CYP6CM1 (Nauen et al. 2013, 2015b).

Bemisia tabaci resistance management

The most common solutions to control B. tabaci pest attacks have been insecticides, because of their efficacy and convenience (e.g., Palumbo et al. 2001; Horowitz et al. 2011). However, using insecticides alone is harmful to natural enemies and the environment, and in addition, intensive use of chemical insecticides results in development of resistance with striking phenotypes that may jeopardize pest control efficacy.

There are a number of major principles for successful resistance management at a technical level to be followed in chemical control, including (a) insecticides should be used according to label recommendations; (b) select insecticides based on known local efficacy and selectivity (IPM); (c) rotate insecticides from different Modes of Action (MoAs) employing a ‘MoA treatment windows’ approach; and (d) nonchemical control methods should be incorporated (IPM). The entire above are essential for the successful implementation of IRM strategies (Table 2). However, a nontechnical parameter that can affect the success of resistance management schemes is the understanding of the resistance mechanisms to avoid cross-resistance issues compromising a developed IRM strategy. Ideally, IRM is supported by educational courses and communication plans as advocated by the Insecticide Resistance Action Committee (IRAC) (Sparks and Nauen 2015).

Table 2 Current statuses and future prospects of alternative whitefly control methods implemented in integrated and/or biological pest management schemes (see text for details)
Full size table

“Window” programs—rotation of modes of action and insecticide applications

It has been demonstrated that selection pressure enforced by the frequent use of insecticides is the main driving force for the development of resistance via the gradual selection of the individuals carrying the resistant alleles (Georghiou and Lagunes-Tejeda 1991; Denholm and Rowland 1992). However, applying the same insecticide MoA frequently in sequence, within a crop cycle, was a very common practice, particularly for novel and highly effective products. The resistance selection process can be interrupted by using insecticides of different MoAs based on IRAC’s MoA classification scheme (Sparks and Nauen 2015). The rationale behind this strategy is that insecticides of different modes of action usually select for different resistance mechanisms (Sparks and Nauen 2015). Cross-resistance exceptions to the aforementioned rule have been demonstrated, e.g., neonicotinoids and pymetrozine (Gorman et al. 2010; Nauen et al. 2013). In addition, the development of a multiple resistance cannot be excluded if selection pressure is of extreme level (Roditakis et al. 2005). Thus, it is essential to take into account all available information when a rotation of insecticides of different MoAs is designed. In addition, selecting the most appropriate chemical from available, officially registered products depends on various parameters such as the crop stage, post-harvest interval, use of beneficial/pollinators in the crop, the infestation level, the presence of other coexisting pests and resistance history in the crop. A list of available MoAs and chemicals that could be used in rotation schemes for whitefly control is provided in Table 3.

Table 3 Insecticide modes of action and chemical classes for whitefly resistance management; the availability of different chemical classes depends on regional registrations and therefore varies (MoA classification according to IRAC (Sparks and Nauen 2015)
Full size table

The most widely followed MoA rotation approach in IRM is that suggested by IRAC (www.irac-online.org), namely the ‘MoA treatment windows’ approach, where several rules apply for the proper implementation of the particular rotation scheme. The basic aim of the IRAC strategy is to avoid treating consecutive generations of the target pest with insecticides of the same MoA. Multiple applications with chemicals of the same MoA are allowed within a generation ‘window.’ As the generation time for B. tabaci ranges between 24 and 30 days, a generation ‘window’ is set to 30 days for simplicity. Additional required applications beyond the 30-day window should be performed with insecticides of a different MoA. A compound with a specific MoA should not be reused, unless a 60-day interval is allowed (i.e., approximately two generations). In addition, all applications should strictly follow the product label with regard to the rate, the target pest, the method and number of applications.

Insecticide mixtures

Application of insecticide mixtures was used extensively for controlling whiteflies as a tactic for managing insecticide resistance in B. tabaci. (Horowitz and Ishaaya 1996; Denholm et al. 1998; Castle et al. 2002). This approach was based on mixing chemicals of different MoAs lacking cross-resistance (Denholm and Rowland 1992; Horowitz and Ishaaya 1996) that could delay resistance development, because mechanisms required to resist both insecticides simultaneously commonly exist in scarcity in a pest population (Georghiou 1994). Unfortunately, the intensive use of synergized insecticides, particularly of OPs and pyrethroids for whitefly control (Denholm et al. 1998), resulted in high resistance levels to both chemicals and major pest control failures (Dennehy and Williams 1997). The insecticide mixtures approach has been thoroughly investigated in numerous pest systems and still remains controversial since several assumptions pertain in each case, dictating the overall success of the method (Cloyd 2010; South and Hastings 2018). The Insecticide Resistance Action Committee (IRAC) provides more detailed information on the use of insecticide mixtures and their value in IRM and pest control in general (refer to www.irac-online.org). Despite the extensive discussion on this topic, the use of insecticide mixtures is still wildly adopted in B. tabaci management.

Sustainable IPM approaches

Whitefly control can rely on various methods alternative or complementary to chemical insecticides. Prevention methods such as insect proof netting on greenhouse ventilation openings, UV-blocking films (Monci et al. 2004; Chiel et al. 2006; Horowitz et al. 2011; Monci et al. 2019), reflective mulches (Greer and Dole 2003; Simmons et al. 2010; Rajasri et al. 2011) or ground cover crops (Hilje and Stansly 2008) have been adopted to varying extent. Novel approaches such as the use of supplementary UV radiation (Prieto-Ruiz et al. 2019) may also be a promising addition in the immediate future. Mass trapping with sticky traps has been used extensively, in various forms, having as basis of yellow-colored sticky surfaces (Lu et al. 2012); however, sticky traps are also important tools for whitefly population monitoring (Gerling and Horowitz 1984).

Entomopathogenic fungi have been suggested for whitefly control (Lacey et al. 1999; Wraight et al. 2000; Cuthbertson and Walters 2005); however, this approach was adopted to a limited extent in practice. Nonetheless, recent progress may provide novel tools and a larger market share (Garrido-Jurado et al. 2017; Anwar et al. 2018; Jaber et al. 2018; Santos et al. 2018; do Nascimento Silva et al. 2019) without the adverse effect of resistance development (Gao et al. 2017). One of the major principles of IPM programs is the use of natural enemies, such as predators and parasitoids (Gerling et al. 2001; Horowitz et al. 2011). Numerous predators have been reported praying on whiteflies, in which the phytoseiid mite Amblyseius swirskii (Athias-Henriot) can be considered among the most important. Its introduction to the market has changed the balance of plant protection practices against B. tabaci in favor of IPM (Nomikou et al. 2001; van der Blom et al. 2008; Calvo et al. 2009, 2012). Mirid bugs like Nesidiocoris tenuis (Reuter) and Macrolophus sp have been introduced as generalist predators for many pests including B. tabaci (Alomar et al. 2006; Arnó et al. 2010). Parasitoids are also key biocontrol agents, playing a major role in IPM for whiteflies. Among others, aphelinids Encarisa sp and Eretmocerus sp have been successfully incorporated in IPM schemes (Foltyn and Gerling 1985; Heinz and Nelson 1996; Van Lenteren et al. 1997; Qiu et al. 2004).

In field crops, it was demonstrated that the conservation of natural enemies is a key element in IPM programs, since they serve as efficient factors for the control of B. tabaci (Naranjo and Akey 2005; Naranjo and Ellsworth 2009a; Vandervoet et al. 2018; Togni et al. 2019). Several years back, the cotton crops served as a model, where the concept of natural enemies’ conservation was conceived and implemented, altering the pest status of whiteflies in the cotton growing system of Arizona (Naranjo et al. 2002; Naranjo and Ellsworth 2009b). The idea of conservation was also adopted, with modifications, in greenhouse crops, by modifying the flora surrounding greenhouses (Rodríguez et al. 2018, Roditakis pers. comm.).

Essential oils and plant extracts have been extensively investigated for their activity on B. tabaci (Kim et al. 2011; Baldin et al. 2013; Deletre et al. 2016; Vite-Vallejo et al. 2018; Wagan et al. 2018; Cruz-Estrada et al. 2019); however, their use is currently limited. Biotechnological insecticides based on RNA interference (RNAi) that specifically silence the function of vital genes can serve as potential novel pest management tools, though not yet technically feasible (Ghanim et al. 2007; Upadhyay et al. 2011). However, the proof of concept has been provided (Malik et al. 2016; Luo et al. 2017) and several studies demonstrate promising results (Raza et al. 2016; Vyas et al. 2017).

Many of the aforementioned approaches are key element of sustainable IPM schemes that promote alternative pest management tactics and result in substantial reduction of pest pressure and subsequent reduction of insecticide applications making implementation of rational IRM possible.

Farmer education

Scientific evidence of insecticide resistance and IRM schemes can only be useful and contribute to changes in the actual agricultural practice if socioeconomic factors that are occasionally ignored are wisely managed (FAO 2012). These factors include concerns about the cost, the necessity of suggested alterations, the feasibility from a technical perspective and overall a thorough education on resistance management tactics along with its implications in crop protection (FAO 2012). An exceptional example of farmer-level adoption of an IPM program for whiteflies is the case of Arizona. The initiative was driven by governmental officials and academia with great agroecological and financial benefits for the agricultural industry (Naranjo and Ellsworth 2009b). Resistance monitoring is essential for early detection of incipient resistance cases (Ellsworth et al. 2013); of course, this information alone cannot reverse the increasing trend of resistance. The resistance monitoring data should serve as a basis to develop a sustainable resistance management strategy followed by all stakeholders. It is more than evident that acceptance of any IRM strategy at the farmer level is essential for its successful implementation in the management of any pest, including B. tabaci.

Conclusion

This paper reviews insecticide resistance and management issues among species of the serious crop pest, B. tabaci, focusing mainly on studies published in the past decade. At present, the use of insecticides is the main approach employed to manage B. tabaci populations because of their efficacy and convenience. This practice is considered problematic due to both environmental concerns and the widespread insecticide resistance that B. tabaci has developed.

Bemisia tabaci has evolved resistance to insecticides from most chemical classes including new insecticides. Among the common cryptic species, MED is considered more resistant than the MEAM1 to insecticides such as pyriproxyfen and neonicotinoids; however, in recent years there are other species of B. tabaci including MEAM1, Asia I and Asia II-1 that have developed high resistance levels to various groups of insecticides. The mechanisms of resistance in B. tabaci are similar to those that have been described from many other pest species, and they are generally classified as metabolic, involving esterase-, glutathione S transferase (GST)- or P450 monooxygenase-based detoxification, or point mutations in the target site. Advanced methods based on the molecular and gene sequence data obtained from resistant and susceptible field-collected B. tabaci populations resulted in a better understanding of resistance mechanisms in this pest.

There are several components of IPM-IRM programs applicable to managing the resistance in B. tabaci, namely chemical control with selective insecticides, rotation of MoAs, insecticide mixtures, reducing chemical insecticide applications and nonchemical control methods using IPM practices (e.g., biological control, crop plant resistance and physical/mechanical methods). It is hoped that the integration of these methods will contribute to improving the management of the pest, thus helping to guarantee sustainable yields in the future.

Author contributions

ARH wrote the first draft and assembled all co-authors. ARH, MG, ER, RN and II all contributed equally to the formation of the outline and writing the content of this review.