Introduction
Since the first review of stored product entomology by Parkin (Reference Parkin1956), there has been a considerable amount of published work, including books and textbooks, that has covered the integrated pest management of stored product insects. The problems caused by those insects associated with human activities lies in the competition between several species, including humans, for food resources. With a real shortage of food in many countries on the different continents and the possibility that basic food commodities may decline in future, the motivations for current research is high. Current projections indicate that future population and economic growth will require a doubling of current food production, including an increase from 2 to 4 billion tons of grain annually (Tubiello et al., Reference Tubiello, Soussana and Howden2007). In the same time, the economic cost of post-harvest losses is always a risk, even if it is difficult to estimate precisely the loss due to the pests concerned. Insects and mites are responsible for the deterioration of stored food, and they cause yearly losses estimated at about 30% of 1800 million tons of stored grain (Haubruge et al., Reference Haubruge, Arnaud and Mignon1997). Despite all the pesticides used/misused, insects still destroy over 30% of the world's food crops every year. Over 2 billion tons of grain are produced yearly for food and feed, providing two-thirds of the total direct and indirect protein intake (Tubiello et al., Reference Tubiello, Soussana and Howden2007). When observing the stock market value exchanges for maize or wheat on the American continent or in Europe, the price per ton is more than 200 dollars (i.e. tender wheat reached 385 $/ton in January 2008). Although we are unable to give a precise cost, a global worldwide cost of at least one hundred billion US dollars is often suggested (Haines, Reference Haines2000). Nearly 300 different species of stored product pests may be encountered but only 18 species are of primary economic importance. Stored product insects are adapted to infesting raw grains and cereal products, and are a constant threat to storage facilities worldwide. Post-harvest insect pests may be primary, i.e. able to attack intact grains such as in the genus Sitophilus, while others are secondary pests, attacking already damaged grains or grain products such as those from the genus Tribolium (Parkin, Reference Parkin1956). Two major groups of insects harbour the most economically important post-harvest insect pests: Coleoptera (beetles) and Lepidoptera (moths) (table 1). Several Coleopteran and Lepidopteran species attack crops both in the field and in store. Crop damage by Lepidoptera is only done by the larvae. Several lepidopteran larvae entangle the feeding media through silky secretion, which turn products into entwined lumps (Trematerra & Pavan, Reference Trematerra and Pavan1995; Wang et al., Reference Wang, Yin, Tang and Hansen2004). In the case of Coleoptera, both larvae and adults often feed on the crop; and the two stages are responsible for the damages on various crops, including maize, wheat, sorghum, barley, and other cereals (Daglish et al., Reference Daglish, Eelkema and Harrison1995).
List of the store-product insect species and their common names.
Current control methods are based on the use of insecticides, which are generally the most effective management tools and provide the only feasible method of reducing insect pest populations to acceptable levels (Harein & Davis, Reference Harein, Davis and Sauer1992; Perez-Mendoza, Reference Perez-Mendoza1999). The first experiments were carried out with organochlorine and organophosphorous insecticides, which were registered for their use in the control of stored product insects. They were then replaced by pyrethroids, especially pirimiphos-methyl and deltamethrin, that were shown to be very efficient against arthropods. Two fumigants are currently used for the protection of stored foods: phosphine and methyl bromide. However, the use of methyl bromide was restricted due to its ozone depleting properties and its very high toxicity to warm-blooded animals until it was banned according to the Montreal Protocol (Dansi et al., Reference Dansi, Van Velson, Vander and Heuden1984). Phosphine remains one of the most commonly used insecticides. In parallel, carbon dioxide is an important element enhancing the efficacy of controlled atmosphere treatments aimed at increasing pest mortality (Wang et al., Reference Wang, Zhao and Tsai2000). More recently, there was an increasing interest in testing and using natural oils. Essential oils are an alternative to the currently used fumigants. Papachristos & Stamopoulos (Reference Papachristos and Stamopoulos2003) have reviewed the different deployment methods, i.e. as fumigants (Stamopoulos, Reference Stamopoulos1991), contact insecticides (Saxena et al., Reference Saxena, Dixit and Harshan1992), repellents (Saim & Meloan, Reference Saim and Meloan1986), antifeedants (Harwood et al., Reference Harwood, Moldenke and Berry1990) and also deployment to influence some biological parameters, such as growth rate, life span and reproduction (Gunderson et al., Reference Gunderson, Samuelian, Evans and Brattsten1985). The other insecticides used are diverse and include microbial pesticides, insect growth regulators and synergists (Daglish et al., Reference Daglish, Eelkema and Harrison1995). Integrated pest management systems to control insect pests should combine both parasitoid and host plant resistance (Schmale et al., Reference Schmale, Wackers, Cardona and Dorn2003).
In the past few years, more than 504 species of insects and mites with insecticide resistance have been recorded, and there is still a steady increase in resistance to specific chemicals, with many species now resistant to several families of molecules (Georghiou, Reference Georghiou1990; Lee, Reference Lee2002a). Insects have successfully adapted to most insecticides by becoming physiologically or behaviorally resistant (Sawicki & Denholm, Reference Sawicki and Denholm1984). In post-harvest ecosystems, the development of insecticide resistance is of major concern in many countries (fig. 1, table 2). Cases of resistance of stored products insect to grain protectants (Arthur, Reference Arthur1996; Ding et al., Reference Ding, Wang, Zhao and Tsai2002) and fumigants (Champ & Dyte, Reference Champ and Dyte1977; Leong & Ho, Reference Leong and Ho1994) have been well documented. Resistance to insecticides such as malathion, pirimiphos-methyl, fenitrothion have been reported, for example, in Rhyzopertha dominica (F.), Sitophilus oryzae (F.), Sitophilus zeamais (Motschulsky), Tribolium castaneum (Herbst) (Guedes et al., Reference Guedes, Lima, Santos and Cruz1994, 1995). S. zeamais is resistant to DDT (DichloroDiphenylTrichloroethane) and deltamethrin (Lorini & Galley, Reference Lorini and Galley1999). Resistance to DDT and pyrethroids was reported in the early 90 s and, more recently, a few cases of organophosphate as well as pyrethroid resistance have been reported (Fragoso et al., Reference Fragoso, Guedes and Rezende2003; Ribeiro et al., Reference Ribeiro, Guedes, Oliveira and Santos2003). Insecticide resistance has a patchy distribution in Brazilian populations of maize weevil without significant spread, suggesting that the grain trade within the country and local selection are probably the major forces driving the evolution and spread of insecticide resistance in this study case (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995; Fragoso et al., Reference Fragoso, Guedes and Rezende2003, Reference Fragoso, Guedes and Peternelli2005; Ribeiro et al., Reference Ribeiro, Guedes, Oliveira and Santos2003). Perez-Medoza (Reference Perez-Mendoza1999) also described resistance in strains of S. zeamais in Mexico. In this country, maize weevil resistance to deltamethrin and permethrin was in its initial stages because these insecticides were registered as grain protectants only after 1992 (Perez-Mendoza, Reference Perez-Mendoza1999). Oryzaephilus surinamensis (L.) in Australia is another example. This insect was described as resistant to commonly used pesticides, such as fenitrothion, pirimiphos-methyl and chlorpyrifos methyl (Beckett et al., Reference Beckett, Evans and Morton1996). The field-collected strains showed resistance to DDT (1.3- to 14.1-fold), lindane (4.7- to 20.9-fold), malathion (1.6- to 31.4-fold), pirimiphos-methyl (3.0- to 3.7-fold), deltamethrin (1.2- to 1.8-fold) and permethrin (2.3- to 3.5-fold). In Morocco, 50 of the 51 insect populations that were studied have shown resistance (Benhalima et al., Reference Benhalima, Chaudhry, Mills and Price2004). Resistance to fumigants (phosphine, methyl bromide and ethylene dibromide) has also been reported in different parts of the world (Srivastava, Reference Srivastava1980; Mills, Reference Mills1983; Tyler et al., Reference Tyler, Taylor and Rees1983; Zettler, Reference Zettler1990; Athie et al., Reference Athie, Gomes, Bolonhezi, Valentini and De Castro1998) and has been well documented (Champ & Dyte, Reference Champ and Dyte1977; Leong & Ho, Reference Leong and Ho1994; Ho & Winks, Reference Ho and Winks1995). At least 11 species of stored-product insects are now known to have developed resistance to phosphine (Chaudhry, Reference Chaudhry2000), which has been linked to selection pressures by repeated ineffective fumigations in situations where phosphine gas was rapidly lost due to leakage (Halliday et al., Reference Halliday, Harris and Taylor1983; Tyler et al., Reference Tyler, Taylor and Rees1983; Benhalima et al., Reference Benhalima, Chaudhry, Mills and Price2004). Similarly, the extensive use of controlled atmosphere in insect control could lead to the selection of insect populations resistant to hypercarbia and hypoxia (Donahaye, Reference Donahaye1990b,Reference Donahayec; Wang et al., Reference Wang, Zhao and Tsai2000). Unfortunately, in the majority of these cases, the mechanisms of resistance are not reported nor studied.
Locations of observed resistances in stored product insects. Countries where the major studies on stored-product insect and insecticide resistances have been carried out since 1995.
Different control methods and type of resistances in stored-product insects described in the literrature since 1995.
Most recent research advances in insect topics, especially in resistance and in molecular and genetic advances focus on Diptera, particularly Drosophila and mosquitoes. Hemingway & Ranson (Reference Hemingway and Ranson2000) and Li et al. (Reference Li, Schuler and Berenbaum2007) deciphered the biochemical and molecular pathways of resistance developed by insects and Hemingway & Ranson (Reference Hemingway and Ranson2000) described the resistance mechanisms involving target site modification and metabolic resistance. The target site mutations (GABA receptor, AchE mutation, kdr mutation) led to the insecticide insensitivity, while the metabolic resistance, involving esterase, mono-oxygenase and gluthatione S-transferase enzymes, increased the metabolism of insecticides (Hemingway & Ranson, Reference Hemingway and Ranson2000). This article also enhanced the mutation in structural genes, gene amplification and transcriptional regulation in mosquitoes. Recently, Li et al. (Reference Li, Schuler and Berenbaum2007) described the involvement of transposable elements, allochemical tolerance and molecular mechanisms of metabolic resistance (upregulation, coding sequences changes, catalytic site). Research on stored-product insects was published in the Journal of Stored Products Research which was created in 1965. Another major motivation for research on stored product insects is the effect of pesticides on workers, currently under regulatory pressures, and inadequately documented. A recent review of alternative approaches has been produced (Phillips & Throne, Reference Phillips and Throne2010); but, until now, there was no overview (review) of the resistance mechanisms of insect stored products to insecticides.
Control methods
Heavily used methods
Physical control
Controlled atmospheres have been used to kill a wide range of quarantine and storage pests effectively, including members of the families Tephritidae, Tortricidae, Curculionidae, Miridae and Liposcelididae (Soderstrom et al., Reference Soderstrom, Brandl and Mackey1990; Ke & Kader, Reference Ke and Kader1992; Whiting et al., Reference Whiting, Foster, Heuvel and van den Maindonald1992; Leong & Ho, Reference Leong and Ho1995; Wang et al., Reference Wang, Zhao and Tsai2000). Carbon dioxide is an important factor affecting the efficacy of controlled atmosphere treatments for pest mortality. Generally, the combination of low O2 and high CO2 leads to higher mortality than either gas alone because of the combined effects of anoxia and hypercarbia (Wang et al., Reference Wang, Zhao and Tsai2000). CO2 is efficient only when concentrations higher than 40% are maintained for long periods. Exposure periods longer than 14 days are required to kill the insects when the concentration of CO2 in the air is below 40% (Kashi, Reference Kashi1981; Athie et al., Reference Athie, Gomes, Bolonhezi, Valentini and De Castro1998).
Fumigants
Two fumigants are currently used for the protection of stored foods: phosphine and methyl bromide. Methyl bromide (MeBr) fumigation of tree nuts was widely used to meet commercial phytosanitary requirements to control insect pests. However, it was used after careful consideration because of its very high toxicity to warm-blooded animals (Dansi et al., Reference Dansi, Van Velson, Vander and Heuden1984), and its use was restricted due to its ozone depleting properties (FAO, 1975).
The most commonly used fumigant is the phosphine, but its use was also limited because of increasing evidence that stored product insects were becoming resistant to the compound. This was observed in more than 45 countries (Bell & Wilson, Reference Bell and Wilson1995). Therefore, an effort is needed to develop a new compound to replace the conventional fumigants. The application of fumigant mixtures has been recognized as a means of overcoming the disadvantages of using a single fumigant. A combination of fumigants is advisable, because none of the common fumigants, used singly, possesses the ideal characteristics (Navarro et al., Reference Navarro, Carmi, Kashanchi and Shaaya1986; Athie et al., Reference Athie, Gomes, Bolonhezi, Valentini and De Castro1998).
Organochlorines
Organochlorines are persistent in the environment and are known for bioaccumulating or building up in sediments, plants and animals. DDT was the most widely used insecticide to protect stored maize in Brazil until 1985 (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995). Topical application bioassays of DDT and lindane were undertaken with 11 field strains of maize weevil, Sitophilus zeamais Motschulsky, collected from nine states in Mexico (Perez-Mendoza, Reference Perez-Mendoza1999) in order to compare them with new insecticide treatments. Nowadays, both DDT and lindane are officially withdrawn.
Organophosphates
When the use of organochlorines was restricted, they were replaced by organophosphorus compounds, like malathion, for the control of stored grain insects. Organophosphates replaced DDT, but the extensive use of malathion for pest control on stored cereals has resulted in a worldwide resistance of several species like Tribolium castaneum in 1961 in Nigeria or Sitophilus zeamais in Brazil (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995). The use of malathion decreased significantly after control failures in stored grain. Thus, this compound has been replaced by other organophosphorous, such as pirimiphos-methyl, chlorpyrifos-methyl, dichlorvos, etrimfos and fenitrothion.
Pyrethroids
Organophosphorous have been replaced by pyrethroids, such as phenothrin, deltamethrin, cypermethrin, permethrin with/without piperonyl butoxide. The deltamethrin shows a great efficacy against S. zeamais (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995). Some other chemical alternatives such as the α-cyano phenoxybenzyl cyclopropanecarboxylate pyrethroids and, particularly, deltamethrin synergized with piperonyl butoxide, which is an inhibitor of P450 s, have then been used (Bengston et al., Reference Bengston, Desmarchelier, Hayward, Henning, Moulden, Noble, Smith, Snelson, Sticka, Thomas, Wallbank and Webley1987; Arthur, Reference Arthur1994).
Alternative methods
Semiochemicals
Most semiochemicals are oils extracted from plants with pesticide properties. Essential oils are easily distilled and may act as fumigants against stored product insects (Stamopoulos, Reference Stamopoulos1991), contact insecticides (Saxena et al., Reference Saxena, Dixit and Harshan1992), repellents (Saim & Meloan, Reference Saim and Meloan1986), antifeedants (Harwood et al., Reference Harwood, Moldenke and Berry1990) and may also affect some biological parameters, such as growth rate, life span and reproduction (Gunderson et al., Reference Gunderson, Samuelian, Evans and Brattsten1985; Papachristos & Stamopoulos, Reference Papachristos and Stamopoulos2003). The monoterpenes cineol and limonene, which are commonly found in leaves of Eucalyptus globulus Labidalliere, E. camaldulensis Denhardt and E. cameroni Blakely & McKie, and in peel of Citrus aurantium L. and Citrus limonum Risso have a significant insecticidal effect (Prates et al., Reference Prates, Santos, Waquil, Fabris, Oliveira and Foster1998). These substances are toxic by penetrating the insect body via the respiratory system (fumigant system), the cuticle (contact effect) or the digestive system (ingestion effect) (Prates et al., Reference Prates, Santos, Waquil, Fabris, Oliveira and Foster1998). The toxicity of the evaporated substance is sufficient to knock down and kill insects, in a period of time as short as 24 h (Prates et al., Reference Prates, Santos, Waquil, Fabris, Oliveira and Foster1998). Essential oils are potential alternatives to current fumigants because of their low toxicity to warm-blooded mammals, their high volatility and their fumigation toxicity to stored grain insect pests (Shaaya et al., Reference Shaaya, Ravid, Paster, Juven, Zisman and Pissarev1991, Reference Shaaya, Kostjukovski, Eilberg and Sukprakarn1997; Regnault-Roger et al., Reference Regnault-Roger, Hamraoui, Holeman, Theron and Pinel1993). In a fumigation toxicity test of essential oils and monoterpenes, the alcohol and phenolic monoterpenes showed the greatest activity against Oryzaephilus surinamensis (L.), the sawtoothed grain beetle (Shaaya et al., Reference Shaaya, Ravid, Paster, Juven, Zisman and Pissarev1991; Lee et al., Reference Lee, Choi, Lee and Park2000b). Some essential oils have an acute toxicity, a repellent action, a feeding inhibition, or harmful effects on the reproductive system of insects. Additionally, secondary metabolites from higher plants have recently been used as pesticides or models for new synthetic pesticides, as, for instance, toxaphene (insecticide and herbicide) and cinmethylin (herbicide) (Prates et al., Reference Prates, Santos, Waquil, Fabris, Oliveira and Foster1998). Those chemicals were developed from plant-derived products such as terpenoids that can be found in essential oil secreted by the glandular trichomes of Artemisia (Compositae) or closely related genera. Pine oil, a by-product of the sulphate wood pulping industry, has the monoterpene α-terpineol among its major constituents. These substances present a toxicity to the house fly (Musca domestica L.), German cockroach (Blatella germanica L.), rice weevil (Sitophilus oryzae L.), red flour beetle (Tribolium cataneum Herbst) and Southern corn rootworm (Diabrotica unidecimpunctata howardi Barber) (Rice & Coats, Reference Rice and Coats1994a,Reference Rice and Coatsb).
Microbial insecticides
Microbial pesticides, such as spinosad or Bacillus thuringiensis, are biopesticides composed of a particular species of microbe, generally producing one or several toxins that will kill the pest. Microbial pesticides are supposed to be very selective and affecting the target pest (Abdel-Razek et al., Reference Abdel-Razek, Salama, White and Morris1999; Hertlein et al., Reference Hertlein, Thompson, Subramanyam and Athanassiou2011).
Botanical insecticides
The combination of applications of neem seed oil and use of resistant cowpea varieties appears to have great potential for the management of C. maculatus in stored cowpea with the reduction of egg-laying and adult emergence (Lale & Abdulrahman, Reference Lale and Abdulrahman1999; Lale & Mustapha, Reference Lale and Mustapha2000). In addition, their joint use in bruchid control would be likely to delay the emergence of biotypes of the bruchid that are capable of breaking down resistance in cowpea varieties or strains of C. maculatus with resistance to neem seed oil. Essential oils have low toxicity to warm-blooded animals, high volatility, and toxicity to stored grain insect pests (Shaaya et al., Reference Shaaya, Ravid, Paster, Juven, Zisman and Pissarev1991, Reference Shaaya, Kostjukovski, Eilberg and Sukprakarn1997; Regnault-Roger et al., Reference Regnault-Roger, Hamraoui, Holeman, Theron and Pinel1993).
Natural proteins
Natural insecticidal compounds from plant seeds have been detected and characterized (Soares et al., Reference Soares, Freitas, Oliveira, Sousa, Sales, Barreto-Filho, Bandeira and Ramos2007; Velten et al., Reference Velten, Rott, Cardona and Dorn2007). The arcelin from common beans Phaseolus vulgaris L. inhibited the development of Acanthoscelides obtectus; the seeds treated with arcelin delayed the growth of immatures (Velten et al., Reference Velten, Rott, Cardona and Dorn2007). In the same way, the weight of Callosobruchus maculatus larvae has been influenced, and decreased, by globulins and albumins from Luetzelburgia auriculata (Allemao). Depending of the concentrations, insecticidal effects could be observed (Soares et al., Reference Soares, Freitas, Oliveira, Sousa, Sales, Barreto-Filho, Bandeira and Ramos2007).
Insect growth regulators
Insect growth regulators (IGR) act in the insect to disturb a physiological regulatory process essential in the normal development of the insect or its progeny (i.e. emergence from pupae to adult). IGR insecticides are selective because of their narrow spectrum of activity, low mammalian toxicity, and are considered integrated pest management compatible (Ayalew, Reference Ayalew2011). The efficacies of chlorpyrifos-methyl, methoprene and piperonyl butoxide used as synergists have been tested on maize against resistant strains of Sitophilus zeamais, S.oryzae, R. dominica, T. castaneum and O. surinamensis and confirmed the efficacy of a combination of chlorpyrifos-methyl and methoprene and mentioned that methoprene alone could be used as part of a resistance management strategy against R. dominica (Daglish et al., Reference Daglish, Eelkema and Harrison1995). Daglish (Reference Daglish2008) showed that binary combinations of spinosad, chlorpyrifos-methyl and s-methoprene could control resistant strains of S.oryzae, R. dominica, T. castaneum, O. surinamensis and Cryptolestes ferrugineus. He also demonstrated the difficulties of finding the right combinations of products against a wide range of species regarding the development of resistance in different countries. The effects of N,N-diethyl-m-toluamide (DEET) known as an insect repellent (Watson & Barson, Reference Watson and Barson1996) have also been tested on different strains of O. surinamensis. The results showed an avoidance behaviour during the first seven hours, which disappeared after 24 h for all the strains.
Others
Integrated pest management (IPM) systems to control insect pests should combine the parasitoid and host plant resistance. The contribution of the combination of certain arcelin-enriched bean varieties with the parasitoid proved to be of significant advantage. The control system should be further optimized to promote host-feeding of the parasitoid (Schmale et al., Reference Schmale, Wackers, Cardona and Dorn2003). The main difficulties associated with the introduction of alternative control methods are a low acceptance by farmers and consumers, e.g. treatment of the grain with oil or ashes, or their high costs, e.g. storing of the grain in metal bins (Schmale et al., Reference Schmale, Wackers, Cardona and Dorn2003).
The different mechanisms of insecticide resistance
Cross and multiple resistance
A resistance to one insecticide is often related to a previous resistance to another molecule. A study on the resistance mechanisms of Sitophilus zeamais from Brazil (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995) mentioned that the knockdown resistance (kdr) in resistant insects is due to an alteration in the site of action of insecticides. Authors observed that kdr was the major resistance mechanism involved in cypermethrin and permethrin resistance, which were not used against stored grain pests in Brazil. These results support the contention that cross-resistance to pyrethroids in Brazilian populations of maize weevil occurred in seed storage facilities which were subjected to heavy DDT use in the past.
In the literature, cross-resistance has been mentioned without a definition of the mechanism involved. Lee et al. (Reference Lee, Hemingway, Yap and Chong2000a) and Lee (Reference Lee2002b) mentioned a possible cross-resistance to essential oils. In Brazil, Ribeiro et al. (Reference Ribeiro, Guedes, Oliveira and Santos2003) mentioned that the resistance to these compounds is likely to be caused by cross-resistance from another compound used as a grain protectant. Assumptions about the involvement of cross-resistance were expressed to explain observed resistance without any evidence and explanations. Fragoso et al. (Reference Fragoso, Guedes, Goreti and Oliveira2007) called the possibility of cross and multiple resistance from field observations, and suspected that resistance could be due to a result of cross-selection by another insecticide.
Chapman & Penman (Reference Chapman and Penman1979) described cross-resistance as a resistance to one compound conferring resistance to other compounds of the same group. Ishaaya (Reference Ishaaya2001) completed the definition as follows: cross-resistance appears when a strain (or population, or species) resistant to one insecticide becomes resistant to a second insecticide; in parallel, this strain, selected with the second insecticide, must become resistant to the first insecticide. In stored-product studies, multiple resistance occurs when a population (or strain) of insects that has developed resistance to one insecticide exhibits resistance to one or more insecticide(s) it has never been in contact with, or when insects develop resistance to several compounds by expressing multiple resistance mechanisms. Multiple resistance could include the developed resistance to one insecticide leading to the resistance to one or more insecticide(s) with a single or multiple resistance mechanisms.
Behavioural resistance
Wang et al. (Reference Wang, Yin, Tang and Hansen2004) observed that diapausing codling moth larvae had higher heat resistance and that the 5th instar was more resistant to heat. Authors also described a better resistance to heat after a first contact to high temperature (Wang et al., Reference Wang, Johnson, Tang and Yin2005; Yin et al., Reference Yin, Wang, Tang and Hansen2006). Some pyrethroid insecticides are known to be repellent to R. dominica and studies have shown that insects avoided treated grains (Laudani & Swank, Reference Laudani and Swank1954; Collins, Reference Collins1998; Lorini & Galley, Reference Lorini and Galley1998). Barson et al. (Reference Barson, Fleming and Allan1992) demonstrated that the avoidance behaviour in O. surinamensis was not only dependent on the relative sensitivity of each strain to the toxicant but also to the quality of the diet in terms of nutritional value and egg-laying sites. Sparks et al. (Reference Sparks, Lockwood, Byford, Graves and Leonard1989) identified the role of insect mobility in avoidance behaviour, and Wildey (Reference Wildey and Lawson1987) demonstrated the importance of insecticide formulation on contact repellency. Watson & Barson (Reference Watson and Barson1996) insisted on the effects of high insecticide concentrations leading to one avoidance behaviour of O. surinamensis. When applied at the highest tested doses, permethrin, pirimiphos-methyl and etrimfos caused disorientation. Tested insects demonstrated evidence of avoidance behaviour to high insecticide concentrations (Watson & Barson, Reference Watson and Barson1996). However, studies on the behavioural resistance of stored-product insects were not further carried out because the results did not show promising developments and uses. Finally, Haubruge et al. (Reference Haubruge, Arnaud and Mignon1997) demonstrated a particular behaviour in females of Tribolium custaneum leading to an increase of the resistance acquisition. Females have multiple mating and the last batch of male sperm preferentially fertilizes subsequent eggs leading to a sexual selection. They demonstrated an increase resistance transmission in populations (Haubruge et al., Reference Haubruge, Arnaud and Mignon1997). Also, some adaptations, such as reduced movement and avoidance, have been described in T. castaneum srains to survive to diatomaceous earth (Rigaux et al., Reference Rigaux, Haubruge and Fields2001)
Metabolic resistance
Resistance suppression by a particular synergism suggests that detoxification enzymes are involved in resistance mechanisms. The use of insecticide synergists for providing preliminary evidence of the resistance mechanisms has been fully explored in stored-grain insect pests (Guedes et al., Reference Guedes, Kambhampati, Dover and Zhu1997; Guedes & Zhu, Reference Guedes and Zhu1998). Three major families of enzymes were studied, including esterases, monooxygenases and glutathione S-transferases.
Esterases
Considerable focuses on the role of esterases have been described in pyrethroid tolerance. A clear relationship between the levels of esterases and populations of Nilaparvata lugens from pyrethroid treated and non-treated areas has been recorded (Hemingway et al., Reference Hemingway, Karunaratne and Claridge1999a). Kranthi et al. (Reference Kranthi, Armes, Rao, Raj and Sundaramurthy1997) and Gunning et al. (Reference Gunning, Moores and Devonshire1999) described the same correlations for Helicoverpa spp., respectively, in India and Australia. Esterases have been involved in the German cockroach pyrethroid resistance (Prabhakaran & Kamble, Reference Prabhakaran and Kamble1996; Scharf et al., Reference Scharf, Hemingway, Reid, Small and Bennett1996; Park & Kamble, Reference Park and Kamble1998). Lee & Clark (Reference Lee and Clark1996, Reference Lee and Clark1998) suggested that the pyrethroid was being sequestered in the haemolymph through a high affinity binding site on carboxylesterases. In other cases, no relationship was found between esterase levels/patterns and pyrethroid resistance (Moores et al., Reference Moores, Denholm and Devonshire1998; Barber et al., Reference Barber, Moores, Tatchell, Vice and Denholm1999; Guerrero et al., Reference Guerrero, Pruett, Kunz and Kammlah1999; Ali & Turner, Reference Ali and Turner2001). Despite the high level of variability in the esterases among the populations of Liposcelis bostrychophila, Ali & Turner (Reference Ali and Turner2001) were unable to link this variability with the permethrin tolerance. The involvement of esterases in resistance mechanisms to organophosphorus insecticides in Tribolium castaneum was mentioned early (Dyte & Rowlands, Reference Dyte and Rowlands1968). Triphenyl phosphate, a carboxylesterase inhibitor, was used as an indicator of carboxylesterase involvement in malathion resistance in laboratory tests (Dyte & Rowlands, Reference Dyte and Rowlands1968). Malathion resistance in most T. castaneum strains was due to this mechanism (Navarro et al., Reference Navarro, Carmi, Kashanchi and Shaaya1986; White & Bell, Reference White and Bell1988; Subramanyam et al., Reference Subramanyam, Harein and Cutkomp1989; Wool & Front Reference Wool and Front2003). Grain storage and warehouse operators should be aware that controlled atmosphere (CA) treatments can induce the esterase activities, which in turn can promote selection of pest strains resistant to CA treatments (Bond & Buckland, Reference Bond and Buckland1979) and the rates of development of CA resistance are similar to those recorded for laboratory induced resistance to fumigants (Donahaye, Reference Donahaye1990a,Reference Donahayec). Many similarities exist between CA resistance and resistance to methyl bromide (Monro, Reference Monro1964; Upitis et al., Reference Upitis, Monro and Bond1973; Wang et al., Reference Wang, Zhao and Tsai2000).
Glutathione S-transferases
Glutathione S-transferases are often described in insect resistance to insecticides. The involvement of GSTs in the defense against organophosphates, organochlorines and cyclodienes, is widely reported and continues to focus attention (Yu, Reference Yu1996, Reference Yu2002; Boyer et al., Reference Boyer, Tilquin and Ravanel2007; Fragoso et al., Reference Fragoso, Guedes, Goreti and Oliveira2007). The role of GSTs has been suggested in insecticide resistance of German cockroach species (Wu et al., Reference Wu, Scharf, Neal, Suiter and Bennett1998) and in the mite Varroa jacobsoni Oud. (Hillesheim et al., Reference Hillesheim, Ritter and Bassand1996). Kranthi et al. (Reference Kranthi, Armes, Rao, Raj and Sundaramurthy1997) suggested that the synergistic insensitive tolerance of Helicoverpa armigera (Hubner) was due to nerve insensitivity, and a similar mechanism was reported for Plutella xylostella (L.) (Yu & Nguyen, Reference Yu and Nguyen1996; Ali & Turner, Reference Ali and Turner2001). GST activity levels towards the substrate chloro-dinitro benzene (CDNB) were always higher, but not always significant in the resistant populations when compared with the susceptible population. The usually higher GST activity of the resistant populations is a likely consequence of their distinct selection history (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995; Ribeiro et al., Reference Ribeiro, Guedes, Oliveira and Santos2003; Fragoso et al., Reference Fragoso, Guedes, Goreti and Oliveira2007), which also seems to lead to differences in fitness cost associated with insecticide resistance in those populations (Fragoso et al., Reference Fragoso, Guedes and Peternelli2005, Reference Fragoso, Guedes, Goreti and Oliveira2007; Guedes et al., Reference Guedes, Oliveira, Guedes, Ribeiro and Serrao2006). The higher catalytic activity of GSTs provides support for the hypothesis of their involvement in the resistance to this insecticide group in some maize weevil populations. GSTs may act as binding proteins increasing the activity of other pyrethroid detoxification enzymes such as esterases (Grant & Matsumura, Reference Grant and Matsumura1989; Kostaropoulos et al., Reference Kostaropoulos, Papadopoulos, Metaxakis, Boukouvala and Papadopoulou-Mourkidou2001). Their activity as antioxidant agents decreasing the oxidative stress initiated by pyrethroids was also suggested (Vontas et al., Reference Vontas, Small and Hemingway2001). The role of enhanced GST activity in pyrethroid resistance in Brazilian populations of maize weevil is suggested, but this resistance mechanism is apparently of secondary importance to altered target sites (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995; Fragoso et al., Reference Fragoso, Guedes and Rezende2003; Ribeiro et al., Reference Ribeiro, Guedes, Oliveira and Santos2003) and is not so stable as observed on demographic and physiological studies with the same populations of Sitophilus zeamais (Fragoso et al., Reference Fragoso, Guedes and Peternelli2005, Reference Fragoso, Guedes, Goreti and Oliveira2007; Guedes et al., Reference Guedes, Oliveira, Guedes, Ribeiro and Serrao2006).
Monooxygenases
The monooxygenases are a complex and large family of enzymes known to be involved in the adaptation of insects and in the metabolism of insecticides. A number of mechanisms have been recently suggested to explain the tolerance or resistance to pyrethroid insecticides. Microsomal cytochrome P450-dependent mono-oxygenases are of importance in mosquitoes (Boyer et al., Reference Boyer, David, Rey, Lemperière and Ravanel2006; David et al., Reference David, Boyer, Mesneau, Ball, Ranson and Dauphin-Villemant2006), Lepidoptera (Kranthi et al., Reference Kranthi, Armes, Rao, Raj and Sundaramurthy1997), house flies (Korytko & Scott, Reference Korytko and Scott1998), headlice (Hemingway et al., Reference Hemingway, Miller and Mumcuoglu1999b) and Blatella germanica (L.) (Scharf et al., Reference Scharf, Hemingway, Reid, Small and Bennett1996, Reference Scharf, Hemingway, Small and Bennett1997; Wu et al., Reference Wu, Scharf, Neal, Suiter and Bennett1998). For example, the indirect synergistic evidence suggested that the detoxification mechanisms in L. bostrychophila are of microsomal mono-oxygenase type (Turner et al., Reference Turner, Maude-Roxby and Pike1991; Ali & Turner, Reference Ali and Turner2001). In our area of investigation, some recent studies mentioned the possible involvement of P450 on natural insecticides. A large number of essential oils extracted from various spices and herb plants have already been screened for toxicity as potential fumigants. Monoterpenes rich in essential oils also showed strong fumigant toxicities against several stored-grain insect pests (Shaaya et al., Reference Shaaya, Ravid, Paster, Juven, Zisman and Pissarev1991). Monoterpenes can be degraded by the cytochrome P450-dependent mono-oxygenase system. In insects, 1,8-cineole was metabolised to 2b-hydroxycineole when the pyrgo beetle Paropsisterna tigrina Chapuis was fed on leaves of the Australian tea tree, Melaleuca alternifolia (Maiden & Betche) Cheel (Southwell et al., Reference Southwell, Maddox and Zalucki1995). Essential oils or monoterpenes could induce the concentration and aldrin epoxidase activity of cytochrome P450-dependent mono-oxygenase in rats and insects (Brattsten et al., Reference Brattsten, Wilkinson and Eisner1977; Hiroi et al., Reference Hiroi, Miyazaki, Kobayashi, Imaoka and Funae1995; Lee et al., Reference Lee, Choi, Lee and Park2000b). Collins et al. (Reference Collins, Rose and Wegecsanyi1992) also reported the 21.9-fold higher aldrin epoxidase activity and 12.5-fold higher concentration of cytochrome P450 in a CM-resistant strain, VOSCM in comparison to VOS48. Therefore, cytochrome P450 mono-oxygenase activity is presumably related to the detoxification of essential oil or monoterpenes in O. surinamensis (Lee et al., Reference Lee, Choi, Lee and Park2000b; Lee, Reference Lee2002b). A P450 gene (CYP345D3) has been described from T. castaneum (Jiang et al., Reference Jiang, Wang, Liu and Dou2008). Sharing 91% of identity with another gene CYP345D1 described in T. castaneum, the real function of the sequence is still unnkown. Two novel P450 genes (CYP6CE1, CYP6CE2) were described in Liposcelis bostrychophila, which were related with a deltamethrin exposure (Jiang et al., Reference Jiang, Tang, Xu, An and Wang2010). But no functional role has been determined.
Previous examples suggested that P450 mono-oxygenases are involved with the appearance of resistance to essential oil vapour. Pretreatment of the insects with diethylmaleate, an inhibitor of the glutathione S-transferases (Raffa & Priester, Reference Raffa and Priester1985; Welling & De Vries, Reference Welling and De Vries1985), caused a partial suppression of resistance to lavender essential oil vapour. Conversely, triphenyl phosphate, an esterase inhibitor (Guedes & Zhu, Reference Guedes and Zhu1998; Guedes et al., Reference Guedes, Kambhampati, Dover and Zhu1997), did not show a degree of synergism indicating that these enzymes are not involved in the detoxification of lavender essential oil vapour by Acanthoscelides obtectus (Papachristos & Stamopoulos, Reference Papachristos and Stamopoulos2003). Those studies suggested that P450 and GST play a role in the resistance to lavender essential oil vapour but not the esterases.
Others
Activities of carboxyl esterase and super oxide dismutase were positively correlated to CO2 resistance in the psocid, Liposcelis bostrychophila (Wang et al., Reference Wang, Zhao and Tsai2000). The involvement of the same enzymes in the same species has been suggested (Ding et al., Reference Ding, Wang, Zhao and Tsai2002).
Target site resistance
Acetylcholinesterases
The mode of action of fumigant toxicity of essential oil or monoterpene against insects may also be due to the inhibition of acetylcholinesterase (AChE) (Ryan & Byrne, Reference Ryan and Byrne1988). These authors determined that five monoterpenes inhibited AChE activity in the electric eel and killed adults of the red flour beetle, Tribolium castaneum (Herbst). The enhanced carboxyl esterase and anti-oxidation enzyme (superoxide dismutase and catalase) activities could reduce the effects of these toxic products on insects resulting in an increase of insect resistance to CO2. Although the resistance mechanisms of dichlorvos have not been elucidated, it is well known that organophosphate pesticides exert their neurotoxic effects by inhibiting the acetylcholinesterase (AChE), thereby prolonging the residence time of acetycholine at cholinergic synapses and producing hyperexcitation of cholinergic pathways.
Knockdown resistance (kdr)
The kdr resistance was described first in the house fly Musca dominica and then further and intensively studied in mosquito species (Martinez-Torres et al., Reference Martinez-Torres, Chandre, Williamson, Darriet, Bergé, Devonshire, Guillet, Pasteur and Pauron1998; Kasai et al., Reference Kasai, Ng, Lam-Phua, Tang, Itokawa, Komagata, Kobayashi and Tomita2011). The kdr resistance is a common resistance mechanism encountered in several insect species, which gives a reduced sensitivity (up to 20 times) to DDT and pyrethroids because of the alteration, in active sites, of the protein targeted by the insecticides in the voltage-gated sodium channel (Araujo et al., Reference Araujo, Williamson, Bass, Field and Duce2011). The involvement of the kdr mutation in the insecticide resistance (including DDT and pyrethroids) of Sitophilus zeamais has been described in Brazil (Guedes et al., Reference Guedes, Lima, Santos and Cruz1995; Ribeiro et al., Reference Ribeiro, Guedes, Oliveira and Santos2003; Araujo et al., Reference Araujo, Williamson, Bass, Field and Duce2011). This kdr resistance has also been observed and characterized in the Colorado potato beetle, Leptinotarsa decemlineata, and involved in permethrin resistance (Lee & Clark, Reference Lee and Clark1999).
Gene involvement with undefined-role
Studies on Tribolium castaneum and Rhyzopertha dominica were mostly conducted by Beeman and Collins (Beeman, Reference Beeman1983; Beeman & Nanis, Reference Beeman and Nanis1986; Beeman & Stuart, Reference Beeman and Stuart1990; Collins, Reference Collins1998; Collins et al., Reference Collins, Daglish, Bengston, Lambkin and Pavic2002; Schlipalius et al., Reference Schlipalius, Cheng, Reilly, Collins and Ebert2002). Malathion-specific resistance has been particularly documented in T. castaneum. Most studies concluded that this resistance was controlled by a single factor (Beeman, Reference Beeman1983; White & Bell, Reference White and Bell1990), but there were evidences of a second allele giving a weaker resistance to malathion, also segregated at this locus (Beeman & Nanis, Reference Beeman and Nanis1986). Lindane resistance was also reported as being multifactorial, and this resistance was described as controlled by a single semi-dominant gene located on chromosome III. (Beeman & Stuart, Reference Beeman and Stuart1990; Collins, Reference Collins1998). Collins (Reference Collins1998) suggested that pyrethroid resistance in T. castaneum was autosomally inherited, and maternal effects were absent, estimating that there were two or three independent genes controlling the response of F1 backcrosses (Collins, Reference Collins1998). Assie et al. (Reference Assie, Francis, Gengler and Haubruge2007) showed that the increase of a high malathion-specific resistant strain was due to a genetic background and could depend in changes occurring in environmental parameters. They also suggested that two generations of selection could be sufficient to detect the potential for the increase of resistance (Assie et al., Reference Assie, Francis, Gengler and Haubruge2007). As suggested by Collins, extra resistance genes, with different characteristics, might have evolved in different regions. Collins (Collins et al., Reference Collins, Daglish, Bengston, Lambkin and Pavic2002) mentioned that resistance to phosphine in Rhyzopertha dominica species is complex and could involve between at least two, and possibly five, different genes (Collins et al., Reference Collins, Daglish, Bengston, Lambkin and Pavic2002; Schlipalius et al., Reference Schlipalius, Cheng, Reilly, Collins and Ebert2002).
Conclusions
The objectives were to give an overview of the information on the resistance of stored-product insects to the different types of control treatments. There are very few fundamental studies on stored product insects, as compared to applied research generating results with data useful in the field. Solving the problem of resistance requires information on the history of pesticide use, pest management strategies and decision making. Several studies point the need for more precision on the mechanisms of resistance (Soares et al., Reference Soares, Freitas, Oliveira, Sousa, Sales, Barreto-Soderland, Bloomquist, Rousch and Tabashnik1990; Kljajic & Peric, Reference Kljajic and Peric2006). As the number of insecticides and fumigants for insect control has decreased, low cost, convenient to use and environmentally friendly alternatives need to be developed (Papachristos & Stamopoulos, Reference Papachristos and Stamopoulos2003).
Phylogeographical issues also need to be highlighted. There are no existing data on the possible relationship between evolution of resistance and genetic polymorphism in stored-product species. Further studies could be helpful in understanding where these species originated from and what are the natural enemies in the original area, also in understanding the world-wide spread of a given species and studying the differences in the evolution of resistance among the different geographical areas. A very detailed study by Black & Vontas (Reference Black and Vontas2007) reported the sequencing methods currently used (more than 20) and explained the single nucleotide polymorphism mechanisms involved. The benefits, failures and costs were studied for every technique. In our laboratory, RFLP primers were developed to study the phylogeography of R. dominica sampled on the five continents. Furthermore, the study of insecticide resistance should use evolutionary and ecological approaches to explore its genetic basis, together with the way selection acts to bring genetic changes and the use of this information to delay the onset of resistance (Assie et al., Reference Assie, Francis, Gengler and Haubruge2007). The cost of new and innovative control methods in the developing countries needs to be supported by developed countries through collaborations and joint projects (Black & Vontas, Reference Black and Vontas2007). Indeed, the archives on insecticide treatments, the cases of insecticide resistance, the number of species and insecticides studied, the mechanisms involved and results in genetic studies could be helpful to predict the development rate of resistance to insecticides. Moreover, the effect of population density, plant/insect interactions on the level of resistance could be integrated into theoretical models (Assie et al., Reference Assie, Francis, Gengler and Haubruge2007).
Acknowledgements
This work was supported by a China Postdoctoral Science Foundation, China National Science and Technology Project of the 11th Five-Year Plan (2006BAD02A18-03 and 2006BAI09B04-06) and Hubei Key Project of Science and Technology. We thank K. Day, University of Coleraine, for reviewing the English of the manuscript.
