Acaricides in modern management of plant-feeding mites

Transcription

1 J Pest Sci (2012) 85: DOI /s ORIGINAL PAPER Acaricides in modern management of plant-feeding mites Dejan Marcic Received: 29 January 2012 / Accepted: 22 May 2012 / Published online: 2 June 2012 Ó Springer-Verlag 2012 Abstract This review focuses on biological profiles of contemporary acaricides, acaricide resistance, and other up-to-date issues related to acaricide use in management of plant-feeding mites. Over the last two decades a considerable number of synthetic acaricides emerged on the global market, most of which exert their effects acting on respiration targets. Among them, the most important are inhibitors of mitochondrial electron transport at complex I (METI-acaricides). Discovery of tetronic acid derivatives (spirodiclofen and spiromesifen) introduced a completely new mode of action: lipid synthesis inhibition. Acaricide resistance in spider mites has become a global phenomenon. The resistance is predominantly caused by a less sensitive target site (target site resistance) and enhanced detoxification (metabolic resistance). The major emphasis in current research on acaricide resistance mechanisms deals with elucidation of their molecular basis. Point mutations resulting in structural changes of target site and leading to its reduced sensitivity, have recently been associated with resistance in Tetranychus urticae Koch and other spider mites. The only sustainable, long-term perspective for acaricide use is their implementation in multitactic integrated pest management programs, in which acaricides are applied highly rationally and in interaction with other control tactics. Considering that the key recommendation for effective acaricide resistance Communicated by N. Desneux. D. Marcic (&) Department of Applied Entomology and Zoology, Institute of Pesticides and Environmental Protection, Banatska 31B, P.O. Box 163, Belgrade-Zemun, Serbia marcion@bitsyu.net management is reduction of the selection for resistance by alternations, sequences, rotations, and mixtures of compounds with different modes of action, the main challenge that acaricide use is facing is the need for new active substances with novel target sites. Besides implementation of advanced technologies for screening and design of new synthetic compounds, wider use of microbial and plant products with acaricidal activity could also contribute increased biochemical diversity of acaricides. Keywords Acaricides Modes of action Resistance Spider mites Integrated mite management Introduction Until mid-twentieth century, spider mites (Acari: Tetranychidae) and other plant-feeding mites were minor pests of agricultural crops, presumably due to regulation by predatory mites and insects. Advances in agricultural production after World War II, based on the extensive use of synthetic pesticides and fertilizers, irrigation and other cultural practices, induced increase in spider mite populations far above economic thresholds. Grown under favorable conditions, plants became high quality food sources for the mites, which gave rise to outbreaks of their populations and made it possible to compensate for the losses caused by predators. Moreover, populations of spider mite predators were destroyed by widespread use of organochlorine, organophosphorous, and carbamate insecticides. These broad-spectrum neurotoxic compounds, intended for the control of insect pests, were also toxic to insect and mite predatory species, generally more susceptible than their prey. On the other hand, heavy selection pressure by the insecticides caused emergence of tetranychid mite

2 396 J Pest Sci (2012) 85: populations resistant to these compounds. Besides the resistance of spider mites and the elimination of their predators, as the primary causes, insecticides influenced behavior and physiology of pests and/or predators (Huffaker et al. 1969; Jeppson et al. 1975; Hoy 2011). Spider mites, the most important plant-feeding mites, are common pests nowadays in many cropping systems worldwide. After spider mites, the second most important mite plant pests are gall and rust mites (Eriophyoidea), while the other economically harmful species can be found among flat mites (Tenuipalpidae) and tarsonemid mites (Tarsonemidae) (Zhang 2003; Hoy 2011). Since the first serious and widespread outbreaks of spider mites populations, during the 1950s, broad-spectrum neurotoxic insecticides were gradually replaced by specific acaricides, i.e., compounds exclusively or primarily effective against mite pests. Several generations of structurally diverse synthetic acaricides, directed against various biochemical and physiological targets, have been launched until now. Bridged diphenyls, the first specific acaricides, took their place in the market during 1950s and 1960s. Until the mid 1970s the second generation of specific acaricides as organotins, formamidines, quinoxalines, propargite appeared (Jeppson et al. 1975). Mite growth inhibitors (clofentezine, hexythiazox), launched during the 1980s, represented the third generation. In addition to specific acaricides, a number of insecticides with considerable acaricidal activity (pyrethroids, avermectins, benzoylureas) have also been introduced during 1970s and 1980s (Dekeyser and Downer 1994; Knowles 1997; Dekeyser 2005; Pitterna 2007). With the advent of compounds acting on respiration targets, by the beginning of 1990s, the modern era in development of synthetic acaricides began (Dekeyser 2005). Acaricide resistance in plant-feeding mites is a seriously increasing phenomenon, especially in spider mites which have a remarkable intrinsic potential for rapid evolution of resistance (Cranham and Helle 1985; Knowles 1997; van Leeuwen et al. 2010a). Therefore, there is a continual need for development of new acaricides with novel modes of action, but also for optimization of their use in order to delay the evolution of resistance and prolong their life span (Dekeyser 2005). Considering integrated pest management (IPM) as key approach to modern plant protection (Hoy 2011), new acaricides should be effective against the target pests and compatible with their natural enemies; moreover, these compounds must be safe products with respect to human health, beneficial and nontarget organisms and the environment. This review focuses on biological profiles and uses of modern acaricides (including bioacaricides as an alternative to synthetic compounds), acaricide resistance in spider mites, and compatibility of acaricides with the integrated mite management, as major current issues related to acaricide uses in modern management of plant-feeding mites. Modern synthetic acaricides Most of the acaricides of the first and second generation are not present on the global market nowadays. Regarding older broad-spectrum insecticides, almost all organochlorines were severely restricted or banned, mostly due to toxicological and environmental concerns, while several organophosphorous and carbamate compounds are still available for control of plant-feeding mites (Casida and Quistad 1998; van Leeuwen et al. 2010b; Hoy 2011). Nowadays, acaricides are developed and introduced under conditions marked by growing demand of the public opinion for safer, greener pesticides, and increasingly sharp toxicological and eco-toxicological criteria imposed by the regulatory agencies. In the USA, the passage of the Food Quality Protection Act (FQPA) of 1996 brought about significant changes in the way in which pesticides are registered by the US EPA (Environmental Protection Agency). Besides the elimination of many uses of organophosphates and carbamates, which could not meet more rigorous safety standards, priority has been given to reduced-risk pesticides as a replacement for older and potentially riskier chemicals. The list of reduced-risk pesticides includes several new acaricides and insecto-acaricides (EPA 2011a, b). In the European Union, implementation of Directive 91/414 that requires science-based assessment of pesticide risk to human health and the environment, has seriously influenced the EU acaricide portfolio. Nevertheless, new Regulation (EC) 1107/2009 on sustainable use of pesticides revises the Directive and introduces hazard-based regulatory cut-off criteria, thus increasing the safety and leading to the withdrawal of a substantial number of compounds (EU 2009; van Leeuwen et al. 2010b). When looking at the acaricides, from 103 substances, only 30 are currently approved under the Regulation (EU 2011). In the last two decades a considerable number of nonneurotoxic synthetic acaricides and insecto-acaricides emerged in the global market. Most of the modern synthetic acaricides exert their effects through disruption of respiratory processes. Acaricides acting on respiration targets Nervous system of mites has long been the target for most chemicals used for their control organophosphates, carbamates, organochlorines, formamidines, pyrethroids, avermectines (Dekeyser and Downer 1994; Knowles 1997). The situation began to change with the introduction of a number of compounds acting on mitochondrial respiration, that produces most of the energy in cells. This process includes two coupled parts: mitochondrial electron transport (MET) and oxidative phosphorylation. Although some of the older acaricides were known to inhibit

3 J Pest Sci (2012) 85: Fig. 1 Acaricides acting on respiration targets: METI acaricides respiration, the real exploitation of this target started after the 1990s, with the prospects for expanding and developing new, more effective and safer products (Dekeyser 2005; Sparks and DeAmicis 2007). Along the MET chain there are various potential sites for inhibition, but only three have been used so far as target sites of acaricidal activity, at transmembrane enzyme complexes. In the period , four chemically different compounds whose mode of action was inhibition of MET at complex I were launched: fenpyroximate (pyrazole-oxime), tebufenpyrad (pyrazole-carboxamide), pyridaben (pyridazinone), and fenazaquin (quinazoline) (Fig. 1). These compounds, also known as METI acaricides, quickly gained the popularity worldwide as broad-spectrum acaricides with long-lasting effect. Among METI acaricides, only pyridaben is intended also for insect management, because its biological activity spectrum includes whiteflies, aphids, leafhoppers, mealybugs, and thrips (Sparks and DeAmicis 2007; van Leeuwen et al. 2010b). METI acaricides are approved under Regulation 1107/2009 (EU 2011). Fenpyroximate is also on the list of reduced risk and organophosphorus alternative pesticides (EPA 2011). Complex I inhibitors also include two pyrimidinamines, pyrimidifen and flufenerim, introduced in 1995 and 2004, and another pyrazole-carboxamide, tolfenpyrad, launched in These compounds are effective against spider mites and eriophyoid mites, as well as against hemipteran and lepidopteran insect pests (Dekeyser 2005; Sparks and DeAmicis 2007). They have never been notified in the EU. They are registered in Japan and some other Far East countries. The only known complex II inhibitors are the recently introduced two beta-ketonitrile derivatives cyenopyrafen and cyflumetofen (Fig. 2) acaricides intended for spider mite control (Tomlin 2009). The status of cyflumetofen under Regulation 1107/2009 is pending, while cyenopyrafen has never been notified in the EU (EU 2011). These two acaricides are registered in Japan and some other countries. Complex III inhibition is the mode of action of three compounds (Fig. 2). Acequinocyl, a naphthoquinone compound commercialized in 1999, is a pro-acaricide which is bioactivated via deacetylation, and is effective against all stages of spider mites (Dekeyser 2005; Sparks and DeAmicis 2007). It is included in the EPA list of reduced risk pesticides, while the decision on its status under Regulation 1107/2009 is pending (EPA 2011; EU 2011). Bifenazate, a carbazate compound introduced in 1999, is highly effective against motile stages of spider mites, with long-lasting activity (Dekeyser 2007; Ochiai et al. 2007). Although it was first considered to be a

4 398 J Pest Sci (2012) 85: Fig. 2 Acaricides acting on respiration targets: complex II inhibitors, complex III inhibitors, and inhibitors of oxidative phosphorylation neurotoxin, more recent studies (van Leeuwen et al. 2008; van Nieuwenhuyse et al. 2009) indicate complex III as target site. Bifenazate is a pro-acaricide which is bioactivated via hydrolysis of ester bonds, so the organophosphates, as inhibitors of esterase hydrolytic activity, can antagonize the toxicity of this acaricide (van Leeuwen et al. 2007). Bifenazate is classified as a reduced risk pesticide, and it is approved under Regulation 1107/2009 (EPA 2011; EU 2011). Fluacrypyrim, introduced in 2002, shows acaricidal effect against all stages of tetranychids. This is the first strobilurin commercialized as an acaricide (Dekeyser 2005; Sparks and DeAmicis 2007). Fluacrypyrim is registered in Japan, China, and South Korea. Recently, Chai et al. (2011) demonstrated that strobilurin derivatives containing pyrimidine moieties could be used as lead compounds for developing novel acaricides. Diafenthiuron, a thiourea compound (Fig. 2) launched in 1991, is the only modern representative of compounds that disrupt oxidative phosphorylation by inhibition of the mitochondrial ATP synthase. This compound is a pro-acaricide, which is activated by oxidative desulfurization to corresponding carbodiimide. Diafenthiuron is effective against motile stages of spider mites and also provides good eriophyoid and tarsonemid control. It is also effective against whiteflies, aphids, leafhoppers (Ehrenfreund 2007; van Leeuwen et al. 2010b). It is mostly used against the sucking pest complex on cotton in Asia, Australia, and Latin America. Diafenthiuron is banned in EU under Regulation 1107/2009 (EU 2011). Another insecto-acaricide, chlorfenapyr (Fig. 2), a pyrrole compound commercialized in 1995, at biochemical level acts as uncoupler of oxidative phosphorylation via disruption of the proton gradient. This compound is a proacaricide activated by N-dealkylation. Chlorfenapyr is effective against all stages of spider mites and eriophyoid mites. It is also active against many insect pest species in the orders Lepidoptera, Thysanoptera, Coleoptera (Kuhn and Armes 2007; van Leeuwen et al. 2010b). Chlorfenapyr is included in the EPA list as an alternative to organophosphorous compounds (EPA 2011), but is not approved under Regulation 1107/2009 (EU 2011).

5 J Pest Sci (2012) 85: Fig. 3 Acaricides acting on growth and development targets Acaricides acting on growth and development targets Another approach in research of synthetic acaricides launched compounds that affect growth and developmental processes. As mentioned before, in the first half of 1980s clofentezine and hexythiazox appeared. These acaricides are commonly referred to as mite growth inhibitors. However, their exact mode of action is unknown. Likewise, development within the benzoylurea chemical class, by the end of 1980s resulted in comercialization of flucycloxuron and flufenoxuron, which act as growth regulators by inhibition of chitin biosynthesis (Dekeyser and Downer 1994; Knowles 1997). Both are highly active against eggs and immature stages. Although not toxic to adults, mite growth inhibitors/regulators could considerably reduce fecundity of treated females (Grosscurt 1993; Marcic 2003). Etoxazole, a oxazoline compound (Fig. 3) launched in 1998, acts on mites similar to clofentezine and hexythiazox, and it is usually classified together with these acaricides (Pree et al. 2005; Bretschneider and Nauen 2007). On the other hand, Nauen and Smagghe (2006) provided evidence that etoxazole acts as a chitin synthesis inhibitor similar to benzoylureas. Etoxazole is approved under Regulation 1107/2009, and included on the EPA list of reduced risk and organophosphorus alternative pesticides (EPA 2011; EU, 2011). Discovery of spirodiclofen and spiromesifen, tetronic acid derivatives (Fig. 3) launched in , broadened the biochemical diversity of acaricides by introducing a completely new mode of action. These compounds act as inhibitors of acetyl-coa-carboxylase, a key enzyme in fatty acid synthesis. Spirodiclofen and spiromesifen are highly toxic to eggs and immature spider mites, while their effects on adult females are slower with fecundity and egg hatching reduction; their acaricidal effect is long-lasting and stable (Nauen 2005; Bretschneider et al. 2007; Marcic 2007; van Pottelberge et al. 2009a; Marcic et al. 2010, 2011a). These two acaricides are the only new compounds with good control potential against eriophyoid mites as well (van Leeuwen et al. 2010b). Besides acaricidal properties, spirodiclofen shows considerable insecticidal activity against eggs and larvae of pear psylla and scales, while spiromesifen is effective against whiteflies (Bretschneider et al. 2007). Spirodiclofen is approved under Regulation 1107/2009, while the status of spiromesifen in the EU is pending (EU 2011). The latter is included in the EPA list of reduced risk pesticides (EPA 2011). Spirotetramat, recently introduced tetramic acid derivative (Fig. 3), has the same mode of action as spirodiclofen and spiromesifen. Although initially developed for control of whiteflies, aphids and other homopteran pests (Bretschneider et al. 2007; Brück et al. 2009), the studies of its effects on spider mites (Kramer and Nauen 2011; Marcic et al. 2011b, 2012) indicate that spirotetramat is an effective acaricide as well. Spirotetramat is a two-way systemic compound, unique among recently developed insecticides and acaricides. After penetration into the plant tissue it is hydrolised to the enol form that allows its ambimobility,

6 400 J Pest Sci (2012) 85: Fig. 4 Bioacaricides i.e., translocation in both phloem and xylem. Owing to this ambimobile activity, spirotetramat can protect new leaves appearing after foliar application, as well as roots (Brück et al. 2009). This compound is included in the EPA list of reduced risk pesticides (EPA 2011), whereas its status under EU Regulation 1107/2009 is pending (EU 2011). Bioacaricides Growing demands for environmentally friendly, safe and integrative approaches to plant pest management contributed to re-actualize importance of biopesticides as one of alternatives to intensive use of synthetic chemical pesticides, especially broad-spectrum compounds. Biopesticides could be defined as commercial plant protection agents manufactured from living organisms and/or their products. The most common advantages of biopesticides are their safety to beneficial and non-target organisms, short environmental persistence, low mammalian toxicity, lack of harvest and re-entry restrictions, minimum risk for pest resistance development, compatibility with IPM programs and organic crop production (Copping and Menn 2000; Copping and Duke 2007; Chandler et al. 2011; Regnault- Roger et al. 2012). Some of the biopesticides of microbial and plant origin have considerable acaricidal effect. Products isolated from soil actinomycetes are an important source for deriving natural pesticides. Macrocyclic lactones abamectin (a mixture of avermectines B 1a and B 1b, fermentation products of Streptomyces avermitilis), and milbemectin (a mixture of milbemycins A 3 and A 4, fermentation products of S. hygroscopicus subsp. aureolacrimosus) are globaly recognized examples of successful commercialization of acaricides and insecticides of microbiological origin (Fig. 4). These two products, introduced at the end of 1980s and beginning of 1990s, are neurotoxic acaricides (chloride channel activators), effective against spider mites and eriophyoid mites. Abamectin also shows insecticidal activity against lepidopteran, coleopteran, and homopteran pests (Copping and Duke 2007; Pitterna 2007; van Leeuwen et al. 2010b). Abamectin and milbemectin are approved under Regulation 1107/2009 (EU 2011). Entomopathogenic fungi, formulated as mycoacaricides with conidia, blastospores and other live propagules as active ingrediant, can also be efficient alternative to synthetic chemical acaricides (Chandler et al. 2005; Maniania et al. 2008; van Leeuwen et al. 2010b; Gatarayiha et al. 2011). At the beginning of the 1980s, only one mycoacaricide was available (based on Hirsutella thompsoni Fisher), intended for suppression of citrus rust mite. A quarter of a century later, there are some 30 commercial

7 J Pest Sci (2012) 85: Fig. 5 Constituents of essential oils with acaricidal activity products acting against tetranychid, eriophyoid, and tarsonemid mites. More than a third of up-to-date mycoacaricides is made from conidia of two ascomycetes, Beauveria bassiana (Balsamo) Vuillemin and Metarhizium anisopliae (Metschnikoff) Sorokin (de Faria and Wraight 2007). Two strains of B. bassiana and one strain of M. anisopliae are approved under Regulation 1107/2009 (EU 2011). Probably the most studied botanical insecticide in the last 20 years is a triterpenoid azadirachtin (Fig. 4), the major active ingredient of extracts, oils, and other products derived from the seeds of the Indian neem tree (Azadirachta indica), sold by a number of companies worldwide. Azadirachtin is effective growth regulator (moulting disruptor), repellent, antifeedant, and oviposition deterrent (Copping and Menn 2000;Isman2006; Copping and Duke 2007). The studies on plant-feeding mites (Mansour et al. 1997; Martinez-Villar et al. 2005; Venzon et al. 2008), showed that azadirachtin acts as acaricide as well, causing mortality, repellency, and reduction of fecundity and longevity. Azadirachtin is approved under Regulation 1107/2009 (EU, 2011). Essential oils, secondary metabolites derived from various organs of aromatic plants belonging mostly to a few families (e.g., Asteraceae, Apiaceae, Lamiaceae, Myrtaceae, Rutaceae) are important source of natural products showing pesticide activity. Essential oils are highly complex mixtures of terpenoids (monoterpenes and sesquiterpenes) as the major constituents, and related aromatic compounds. Many essential oils and/or their constituents (particularly monoterpenes) primarily act as fumigants (Isman 2006; Han et al. 2010; Regnault-Roger et al. 2012). Neurotoxic activity, i.e., antagonism of the octopaminergic receptors and acetylcholinesterase (AChE) inhibition have been suggested as modes of action of some essential oil constituents. Since they are complex mixtures, essential oils may have more than one site of action (Isman 2006; Badawy et al. 2010; Regnault-Roger et al. 2012). Essential oils from basil, caraway, citronella Java, clove, lemon eucalyptus, mint, pennyroyal, peppermint, rosemary, oregano, thyme, and other plants have shown a significant acaricidal activity (Choi et al. 2004; Miresmailli et al. 2006; Han et al. 2010). As for the constituents of essential oils, carvone, carvacrol, cineole, cinnamaldehyde, cuminaldehyde, eugenol, geraniol, limonene, linalool, menthol, thymol are recognized as effective against spider mites (Fig. 5) (Miresmailli et al. 2006; Badawy et al. 2010; Lim et al. 2011). Examples of registered commercial formulations of acaricides aimed to control of plant-feeding mites include products based on cinnamaldehyde, eugenol, cottonseed, clove and canola oils, rosemary and peppermint oils, American wormseed oil (Copping and Menn 2000; Miresmailli and Isman 2006; Copping and Duke 2007; Cloyd et al. 2009; Regnault-Roger et al. 2012). Products based on citronellol and farnesol act as

8 402 J Pest Sci (2012) 85: attractants; they increase activity of mites which enhance their exposure to a co-applied synthetic acaricide (Copping and Menn 2000; Tomlin 2009; Chandler et al. 2011). Commercial formulations with acaricide activity are also present among other plant extracts and oils (pyrethrum, rotenone, fatty acids, rapeseed oil, soybean oil, potassium salts of plant oils) and fermentation products (polynactins) (Copping and Menn 2000; Copping and Duke 2007; Tsolakis and Ragusa 2008;Marcic et al.2009;tomlin2009). Although the growth of the sector of biopesticides is several times higher compared to synthetic insecticides (Chandler et al. 2011), commercial success of biopesticides still lags far behind their true potential as alternative plant protection products. Their shorter persistence (which can be considered as advantage or disadvantage), susceptibility to unfavorable environmental conditions, slower rate of action, relatively limited shelf-life, inconsistent field results, regulatory barriers, are the reasons for which they are often uncompetitive compared to synthetics (Copping and Menn 2000; Chandler et al. 2011). However, bioacaricides are practically unavoidable plant protection measures in organic production. European Union Regulative (EC) No. 889/2008 (EU 2008) allows the use of products based on microorganisms, azadirachtin, pyrethrins, rotenone, plant oils, fatty acids as plant protection product in organic production. In conventional production, importance of biopesticides is increasing with acceptance of the IPM concept and the rising level of its implementation (Isman 2006; Chandler et al. 2011). Other alternatives Petroleum-derived spray oils (PDSO) have been used for more than a century to control a wide range of crop pests, including plant-feeding mites (Jeppson et al. 1975; Childers et al. 1996; Hoy 2011). Because of high phytotoxicity, their use was limited to dormant application against overwintering pest stages, to avoid injury to green plant tissue. Advances in petroleum chemistry and increasing environmental and health concerns related to the synthetics have led to renewed interest in the use of PDSO. Highly refined agricultural mineral oils ( broad-range petroleum spray oils) and horticultural mineral oils ( narrow-range petroleum spray oils) have a high potential for the control of spider mites and other plant-feeding mites on various field and greenhouse crops (Agnello et al. 1994; Nicetic et al. 2001; Cating et al. 2010; Chueca et al. 2010). PDSO kill only upon contact and thorough coverage is essential to achieve high acaricidal efficacy. The most widely accepted theory on their mode of action is that PDSO primarily act physically by blocking the spiracles in insects or the stigmata in mites, and thus causing suffocation. However, suffocation occurs only when mites and insects are over-sprayed. The oil can enter into the body via integument as well, and it seems to be more relevant way of entry. Rapid penetration through the cuticle followed by accumulation in the lipid-containing tissues and finally penetration into the nerve cells has been recently suggested as an alternative mode of action of PDSO (Najar-Rodriguez et al. 2008; Stadler and Buteler 2009). Owing to their short-term residual activity, the lack of evidence of mite or insect resistance, and negligible impact on environment and human health, PDSO can be recommended under IPM programs. On the other hand, the fact that it may take multiple treatments to achieve effective control could be considered as disadvantage. Moreover, phytotoxicity can occur after application to heat- or drought-stressed plants (Childers 2002; Hoy 2011). PDSO are considered compatible with organic farming (EU 2008). Sulfur (elemental sulfur, lime sulfur) is the oldest know acaricide that have been used against eriophyoid mites over the years (Jeppson et al. 1975; Childers et al. 1996). Nowadays, it is one of the few organically approved pesticides (EU 2008) and is approved under Regulation 1107/2009 (EU 2011). However, sulfur-containing products have long been identified as disruptive to integrated mite control. Several studies showed a relationship between increased density of spider mite populations and sulfur use, with suppression of phytoseiids, plant-based effects and other causes as explanations (Hanna et al. 1997; Costello 2007; Beers et al. 2009; James and Prischmann 2010). Considering these findings, sulfur should not be recommended in modern IPM. Acaricide resistance in spider mites As a result of the exceptional intrinsic ability of mites to rapidly develop resistance (Cranham and Helle 1985; van Leeuwen et al. 2010a) the acaricide resistance in spider mites has become a global phenomenon. Arthropod Pesticide Resistance Database (APRD) supported through a partnership between Insecticide Resistance Action Committee (IRAC), US Department of Agriculture, and Michigan State University contains published data on resistance in insects and mites important for agriculture, veterinary medicine, and public health, from 1914 to the present date (Whalon et al. 2008, 2011). This database, which is useful for comprehension of acaricide resistance on a global level, at the end of 2011 contained 1177 reports on resistance in 79 species from Acari subclass. Out of this number, 760 reports concern 27 species belonging to three families of plant-feeding mites: Tetranychidae, Eriophyidae and Tenuipalpidae. Approximately 98 % of reports

9 J Pest Sci (2012) 85: deal with the resistance of spider mites, with two predominant species: two-spotted spider mite, Tetranychus urticae Koch, the most important plant-feeding mite (53 % of spider mite reports) and European red mite, Panonychus ulmi Koch (25 % of spider mite reports). The authors of the APRD created the list of the top 20 resistant arthropod pests in the world, ranked by number of unique active ingredients for which resistance has been reported. On this list, T. urticae and P. ulmi are ranked first and sixth, respectively, by data for 93 and 45 compounds (Whalon et al. 2008, 2011). For both species, the majority of reports refer to resistance to organophosphates documented during the 1950s, 1960s, and 1970s; however, there are more recent reports, because these substances still account for significant share of global insecticide market. The important part of the APRD database concerns pyrethroid resistance with the increasing number of cases that have been registered in the recent past. As for other acaricides and insecto-acaricides, there is practically no one without documented cases of resistance, but there is an obvious difference in the scope of phenomenon between compounds. For instance, global popularity of METI-acaricides contributed to relatively rapid development of resistant spider mite populations in several different geographical regions. On the other hand, the number of reports on resistance to propargite and organotins is very limited, although they have been in use for four decades now (van Leeuwen et al. 2009; Whalon et al. 2011). In addition to comprehensive documenting of acaricide resistance in spider mites, the factors affecting this phenomenon of microevolution were also studied, as well as its physiological, biochemical, and genetic mechanisms. The results of these studies were reviewed by Cranham and Helle (1985), Knowles (1997), and van Leeuwen et al. (2009, 2010a), and the largest number of data refers to populations and strains of T. urticae. As in other arthropods, the resistance in spider mites is predominantly caused by a less sensitive target site (target site resistance) and/or enhanced detoxification by metabolizing enzymes (metabolic resistance). The major emphasis in current research on acaricide resistance mechanisms deals with elucidation of their molecular basis. Point mutations (replacement of one nucleotide by another) resulting in structural changes of target site (amino acid substitutions) and leading to its reduced sensitivity, have recently been associated with resistance in T. urticae and other spider mites. As for molecular characterization of metabolic resistance, there are currently no available data on genes associated with this type of resistance mechanism (van Leeuwen et al. 2009, 2010a). Reduced sensitivity of AChE, a key enzyme in nervous impulse transmission, seems to be the most common type of T. urticae resistance to organophosphates. This species was the first arthropod in which target site resistance was proven to be the mechanism of resistance in the early 1960s (Cranham and Helle 1985; Stumpf et al. 2001, Tsagkarakou et al. 2002; van Leeuwen et al. 2009, 2010a). In European strains of T. urticae resistant to organophosphates Khajehali et al. (2010) found three AChE substitutions involved in the resistance: F331W (indicated as the most important), G328A, and A201S. The F331W mutation was also found in a monocrotophos-resistant T. urticae strain from South Korea, as well as G119S and A280T mutations (Kwon et al. 2010b). All these mutations, except A280T, have been previously characterised in insects. Metabolic resistance, hydrolysis by carboxylesterases or oxidation by microsomal monoxygenases was found in several cases of pyrethroid resistance in two-spotted spider mite (Ay and G}urkan 2005; van Leeuwen et al. 2005; van Leeuwen and Tirry 2007), but target-site (sodium channel) insensitivity has been reported as well. The F1538I substitution (one of the most highly effective resistance loci for pyrethroids) was found to be associated with bifenthrin resistance in T. urticae strains from Greece (Tsagkarakou et al. 2009) and fenpropathrin resistance in a Chinese strain of Tetranychus cinnabarinus (Boisduval) [synonym: T. urticae] (Ya-ning et al. (2011). On the other hand, in a fenpropathrin-resistant strain of T. urticae from South Korea, the L1022V mutation was proposed to play a major role in the resistance (Kwon et al. 2010a), while bifethrin resistance in Tetranychus evansi Baker & Pritchard was associated with the M918T mutation (Nyoni et al. 2011). These two mutations have not previously been found in any other mite species resistant to pyrethroids. Oxidative metabolism appears to play a major role in twospotted spider mite resistance to METI-acaricides, but the involvement of alternative or additional mechanisms has also been suggested (Stumpf and Nauen 2001; Kim et al. 2006;van Pottelberge et al. 2009c). Metabolic resistance has also been reported as mechanism in Panonychus citri (McGregor) resistance to pyridaben (Niu et al. 2011). The increase of detoxification enzyme activity has been associated with resistance to chlorfenapyr (van Leeuwen et al. 2006) and clofentezine (Ay and Kara 2011) in two-spotted spider mite. Van Pottelberge et al. (2009b) suggested that oxidative metabolism might play the most important role in spirodiclofen resistance in T. urticae. Kramer and Nauen (2011) also indicated involvement of monooxygenases in P. ulmi resistance to this acaricide. The results reported by Stumpf and Nauen (2002) and Khajehali et al. (2011) indicated increased metabolism, while Kwon et al. (2010c) found insensitivity of the target site (glutamate-gated chloride channel) as mechanism of T. urticae resistance to abamectin. Target site resistance, highly correlated with reduced sensitivity of the mitochondrially encoded redox protein cytochrome b, was found in T. urticae and P. citri strains resistant to bifenazate (van Leeuwen et al. 2008, 2011).

10 404 J Pest Sci (2012) 85: Discovery that bifenazate resistance is inherited only maternally is the first report of non-mendelian inheritance of pesticide resistance in arthropods. In both species, in almost all highly resistant strains, the most encountered amino acid substitution was G126S, always accompanied by another substitution. Mutations conferring resistance had no adverse effects on overall fitness in T. urticae. Biological, biochemical, and molecular characterization of resistance is one of the essential elements in defining the strategy for management of acaricide resistance in spider mites. An effective acaricide resistance management program could be based on general resistance management principles endorsed by IRAC. The key recommendation is reduction of the selection for resistance by alternations, sequences, rotations, and mixtures of compounds with different modes of action. The IRAC Mode of Action Classification Scheme provides a valuable guide to the selection of acaricides (Elbert et al. 2007; Whalon et al. 2008). In European Union, the list of the acaricides approved under Regulation 1107/2009 allows choice of active substances from seven classes with different modes of action (EU 2011). However, choosing possibilities become much more narrow, considering the intended uses of the acaricides, as well as the resistance to organophosphates, pyrerthroids, and METI acaricides evolved in spider mite populations in many crops and regions. Likewise, some acaricides can not provide effective control of eriophyoid mites (van Leeuwen et al. 2010b), which makes the choice even more narrow and additionally threaten resistance management. Acaricides and IPM The strategy of relying solely on application of synthetic acaricides to control plant-feeding mites has been unsustainable. On the other hand, biological control by predatory mites (mostly Phytoseiidae) has proven to be a successful alternative, especially on protected crops, but it also showed some limitations. In modern plant protection, the key approach is integration of chemical, biological, cultural, and other control tactics in IPM programs, so as all the tactics are compatible with each other (Hoy 2011). As an element of IPM programs, acaricides should be selective, i.e., highly effective against mite pests and relatively safe to their predators. Therefore, it is very important to study the effects of acaricides on phytoseiid mites, other predatory mites and insect predators of plantfeeding mites. In addition to direct mortality, pesticides also cause a variety of sublethal (either physiological or behavioral) effects on individuals that survive exposure to lethal or sublethal doses/concentrations. These effects must be considered for a complete analysis of pesticide impact on natural enemies (Desneux et al. 2007). International Organization for Biological and Integrated Control/Western Palearctic Regional Section (IOBC/WPRS) working group Pesticides and beneficial organisms has developed the sequential procedures for testing side-effects of pesticides on the most important natural enemies (including phytoseiid mites) which comprises laboratory, semi-field, and field trials. Assessment of pesticide effect on reproductive capacity has been included in laboratory tests in addition to mortality (Hassan 1992; Blümel et al. 1999). Regarding phytoseiids, some aspects of these procedures (way of exposure, choice of doses/concentrations, evaluation criteria, toxicity ranking, etc.) have been discussed with suggestions for improvements (e.g., Sterk et al. 1994; Bakker and Jacas 1995; Amano and Haseeb 2001; Duso et al. 2008). French ANPP/CEB guideline No.167 has been used as an alternative test method (Bonafos et al. 2008). In order to obtain a better understanding of the longer-term impact of pesticides, the use of demography and population modeling for estimation of pesticide effects on arthropods was also proposed (Stark and Banks 2003; Stark et al. 2007). The primary objective of testing pesticide side-effects on predators of plant-feeding mites is finding physiologically selective compounds. However, results obtained in one test should not be taken as general conclusion on (non)compatibility of an acaricide. Besides intrinsic differences among predatory species in susceptibility to the same acaricide, there have been a lot of different, and sometimes even contrasting results on the same active substance and the same species, due to different test procedures. Moreover, the results obtained by standardized methods are affected by the product formulation type, origin of strains and other factors. On the other hand, the intrinsically non-selective compounds can be made safer by using various operational tactics, e.g., spot treatments, reduction of application rates, application timing to avoid or minimize exposure of predators, use of acaricide-resistant strains of predators (Knowles 1997; Zhang 2003; Blümel et al. 1993, 1999; Hoy 2011). Many experts promote IPM as the best approach to make plant protection more sustainable. Recognising general IPM principles, Hoy (2011) points out that effective IPM programs require multiple tactics such as monitoring of plant-feeding mites and their natural enemies (in order to determine if the pest population exceeds the economic injury level), cultural controls (all modification to agronomic practices that are intended to reduce pest damage), host plant resistance, biological control (mostly release of commercially produced phytoseiid mites and other natural enemies), and regulatory methods. Chemical control (using intrinsically selective or operationally compatible acaricides) is considered as the last resort, i.e., if other applied

11 J Pest Sci (2012) 85: measures are not sufficient in keeping the pest population below the economic threshold. Although in many cropping systems worldwide control of plant-feeding mites still predominantly relies on application of synthetic acaricides, the only long-term, sustainable perspective for acaricides is their implementation in multitactic IPM programs, which is possible to different levels of sophistication. Transition from conventional pest control to IPM actually changes the role of acaricides in modern plant protection: within the principles of IPM, acaricides are applied highly rationally and in interaction with other control tactics. At the same time, the basic challenge still remains a growing need for active substances with novel primary target sites. Beside use of advanced technologies for screening and design of new synthetic compounds, wider use of bioacaricides could, to some extent, contribute to increased diversity of modes of action. 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