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Activity Spectrum of Spinosad and Indoxacarb: Rationale for an Innovative Pyrethroid Resistance Management Strategy in West Africa O.G. Ochou T. Martin Centre de Coopération
International en Recherche Agronomique (CIRAD) ABSTRACT To face pyrethroid resistance in the cotton bollworm Helicoverpa armigera (Hübner), endosulfan (700 g/ha) has been used in a resistance management strategy for four years in Côte d'Ivoire, West Africa. Actually, its recommendation is being questioned with regard to its acute toxicity and environmental issues. Earlier prospects revealed that insecticides such as spinosad (48 g/ha) and indoxacarb (25 g/ha) proved as effective as endosulfan in controlling H. armigera. In contrast to endosulfan, the activity spectrum of these non pyrethroids insecticides appears to be restricted to a few bollworm and leaf pests. The present study pointed out the strength and weakness of these new insecticides with respect to major insect pests and beneficial species. On the basis of their activity spectrum and in the light of cotton crop phenology and main pest seasonal occurence, a differential scheme was designed. Indoxacarb is more appropriate to the fruiting stage (101-115 DAE (Day After Emergence)) as it appeared very effective against the cotton stainer Dysdercus voelkeri (Schmidt) while showing lower performance against Earias spp and the mite Polyphagotarsonemus latus (Bank). In contrast, spinosad is to be used preferably at the vegetative stage (45-66 DAE) as it proved safer to coccinellids, more effective against Earias spp while its lower effectiveness against D. voelkeri suggests avoiding its positioning at a late stage of cotton. Various benefits related to these new insecticides strongly advise their use as alternatives to pyrethroids. Still, to be more attractive, their activity needs to be reinforced by other insecticides in such a way to control the whole arthropod pest complex. KEY WORDS: Cotton, Helicoverpa armigera, pyrethroid resistance management strategy, Spinosad, Indoxacarb, Côte d'Ivoire. INTRODUCTION The development of resistance in H. armigera: Known as very effective in controlling Helicoverpa armigera (Hübner) and most cotton bollworm pests, pyrethroids have been widely used for more than twenty years in Côte d'Ivoire. Recently, laboratory data obtained on H. armigera strains within 1996-1998 pointed out significant increase in the LD50 for both deltamethrin (Figure 1) and cypermethrin (Vassal et al., 1997; Vaissayre et al., 1998; Martin et al., 2000). Field data recorded for eight consecutive years (Figure 2) revealed that the pest infestation profiles changed deeply from 1991 to 1998 (Ochou et al., 1998). Moreover, cases of ineffectiveness of the pest control programme against H. armigera have been reported during exceptional pest outbreaks in Côte d'Ivoire. With this regard, the routine calendar-based programme applying six fortnightly sprays of pyrethroid-organophosphate insecticide mixtures over the whole cotton season has been questionned as the pyrethroid resistance in H. armigera was confirmed (Ochou & Martin, 2000). Similar cases of resistance were reported in H. armigera in most West African countries (Benin, Burkina Faso, Guinea, Mali, Senegal, and Togo) (Anonymous, 1999). Development of the IRM strategy against H. armigera: To face pyrethroid resistance in the cotton bollworm, H. armigera, an Insect Resistance Management (IRM) programme, inspired from the "Australian" strategy (Sawicki and Denholm, 1987), was designed in Côte d'Ivoire. In practice, the strategy has led to the determination of a pyrethroid-free season nationwide by using non-pyrethroid insecticides (endosulfan 700-750g/ha and profenofos 750 g/ha) in a kind of "window" programme in order to lessen pyrethroid selection pressure. The pyrethroid-free season is established according to cotton growing zones (August 10 and August 20 respectively for northern and southern regions). The main picture which has come out from the nationwide adoption of the pyrethroid resistance management programme by cotton farmers is the important decrease in the field populations of H. armigera (Figure 2) since 1998 (Ochou & Martin, 2002). Endosulfan has been widely used in the current pyrethroid resistance management programme over the last four years in Côte d'Ivoire, and so far, no resistance to endosulfan has been detected (Martin et al., 2002). However, its recommendation is being actually questioned with regard to its toxicity, environmental issues, and farmer practices. To tackle this problem, investigations are being undertaken to adapt a relatively low dose of endosulfan (525 g/ha) to the actual field infestation of H. armigera (Ochou & Martin, 2000) and to assess microencapsulated formulations of endosulfan, assumed safer than the EC formulations. At the same time, further investigations focused on new insecticides such as spinosad and indoxacarb as potential alternatives to endosulfan. Spinosad is a naturally produced mixture of the actinomycete Saccaropolyspora spinosa. Its mode of action is described as an activation of the nicotine acetylcholine receptor, but at a different site from nicotine or imidachloprid. It is activated by contact and ingestion, causing paralysis (Pesticide Manual, 12th edition, v2). Indoxacarb is an oxadiazine product where the active component blocks sodium channels in nerve cells. It is activated by contact and ingestion, and affected insects cease feeding, with poor co-ordination, paralysis, and ultimately death (Pesticide Manual, 12th edition, v2). Due to their novel mode of action, both insecticides appear ideal for resistance management programmes. However, to be rationally used, there is a need for a precise activity spectrum of these new insecticides which proved as effective as endosulfan in controlling H. armigera (Ochou & Martin, 2002). The present study is to assess the activity spectrum of spinosad and indoxacarb with regard to beneficials and major components of the cotton pest complex in Côte d'Ivoire. The need to reinforce their activity by other insecticides will be also assessed. On the basis of the strength and weakness of these new insecticides and with respect to cotton crop phenology and seasonal occurence of main pests, appropriate recommendations will be stated to justify their integration into the pyrethroïd resistance management programmes. MATERIALS and METHODS The study was carried out for three consecutive years (1999-2001) at the cotton research station of CNRA based at Bouaké and at the experimental station of LCCI at Nambingué. At first, the biological activity of the two specific insecticides (spinosad 48g/ha (Laser 480 SC, Dow AgroSciences) and indoxacarb 25g/ha (Avaunt 150 SC, Du Pont)) was assessed in reference with endosulfan 750 g/ha (Phaser 375 EC, Aventis), and deltamethrin 12 g/ha (Decis 12 EC, Aventis) through a Complete Bloc Design with six replicates. Individual plots were of 10 rows x 15 m. Further field trials were undertaken in a similar design with the two insecticides in association with other insecticides. Tested mixtures included spinosad 48g/ha + profenofos 300g/ha, spinosad 48g/ha + acetamiprid 10g/ha, indoxacarb 25g/ha + profenofos 300g/ha, indoxacarb 25g/ha + acetamiprid 10g/ha, and cypermethrin 36g/ha + profenofos 300g/ha. Insecticides sprays were performed with an adapted horizontal boom knapsack sprayer debiting 60 l/ha of product-water mixture. Plots were treated every 14 days from 45th to 115th DAE (day after emergence of cotton). Fields were scouted directly on plants once a week from 30th to 122nd DAE for sucking pests, leafworms, and exocarpic bollworms pests, and every two weeks on green bolls from 70th to 112th DAE for endocarpic bollworms. Target pests and beneficials were recorded as follows:
Three year average data for all bollworms and one-two year average data for sucking pests, leaf pests, and benefials were considered. RESULTS Effectiveness of spinosad and indoxacarb against cotton bollworms: Data presented in Figures 3a-d show compared effectiveness of the pyrethroid deltamethrin and the non pyrethroïd insecticides on cotton exocarpic bollworm species (H. armigera, Earias spp., D. watersi) and endocarpic bollworm species (C. leucotreta and P. gossypiella). Spinosad activicty on the exocarpic bollworm species was at least equivalent to endosulfan as a reference: H. armigera (3.1 vs 3.4 larvae p. 30 plants), Earias spp, and D. watersi. Overall activity of spinosad against the exocarpic bollworm species was higher than deltamethrin. Indoxacarb activity was at the level of deltamethrin for H. armigera (4.9 vs 5.1 larvae p. 30 plants), and to a certain extent less effective against Earias spp. In contrast, the activity of both insecticides (spinosad and indoxacarb) on endocarpic species remained low in relation to deltamethrin (6.4 and 7.1 vs 3.2 endocarpic larvae p. 100 bolls, respectively for spinosad, indoxacarb, and deltamethrin). Effectiveness of spinosad and indoxacarb against sucking pests: Data presented in Figures 4a-d reveal compared activity of the pyrethroïd deltamethrin and the non pyrethroïd insecticides on cotton sucking pests J. fascialis, A. gossypii, D. voëlkeri, and the mite P. latus. The effect of spinosad was at least equivalent to deltamethrin on the jassid J. fascialis (1.2 vs 1 jassid attacked plants p. 30 plants) and on the mite P. latus (4 mite infested plants p. 3 rows). In contrast, spinosad appeared less effective than endosulfan against the aphid A. gossypii (56.8 vs 36.8 aphid infested plants p. 3 rows) and the cotton stainer D. voëlkeri (169 vs 140.8 Dysdercus p. 30 plants). Contrary to spinosad, the effect of indoxacarb was equivalent to deltamethrin on D. voëlkeri (110.3 vs 101.8 Dysdercus p.30 plants) and on the aphid A. gossypii (43.3 vs 48.8 aphid infested plants p. 3 rows) while showing less effectiveness compared to endosulfan against the mite P. latus (11.5 vs 2.4 mite infested plants p. 3 rows). Effectiveness of spinosad and indoxacarb against cotton leafworms: Data presented in Figures 5a-b show the compared effect of the pyrethroid deltamethrin and the non pyrethroïd insecticides on cotton leafworm S. littoralis and A. flava. Spinosad and indoxacarb proved very effective against the leafworm S. littoralis (0.7 and 0.8 vs 1.5 larvae p. 30 plants, respectively for indoxacarb, spinosad, and deltamethrin). Their activity of on A. flava remained equivalent to deltamethrin and endosulfan (1.2 and 2.2 vs 1.8 larvae p. 30 plants, respectively for spinosad, indoxacarb, and endosulfan). Activity of spinosad and indoxacarb on beneficials: Figures 6a-b show data on the compared activity of the pyrethroïd deltamethrin and the non pyrethroïd insecticides on beneficial predators. Spinosad and indoxacarb to a lesser extent proved safer on ladybirds, Coccinela spp., as compared to endosulfan (10.7 and 5.8 respectively for spinosad and indoxacarb vs 4 coccinellids p.30 plants). The effect of both insecticides on the spiders was equivalent to endosulfan (6.5 vs 7 spiders p.30 plants). Effectiveness of spinosad and indoxacarb in mixture with other insecticides: Data presented in Figures 7a-d showed compared activity of spinosad or indoxacarb based associations with profenofos and acetamiprid, and pyrethroïd based associations on cotton bollworms and some sucking pests. The profenofos based association with spinosad or indoxacarb provided an activity level at least equivalent to cypermethrin-profenofos association against H. armigera (0.3 and 1 vs 1.1 larva p. 30 plants, respectively for indoxacarb-profenofos, spinosad-profenofos and cypermethrin-profenofos). The same tendency was observed against the mite P. latus (0.1 and 2.5 vs 2.9 mite infested plants p. 3 rows). The acetamiprid based association with spinosad was at least equivalent to the cypermethrin-acétamiprid association against D. voëlkeri (74.2 vs 90.7 Dysdercus p. 30 plants). This association was much more effective against D. voelkeri than the indoxacarb-acetamiprid association (109.3 Dysdercus p. 30 plants). Concerning the endocarpic bollworm species (C. leucotreta & P. gossypiella) the spinosad-acetamiprid association showed an activity level equivalent to the cypermethrin-acetamiprid (4 vs 2 larvae p. 100 bolls) while the activity remained very low for the indoxacarb-acetamiprid association (9.5 larvae p. 100 bolls). DISCUSSION The present study pointed out the strengths and weaknesses of spinosad and indoxacarb with respect to major insect pests and beneficial species. The activity of spinosad and indoxacarb varied significantly according to insect pest species or beneficial species. The spinosad activity spectrum comprised exocarpic bollworm species (H. armigera, Earias spp, and D. watersi) and cotton leafworms S. littoralis and A. flava. It appeared to have a certain activity against the endocarpic bollworm species (C. leucotreta & P. gossypiella), the jassid J. fascialis, and the mite P. latus. This activity noticed especially on sucking pests such as the jassid J. fascialis and the mite P. latus need to be confirmed in more field trials, for the manual pesticide states that spinosad is non toxic to sucking pests. Indeed, spinosad appeared very limited against the aphid A. gossypii and the cotton stainer D. voëlkeri. With regard to benefials, spinosad proved safer to Coccinela spp and spiders. In contrast to spinosad, indoxacarb activity spectrum was restricted to a few bollworm species (H. armigera, D. watersi) and the cotton leafworm S. littoralis. In addition, it appeared to have a certain effectiveness against the jassid J. fascialis, the aphid A. gossypii, and the cotton stainer D. voëlkeri. Indoxacarb appeared somehow inactive on Earias spp., the mite P. latus, and the endocarpic bollworm species (C. leucotreta & P. gossypiella). On the basis of their activity spectrum and in the light of cotton crop phenology and seasonal occurence of main pests, differential pyrethroïd resistant management plans could be designed (Figures 8a-b) considering the positioning of spinosad and indoxacarb either at the vegetative or fruiting stages of cotton. Due to its high effectiveness on exocarpic bollworm species mainly H. armigera and Earias spp and its relative safety to major beneficials such as ladybird Coccinela spp, spinosad could be used preferably at cotton vegetative stage (45-66 d.a.e.). The relatively broad activity spectrum of spinosad makes it ideal for use at the vegetative stage of cotton, appearing as a true alternative to endosulfan. Its positioning at the late stage of cotton could be more suitable provided it would be used in association with other insecticides such as acetamiprid, effective against D. voelkeri and A. gossypii. Due to its activity spectrum, which is relatively restricted in relation to spinosad, indoxacarb appears more appropriate to the cotton fruiting stage (101-115 d.a.e) as it proved effective against the cotton stainer D. voelkeri while showing lower performance against Earias spp and the mite P. latus. Association of indoxacarb with other insecticides such as profenofos could enhance its activity mainly on the mite P. latus. The use of indoxacarb is not advisable during the period that coincides with maximum flowering for it had a limited effect on endocarpic bollworm species (C. leucotreta and P. gossypiella) which occur in largest numbers at this stage; it is therefore necessary to maintain a pyrethroid based association in order to control endocarpic bollworm species. Various benefits related to these new insecticides strongly advise their use as alternatives to pyrethroids. Still, to be more attractive, their activity needs to be reinforced by other insecticides in such a way as to control the whole arthropod pest complex. Conjoined laboratory activities are being achieved to help set more reliable strategies and improve the whole pest management strategy. Bioassays performed with several classes of insecticides, especially non pyrethroïd insecticides such as DDT, endosulfan, profenofos, indoxacarb, and spinosad did not show any cross-resistance with pyrethroids in H. armigera (Martin, unpublished data), knowing that pyrethroid resistance in H. armigera from West Africa was due to greater degradation of pyrethroids involving oxidases from the P450 family (Martin et al., 2002). CONCLUSION The earlier use of endosulfan and profenofos as pyrethroid alternatives in H. armigera resistance management in Côte d'Ivoire helped substantially reduce field infestations of H. armigera for the last four years. No resistance was detected for endosulfan and profenofos in field populations indicating the success of these pyrethroid alternatives. However, endosulfan and profenofos resistance was shown in H. armigera from Pakistan (Ahmad et al., 1995) and Australia (Forrester et al., 1993; Gunning et al., 1993) indicating the risk to select resistant larvae in Côte d'Ivoire if those insecticides are to be used for years without alternatives. For the pyrethroid resistance management to be sustainable, there is a clear need to adopt alternative insecticides such as spinosad and indoxacarb in a rational non pyrethroid insecticide rotation plan. Spinosad and indoxacarb could be used in appropriate resistance management programmes either alone or reinforced in mixture by other insecticides or in mosaic with endosulfan and profenofos in such a way to avoid the selection of new cases of resistance. ACKNOWLEDGEMENTS The authors acknowledge the research and development staff of cotton companies of Côte d'Ivoire (CIDT, IC, LCCI) and MM. Konan K. Jérôme, Kouadio René, and Kouadio Gérard of the cotton entomology technical research team of CNRA for their assistance in collecting field data. Thanks are due to chemical companies Dow AgroScience, Du Pont de Nemours, Aventis CropScience, and Syngenta for insecticide samples provided. REFERENCES Ahmad, M., Arif, M.I., Ahmad, Z. 1995. Monitoring insecticide resistance of Helicoverpa armigera (Lepidoptera Noctuidae) in Pakistan. Journal of Economic Entomology. 88 (4): 771-776. Forrester, N.W., Cahill, M., Bird, L. J. and Layland, J. K. (1993) Management of pyrethroid and endosulfan resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) in Australia. In Bull. Entomol. Res. Supplement Series N°1. International Institute of Entomology pp. 1-132. Gunning, R. V. and Easton, C. S. (1993). Resistance to organophosphate insecticides in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in Australia. General Applied Entomology, 25: 27-34. Martin, T., Ochou, G.O., Hala, N.F., Vassal, J.M. and Vaissayre, M. (2000). Pyrethroid resistance in the cotton bollworm, Helicoverpa armigera (Hübner), in West Africa. Pest Management Science, 56, 549-554. Martin, T., Chandre, F., Ochou, O. G., Vaissayre, M. and Fournier, D. (2002). Pyrethroid resistance mechanisms in the cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae) from West Africa. Pesticide Biochemical Physiology, 74 : 17-26. Martin, T., Ochou, O. G., Vaissayre, M. and Fournier, D. (2002). Positive and Negative Cross-resistance to Pyrethroids in Helicoverpa armigera from West Africa. Resistant Pest Management Newsletter, 12, 1. Ochou, O.G., Martin, T. and Hala, N.F (1998). Cotton insect pest problems and management strategies in Côte d'Ivoire, W. Africa. Proceedings of the world Cotton Research Conference-2. Athens, Greece, September 6-12, pp 833-837. Ochou, O.G. and T. Martin (2000). Prévention et gestion de la résistance de Helicoverpa armigera (Hübner) aux pyréthrinoïdes en Côte d'Ivoire. 2ème Rapport d'exécution technique du projet régional PR-PRAO. 93 p. Ochou, G. O. and Martin, T. (2002). Pyrethroïd Resistance in Helicoverpa armigera (Hübner): Recent Developments and Prospects for its Management in Côte d'Ivoire, West Africa. Resistant Pest Management Newsletter, 12, 1. Sawiki, R.M. and I. Denholm (1987). Management of resistance to pesticides in cotton pests. Tropical Pest Management 33 (4):262-272. Vaissayre, M., Vassal, J. M. and Martin, T. (1998). Pyrethroid resistance in the bollworm Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in West Africa. Proceedings of the World Cotton Research Conference-2. Athens, Greece, September 6-12, pp. 701-705 Vassal, J.M., M. Vaissayre and T. Martin (1997). Decrease in the susceptibility of Helicoverpa armigera (Hübner) (Lepidoptera : Noctuidae) to pyrethroid insecticides in Côte d'Ivoire. Resistant Pest Management, 9, 2, 14-15.
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