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Resistance to Insecticides in Heliothine Lepidoptera: a Global View

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Resistance to Insecticides in Heliothine Lepidoptera: a Global View Resistance to insecticides in heliothine Lepidoptera: a global view Alan R. McCa¡ery Zoology Division, School of Animal and Microbial Sciences, and Crop Protection Unit,The University of Reading,Whiteknights, PO Box 228, Reading RG6 6AJ, UK (a.r.mcca¡[email protected]) The status of resistance to organophosphate, carbamate, cyclodiene and pyrethroid insecticides in the heliothine Lepidoptera is reviewed. In particular, resistance in the tobacco budworm, Heliothis virescens, and the corn earworm, Helicoverpa zea, from the New World, and the cotton bollworm, Helicoverpa armigera, from the Old World, are considered in detail. Particular emphasis has been placed on resistance to the most widely used of these insecticide groups, the pyrethroids. In each case, the incidence and current status of resistance are considered before a detailed view of the mechanisms of resistance is given. Contro- versial issues regarding the nature of mechanisms of resistance to pyrethroid insecticides are discussed. The implications for resistance management are considered. Keywords: insecticide resistance; Heliothinae; Heliothis virescens; Helicoverpa armigera; mechanisms of resistance the total population is only trivial (Forrester et al. 1993). 1. INTRODUCTION Any resistance genes would be swamped by susceptible Lepidopteran species in the genera Heliothis and Helicov- genes in the unsprayed refugia. Nevertheless, a ¢eld erpa are grouped together in the Tri¢ne subfamily population of H. punctigera from New South Wales was Heliothinae of the family Noctuidae (Hardwick 1965; recently shown to have developed resistance to a Mitter et al. 1993). The biology and ecology of the species pyrethroid (Gunning et al. 1997). The oligophagous within this complex have recently been reviewed by Fitt species Helicoverpa assulta feeds on tobacco and other (1989), Zalucki (1991) and King (1994). It is signi¢cant solanaceous plants and is found in Africa, Asia, parts of that within the group there exists a large number of Australasia and the South Paci¢c. It is normally highly destructive crop pests against which an unparal- considered to be a minor pest and there is no evidence of leled variety and quantity of insecticides have been used. it having developed resistance anywhere within its range The polyphagous nature of a number of these species, since it is not subject to any signi¢cant insecticide treat- their wide geographic range and their ability to adapt to ment (Armes et al. 1996). In the New World this genus is diverse cropping systems have contributed to this pest represented by the corn earworm, Helicoverpa zea, a key status. Moreover, the ability of certain species within the pest of maize, sorghum, cotton, tomato, sun£ower and complex to develop resistance to insecticides has placed soyabean. It too has developed resistance to a number of the heliothine Lepidoptera among a handful of the the insecticide groups used against it (Sparks 1981; world's most signi¢cant crop pests. Wolfenbarger et al. 1981; Stadelbacher et al. 1990), The genus Helicoverpa (designated Heliothis for a period) although not all the crops it attacks are sprayed and the includes the Old World species Helicoverpa armigera, gener- species remains reasonably amenable to control with ally considered to be the most important species within insecticides. this group. Commonly known as the cotton bollworm, Within the genus Heliothis there are two species of note. gram podborer or American bollworm, H. armigera occurs The New World representative, Heliothis virescens, is in Africa, Asia, southern Europe and Australia and is a distributed throughout the Americas, is commonly known major pest of cotton, maize, sorghum, pigeonpea, as the tobacco budworm and is a major pest of cotton, chickpea, soyabean, groundnut, sun£ower and a range of tobacco, tomato, sun£ower and soyabean. Like H. armi- vegetables. It, above all others in this genus, has gera above, it has developed resistance to all the insecti- developed resistance to virtually all of the insecticides cides that have been used against it in signi¢cant that have been deployed against it in any quantity. quantities (Sparks 1981; Wolfenbarger et al. 1981; Sparks et Helicoverpa punctigera is a pest of cotton, sun£ower, lucerne, al. 1993). The polyphagous species, Heliothis peltigera, has a soyabean, chickpea and sa¥ower in Australia and is broad distribution across central and southern Europe, commonly found alongside H. armigera. Interestingly, until the Canary Islands, Asia Minor and India and it is a pest recently H. punctigera had not developed resistance to of sa¥ower, tobacco, cotton, chickpea, fodder crops, insecticides (Gunning & Easton 1994; Gunning et al. grapevines and various fruit trees. Resistance to 1994), and this may have been because the pool of insecticides has not been reported in this species and this unsprayed insects is so vast that the treated proportion of is presumed to be due to lack of intense selection. Phil. Trans. R. Soc. Lond. B (1998) 353, 1735^1750 1735 & 1998 The Royal Society 1736 A. R. McCa¡ery Resistance to insecticides in heliothine Lepidoptera It is clear that within the Heliothinae there are two al. 1981), although there is little supporting information very signi¢cant pest species that have been subjected to in the literature that resistance to OPs is a signi¢cant intense selection with a range of insecticides and which problem in the control of this species (Sparks et al. have developed signi¢cant levels of resistance to 1993). insecticides: H. armigera and H. virescens. This review will therefore concentrate on resistance in these species and (c) Heliothis armigera will attempt to compare and contrast the phenomenon, H. armigera in Australia have generally been considered particularly with respect to the mechanisms of to be relatively susceptible to OP insecticides. Gunning & resistance. There are a large number of reviews that Easton (1993) found no evidence of resistance to methyl document the historical development of resistance in parathion and today only low levels of resistance are these species and it is not the intention of the present found to profenofos, chlorpyrifos and methyl parathion author to rehearse all of this literature here. The reader (N. W. Forrester, personal communication). In contrast, is directed to earlier works by Sparks (1981), high levels of resistance to monocrotophos and low levels Wolfenbarger et al. (1981) and Sparks et al. (1993). Most of resistance to chlorpyrifos and profenofos have been studies on resistance in heliothine insects in the past 15 recorded in populations of H. armigera in Pakistan years have concerned the pyrethroid insecticides and it (Ahmad et al. 1995), although resistance to profenofos is is for this reason that this review will place special continuing to rise as growers opt to use OPs rather than emphasis on this group, although other insecticide the pyrethroids, to which there is resistance. Low-to- groups will also be considered. moderate resistance was found to quinalphos in Indian An understanding of the mechanisms underlying and Pakistani populations of H. armigera (Armes et al. resistance is central to an ability to continue to e¡ectively 1996), but there was no evidence of signi¢cant resistance use existing insecticide chemistry to which resistance has to monocrotophos. Since 1980, phoxim has been the most already developed. A knowledge of the mechanisms of widely used OP for the control of H. armigera in China. It resistance enables one to understand not only the cross- was highly e¡ective until 1990, when it failed to control resistance patterns within insecticide groups but also populations in North China. Bioassays with insects those between them. Thus, the mechanisms of resistance collected from di¡erent geographical areas of China determine the use of `resistance-breaking' compounds during 1994 and 1995 showed resistance to phoxim to be and areas of new insecticide chemistry. Such considera- widespread (Wu et al. 1997). No resistance to monocroto- tions are crucial in resistance management. A detailed phos was observed in 1992 and 1993 (Wu et al. 1995), but knowledge of resistance mechanisms could also be consid- higher levels were recorded in 1995 (Wu et al. 1996). No ered as essential in the formulation of diagnostics for use resistance to OPs was detected in H. armigera in Thailand in resistance management although, as will be empha- (Ahmad & McCa¡ery 1988). sized later, the very diversity of response to selection in these insects could make the practical use of such diag- nosis especially di¤cult. The design of expression systems 3. MECHANISMS OF RESISTANCE TO for use in insecticide discovery might also be usefully ORGANOPHOSPHATES in£uenced by such information. This review therefore (a) Insensitive acetylcholinesterase: target-site places considerable emphasis on the mechanisms of resis- resistance to organophosphates tance and compares them in heliothine populations The enzyme acetylcholinesterase resides on the post- around the world. synaptic membrane of cholinergic synapses and is respon- sible for the breakdown of acetylcholine after stimulation of nicotinic acetylcholine receptors on the postsynaptic 2. RESISTANCE TO ORGANOPHOSPHATES neuron. Both organophosphate and carbamate insecti- (a) Heliothis virescens cides prevent the breakdown of acetylcholine by inhibiting After the development of resistance to DDT and toxa- the activity of this enzyme. The increased residence time phene, organophosphates (OPs), particularly
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