Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), are one of the most-destructive insect pests of greenhouse-grown horticultural crops, including vegetables and ornamentals (Helyer and Brobyn 1992, Jensen 2000a, Kirk and Terry 2003, Lewis 1997,). Direct plant damage associated with western flower thrips is a consequence of their feeding. Western flower thrips possess piercing-sucking mouthparts that are used to obtain nutrients from plant cells (Harrewijn et al. 1996), which can result in cell death and leaf or flower deformation and can negatively impact marketability due to a decreased aesthetic value (Childers 1997, Chisholm and Lewis 1984, Jensen 2000a). Indirect damage is affiliated with adult transmission of the tospoviruses, Impatiens necrotic spot or Tomato spotted wilt virus, which reduce crop aesthetic values and marketability (Allen and Broadbent 1986, Pappu et al. 2009, Wijkamp et al. 1995). Therefore, due to direct and indirect damage, greenhouse producers have minimal tolerance for this insect pest. Consequently, insecticides are the primary means of suppressing western flower thrips populations in order to mitigate any direct and/or indirect damage (Allen et al. 1993, Cloyd 2009a, Gao et al. 2012, Parrella 1995, Parrella and Murphy 1996). Insecticides, however, may be ineffective in dealing with western flower thrips populations because eggs are inserted into leaf tissues, and pupae are typically located in the growing medium, which protects these life stages from exposure to insecticides (Mound 1996, Reitz 2009). The natural behavior of western flower thrips, where individuals reside in concealed, enclosed areas on plants such as unopened terminal or flower buds, may reduce or limit direct exposure to spray applications of contact insecticides (Hansen et al. 2003, Jensen 2000a, Zhang et al. 2008). In addition, and most importantly, western flower thrips populations have developed resistance to many insecticides (Broadbent and Pree 1997, Gao et al. 2012, Helyer and Brobyn 1992, Immaraju et al. 1992,). Therefore, this paper will focus on two topics related to the use of insecticides against western flower thrips: (a) insecticide resistance and (b) strategies that may mitigate insecticide resistance developing in western flower thrips populations.

Insecticide Resistance

Western flower thrips feed on a range of greenhouse-grown horticultural crops, which increases their exposure to insecticide applications, even insecticides targeting other insect or mite pests. As a result, western flower thrips have a high propensity for developing resistance to different insecticides (Jensen 2000a). The intense selection pressure placed on western flower thrips populations due to frequent applications of insecticides exacerbates the potential for resistance to develop. In addition, natural populations of western flower thrips may already possess resistant alleles at low frequencies before exposure to insecticides. The possession of pre-existing resistant traits increases the likelihood for resistance to develop in western flower thrips populations (Roush and McKenzie 1987). Furthermore, multiple generations per year in greenhouses increases the possibility of western flower thrips populations developing resistance to insecticides (Immaraju et al. 1992). The intensive use of insecticides removes susceptible individuals from the population, consequently increasing the proportion or frequency of individuals with resistant genotypes (Gao et al. 2012). Therefore, excessive use of insecticides will induce rapid development of resistance due to selection pressure for resistant individuals (ffrench-Constant and Roush 1990).

The first case of western flower thrips resistance to insecticides was reported in 1961 when the chlorinated cyclodiene, toxaphene, was found to be ineffective in suppressing populations of the western flower thrips (Race 1961). Although there have been subsequent instances of reduced efficacy of insecticides against western flower thrips, the first actual record affiliated with resistance occurred almost 30 years later (Robb 1989). Worldwide there are currently 153 documented cases associated with western flower thrips populations that are resistant to insecticides in at least seven chemical classes (Arthropod Pesticide Resistance Database, Michigan State University, East Lansing, MI, http://www.pesticideresitance.org; accessed November 2015). Furthermore, differences in resistance may occur between the “lupin” and “greenhouse” strains of western flower thrips (Martin and Workman 1994). Western flower thrips populations are continually exposed to pesticide applications intended to target other pests such as aphids, whiteflies, and mites affiliated with multiple-pest complexes (Hussey 1965, Diabate et al. 2002), thus increasing the rate of resistance development to specific pesticides (Reitz et al. 2003). Another concern is that label rates of pesticides (insecticides and miticides) often vary depending on the specific pest; therefore, a label rate for western flower thrips may be lower or higher than that for other pests, which could possibly enhance the development of resistance due to increased exposure to different pesticides.

There is a well-substantiated hypothesis that only using insecticides to deal with western flower thrips populations in greenhouse production systems will eventually lead to populations developing resistance (Georghiou 1986). The rate of resistance development in western flower thrips populations is primarily associated with three biological parameters: (a) rapid (short) generation time, (b) high female reproductive capacity (fecundity), and (c) a haplo-diploid breeding system (Bielza et al. 2008, Brodsgaard 1989, Denholm et al. 1998, Hou et al. 2014, Jensen 1998, 2000a, Reitz 2009). The rapid generation time allows for multiple generations to be present simultaneously during a crop production cycle (Gaum et al. 1994, Gerin et al. 1994), with generations overlapping continuously. As a result, females can mate with resistant progeny (off-spring) that subsequently increases the frequency of resistant alleles in a population (Immaraju et al. 1992). Individuals that survive exposure to an insecticide may pass on resistant traits to the next generation, thus enriching the gene pool with resistant genes (Jensen 2000a). A high female reproductive capacity or fecundity means that females lay between 150 and 300 eggs during their 45-day lifespan (Gerin et al. 1999), which potentially increases the number of individuals in subsequent generations that are exposed to insecticides.

A haplo-diploid breeding system involves resistant genes in males (haploid with one set of chromosomes) that are directly exposed to selection after an insecticide application, which accelerates the rate of resistance development. Certain genes/alleles associated with resistance are fully expressed in haploid males whereas completely diploid (double set of chromosomes) individuals may only possess resistance if affiliated with recessive or codominant traits (Carrière 2003, Denholm et al. 1998). Therefore, selection for resistance is enhanced in haploid individuals as compared to diploid individuals.

The extensive movement of plant material, both regionally and internationally, has increased problems with western flower thrips populations (Brodsgaard 1994). Moreover, the development of insecticide resistance is an international issue, as resistant genes/alleles associated with western flower thrips populations can be spread through international trade of plant material from off-shore facilities that utilize insecticides against western flower thrips, which, in some cases, are not registered for use in the United States (R.A.C. pers. obs.). Furthermore, the international trade of moving plant material from one country to another may indiscriminately spread western flower thrips populations. In addition, the international trade of plant material may indirectly spread populations (or variants) of western flower thrips with resistant genes/alleles or specific resistance mechanisms (Denholm and Jespersen 1998), which could consequently exacerbate the problem of insecticide resistance (Jensen 2000a). Therefore, mitigating western flower thrips resistance must be dealt with on a global scale involving collaborations among countries (Zhang et al. 2008), which may dictate the need to monitor for and possibly restrict the movement of plant material infested with western flower thrips. Moreover, it will be necessary to obtain records of insecticides used 2 weeks prior to shipping so that greenhouse producers can avoid using similar insecticides once plants are incorporated into production systems. Although the Animal and Plant Health Inspection Service already deals with screening international imports of insects and plants, the problem is that when plant material is received, inspections only account for approximately 10% of all imports due to labor demand and the large quantity of imports. Furthermore, in some countries, phytosanitary regulations are completely absent (Herrick pers. comm.).

One hypothesis is that the absence of susceptible individuals immigrating into western flower thrips populations enhances resistance development (Bielza et al. 2008). However, the presumption is that individuals of wild, field populations of western flower thrips immigrating into greenhouses are actually susceptible (no insecticide resistance) and will breed with resistant individuals, thus delaying resistance by diluting the gene pool of resistant individuals (Georghiou and Taylor 1977). In addition, breeding with resistant individuals will reduce the frequency of resistant alleles in the population (Jensen 2000a) which assumes, however, that the population of individuals immigrating is in fact not resistant to insecticides. Nevertheless, many insecticides used in greenhouse production facilities are initially introduced for use in agricultural cropping systems (R.A.C. pers. obs.). Therefore, immigrating individuals may, in fact, possess resistant alleles or they may not (Jensen 2000a). Moreover, immigration of resistant individuals exposed to insecticides used in agricultural cropping systems may increase the rate at which resistance develops to insecticides registered for use in greenhouses (Immaraju et al. 1992).

Insecticide resistance is prevalent in many western flower thrips populations worldwide and, as noted above, the extensive use of insecticides over the years has led to certain western flower thrips populations developing resistance to insecticides in seven chemical classes including organophosphate (e.g., diazinon and acephate) (Brodsgaard 1994, Zhao et al. 1994), carbamate (e.g., bendiocarb, methiocarb, and methomyl) (Jensen 1998, Zhao et al. 1995a), pyrethroid (e.g., fenvalerate, cypermethrin, and bifenthrin) (Herron and Gullick 2001, Zhao et al. 1995b), neonicotinoid (e.g., imidacloprid) (Herron and James 2005, Zhao et al. 1995c), spinosyn (e.g., spinosad) (Herron and James 2005, Loughner et al. 2005), macrocycle lactone (e.g., abamectin) (Immaraju et al. 1992, Kontsedalov et al. 1998), and pyrazole (e.g., fipronil) (Herron and James 2005). The means by which western flower thrips populations develop resistance is associated with certain resistance mechanisms.

The resistance mechanisms affiliated with western flower thrips populations include enhanced metabolic detoxification and target site modifications (Brodsgaard 1994, Espinosa et al. 2005, Herron and James 2005, Jensen 2000a, Zhao et al. 1995b). In regard to metabolic detoxification, there are three primary enzyme systems involved including esterases, glutathione S-transferases, and cytochrome P-450 mono-oxygenases (Maymo et al. 2002, Soderland and Bloomquist 1990). The main function of these enzyme systems is to convert hydrophobic (water-hating) compounds, such as insecticides, into less-biologically active compounds that are hydrophilic (water-loving) and are subsequently removed during excretion (Jensen 2000a). In addition to enhanced metabolic detoxification, insensitive acetylcholinesterase has been implicated as a resistance mechanism to organophosphates (Zhao et al. 1994). Furthermore, multiple resistance mechanisms may be involved or coexist in a single strain or population of western flower thrips (Jensen 1998, 2000a).

Because western flower thrips are highly polyphagous, feeding on a multitude of horticultural and ornamental plant types, populations of western flower thrips may have inherently evolved the genes/alleles that encode for the three enzyme systems mentioned above, thus promoting resistance development (Li et al. 2007). The most-important metabolic resistance enzyme system affiliated with western flower thrips populations is the cytochrome P-450 mono-oxygenases that confer cross-resistance (based on a single mechanism conferring resistance to insecticides in the same chemical class and/or having similar modes of action) to insecticides within and among different chemical classes (Espinosa et al. 2005). However, cross-resistance depends on the insecticide chemical class, as reports have indicated that ‘knockdown resistance' may be responsible for pyrethroid resistance in certain greenhouse populations of western flower thrips (Immaraju et al. 1992, Zhao et al. 1995b). Moreover, modifications to the enzyme, acetylcholinesterase, may be responsible for resistance to insecticides in the chemical classes associated with organophosphates (e.g., diazinon) and carbamates (e.g., methiocarb) (Jensen 2000b, Zhao et al. 1994). Nonetheless, other mechanisms, such as glutathione S-transferases, esterases, target-site sensitivity, altered acetylcholinesterace, and even reduced penetration, may be involved in resistance to different insecticides (Espinosa et al. 2005).

Spinosad (Conserve^®, Dow AgroSciences LLC; Indianapolis, IN), which is one of the most-widely used insecticides to suppress western flower thrips populations in greenhouse production systems (Loughner et al. 2005), became less effective as a consequence of resistance developing in western flower thrips populations, primarily due to overuse by greenhouse producers (Bielza et al. 2007, Loughner et al. 2005). For instance, failures in suppressing western flower thrips populations with spinosad, which occurred in Florida in 2006, were associated with resistance (Weiss et al. 2009). However, the mechanism involved is not metabolic detoxification but appears to be related to modifications, alterations, or reduced sensitivity of the target site (e.g., nicotinic acetylcholine receptor) (Bielza et al. 2007, Gao et al. 2012, Zhang et al. 2008) and may also be subsequently influenced by several genes or alleles (Zhang et al. 2008). In fact, spinosad resistance may be monogenic (when only one gene confers resistance, resulting in rapid development of resistance) or polygenic (when more than one gene confers resistance, leading to slow resistance development) (Bielza et al. 2007, Zhang et al. 2008). Furthermore, Hou et al. (2014) reported that resistance to spinosad was completely recessive and autosomal.

A major problem is dealing with western flower thrips populations having multiple resistance mechanisms to certain insecticides, which increases the probability of cross-resistance to unrelated insecticides (Gao et al. 2012). For instance, western flower thrips populations may possess two different resistance mechanisms, such as increased acetylcholinesterase activity and insensitive acetylcholinesterase (Jensen 1998, Zhao et al. 1994). There is the perceived implication that the level (based on fitness and stability) of resistance within a western flower thrips population will diminish more rapidly in the absence of insecticide exposure. Resistance, in general, has been observed to be affiliated with fitness costs (Roush and Daly 1990) including reduced longevity, fecundity, fertility, or decreased development time (Argentine et al. 1989, Ferrari and Georghiou 1981). However, western flower thrips populations may not exhibit any fitness costs in regard to insecticide resistance (Bielza et al. 2008). Consequently, a lack of fitness costs enhances the stability of resistance, thereby reducing the prospects of reverting populations back to susceptibility (Roush 1993), which may accelerate the rate of resistance development. Furthermore, the speed or rate of resistance development may be associated with resistant females having a higher fecundity and fertility than susceptible females (Bielza et al. 2008).

Another factor related to insecticide resistance in western flower thrips populations is demographics. The effect of demographics (e.g., north versus south) can influence the selection pressure placed on western flower thrips populations due to differences in longevity of the growing season and, consequently, the number and frequency of insecticide applications, which can influence the propensity for resistance to develop. Moreover, plant material that contains western flower thrips populations that were previously exposed to insecticides may be moved northward (R.A.C. pers. obs.). Typically, during early spring through late fall, greenhouse producers may conduct two to three applications every 5 to 7 days to suppress western flower thrips populations (Robb and Parrella 1995). Any subsequent applications are conducted to kill larvae and adults that were in the egg or pupal stages during previous applications (Parrella 1995).

Strategies that May Mitigate Insecticide Resistance

There needs to be a realization that greenhouse producers are going to continue to use insecticides against western flower thrips due to low tolerance for this insect pest. However, alternative plant protection strategies need to be implemented including cultural control (e.g., fertility), sanitation (e.g., weed and plant debris removal), physical control (e.g., screening greenhouse openings), and biological control (e.g., releasing predatory mites). These strategies, which are well known, may help reduce the selection pressure placed on western flower thrips populations from insecticide applications (Cloyd 2009a, 2015). There are a number of strategies that greenhouse producers currently use and can implement in the future to avoid the prospect of insecticide resistance developing in western flower thrips populations. These include scouting, insecticide rotations, insecticide mixtures, and the use of alternative insecticides with broad-spectrum modes of action.

Conclusion and Future Research Efforts

Insecticides will continue to be used to suppress western flower thrips populations in order to maintain the aesthetics of high-value horticultural and ornamental crops (Gao et al. 2012) as well as the fact that western flower thrips vector a number of tospoviruses (Allen and Broadbent 1986, Pappu et al. 2009). However, problems associated with the introduction of new insecticides for use against western flower thrips populations in greenhouse production systems are the costs and regulations of registering a new active ingredient, subsequently resulting in fewer new active ingredients being introduced into the marketplace against western flower thrips (Lewis 1977, Reitz and Funderburk 2012). In fact, there is the possibility that no new active ingredients will be added to the existing array of insecticides. Nevertheless, greenhouse producers need to exercise caution and judiciously use insecticides in order to prolong their effectiveness (Nauen and Denholm 2005). Although resistance may be a contributing factor responsible for inadequate suppression of western flower thrips populations, failures can also be attributed to insufficient spray coverage or improper timing of applications (Shelton et al. 2006).

Greenhouse producers should assume that populations of western flower thrips in greenhouses are resistant to one or more insecticides. Nevertheless, it is important to rotate insecticides with different modes of action and use insecticides with broad modes of activity in order to reduce the frequency of resistant genes or alleles within a western flower thrips population (Georghiou 1994). Proper rotation programs need to be implemented that do not over-use the same mode of action in order to preserve the effectiveness of existing insecticide products by abiding with the IRAC (Insecticide Resistance Action Committee, http://www.irac-online.org; accessed November 2015) label designations. Moreover, most insecticide labels contain resistance management information in order to curtail the advent of resistance, thus preserving the effectiveness of existing products. For example, the Conserve (active ingredient = spinosad) label states the following:

“Do not make more than two consecutive applications of Group 5 insecticides. If additional treatments are required after two consecutive applications of Group 5 insecticides, rotate to another class of effective insecticides for at least one application.”

However, the sole use of insecticides against western flower thrips is not a sustainable strategy. Therefore, it is important that greenhouse producers implement noninsecticidal strategies (e.g., sanitation, screening, and biological control) in order to reduce the input of insecticides and consequently the selection pressure placed on western flower thrips populations.

Current and future research efforts associated with western flower thrips management in greenhouse production systems include: (a) using multiple biological control agents (Ebssa et al. 2006, Premachandra et al. 2003, Saito and Brownbridge 2016), and (b) integrating insecticides with biological control agents (Messelink et al. 2014, Saito and Brownbridge 2016, Thoeming and Poehling 2006). Both of these strategies are designed to reduce insecticide inputs, thus diminishing selection pressure placed on western flower thrips populations, and to decreasing insecticide resistance.