Somnath et al., IJAVMS Vol. 3, 2009:4-11

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1 Neem based Integrated Approaches for the Management of Tea Mosquito Bug, Helopeltis theivora Waterhouse (Miridae: Heteroptera) in Tea a useful qualitycontrol criterion Somnath Roy 1*, G.Gurusubramanian 2 and Ananda Mukhopadhyay 1 1 Entomology Research Unit, Department of Zoology, University of North Bengal, Darjeeling , West Bengal, India. 2 Department of Zoology, Mizoram Central University, Tanhril, Aizawl , Mizoram, India. The name and address of the institution where the work was done Entomology Research Unit, Department of Zoology, University of North Bengal, Darjeeling , West Bengal, India. Corresponding Author *Dr. Somnath Roy Entomology Research Unit, Department of Zoology, University of North Bengal, Darjeeling , West Bengal, India. entosomnath@yahoo.co.in ; entosomnath@rediffmail.com Fax No Short Running title : Neem based Integrated Approaches for the Management of Tea Mosquito Bug Accepted: May 13, 2009 Abstract Tea mosquito bug, Helopeltis theivora Waterhouse (Miridae: Heteroptera), has been the most destructive pest of tea in North East India since last few decades and the endeavour to control with common insecticides. In order to reduce the load of chemicals in tea, biopesticides, selection and usage pattern of pesticides along with effective spraying strategies, have been integrated for this purpose. The insecticidal property of the wonder tree neem, Azadirachta indica A. Juss. (Meliaceae), has come as a boon for solving many insect pest problems. Different azadirachtin concentrations were evaluated at different doses against the H. theivora to find out the variations of its bioefficacy. Sixty five per cent control of infestation was achieved at ppm azadirachtin concentration whereas 300 and 1500 ppm azadirachtin concentrations gave less than 30% control. Further in case of 3000 and ppm, azadirachtin concentration 30% to 43% reduction was registered. Therefore Azadirachtin concentration and its quality are the major criteria for getting desired bioactivity in all neem formulations. The combination treatments with commonly used conventional insecticides (neem + endosulfan or neem + deltamethrin) had recorded significant reduction in H. theivora incidence even at reduced doses, when compared to sole use of neem formulations or sole insecticidal treatments at recommended doses. Effectiveness and utilization of neem formulation against tea mosquito bug are also discussed. Key Words: Neem formulation; azadirachtin concentration; bioactivity; tea mosquito bug; tea, Helopeltis theivora. Introduction The neem tree, Azadirachta indica A. Juss. (Meliaceae), has been widely studied because it presents a great number of compounds with insecticidal properties and is effective on reducing population of several pest species 6, 13, 20, 21, 22. Its main active compound, azadirachtin, is toxic to over 500 insect species and acts mainly as food deterrent and growth disruptor. Martinez and Van Emden 9 obtained longer period of the larva and reduced larval activity of insect treated with sub-lethal doses of azadirachtin. This insect static

2 effect, also observed in other species 17 favors the association of the neem products with biological control, because it extends the exposure time of the pests to natural enemies 10. Another factor favorable to this association is the fact that azadirachtin presents higher toxicity by ingestion than by contact 8, 11. This makes this compound potentially less toxic to natural enemies in the field 4. Neem is widely used in several countries around the world today either singly in Integrated Pest Management or in conjunction with synthetic pesticides. In spite to that neem is not widely accepted by Indian tea planters, largely because its efficacy is highly variable. In market different neem formulations are available from 300 ppm (0.03 % Azadirachtin) to 50,000 ppm (5.0 % Azadirachtin). Isman et al. 5 envisaged that as azadirachtin concentration of neem oil varies widely and is highly correlated to bioactivity against pest species. In recent years, labour costs have risen steeply, to as much as per cent of total garden expenditure. This and other factors have necessitated greatly enhanced yields per hectare in order to lower costs of production. Increased yields, together with greater appreciation of the losses caused by pests and diseases, have brought the need for controlling their ravages into considerable prominence. The tea mosquito bug, Helopeltis theivora (Waterhouse) (Het.: Miridae), is an important pest of the plantation crops, tea (Camellia sinensis) causing substantial (10-50%) loss in crop. In North east India out of 4.36 lakh hectares of total tea plantation 80% of tea plantations have been suffering from H. theivora infestation. Greater awareness among the planters regarding the drawbacks associated with synthetic insecticides forced the scientific community to look for safer alternatives or reduce the load of the pesticides by any other means. The Maximum Residue Limit (MRL) for most of the chemicals in EU has been fixed at 0.1 and below, which has been a major constraint to tea exporting countries like India 1. Following increasing reports from planters that insecticides are becoming less effective against the tea mosquito bug in Northeast India. According to recent report by Bora and Gurusubramanian 3 and Roy et al. 18 the effective field dosages of commonly used insecticides were computed based on recent LC values 50 of H. theivora, and when compared with the recommended dosages, it suggested about folds decrease in the susceptibility of the test population. The decrease in susceptibility of H. theivora to deltamethrin and endosulfan was the largest. With this likely future in mind, reducing dependence on chemical pesticides in favour of ecosystem manipulations is a good strategy for planters. Hence in this study an attempt was made to explore the potential and utilization of neem by quantify the bioactivity of different azadirachtin concentrations (300, 1500, 3000, 10,000 and 50,000 ppm) against the tea mosquito bug and the effect of neem formulations combined with insecticides against the pest with same recommended dose and reduced doses of endosulfan and deltamethrin on infestation level. Materials and methods Collection and Preparation of different concentrations of Azadirachtin content: Samples of different azadirachtin concentrations (300, 1500, 3000, 10,000 and 50,000 ppm) were obtained from Entomology Research Institute, Loyola College, Chennai, India which were analyzed for azadirachtin concentration through HPLC. From the respective azadirachtin content sample five dilutions were prepared ( 1:200, 1:300, 1:500, 1:1000 and 1:1500) and tested against H. theivora, Field Evaluation of Azadirachtin concentration and their bioactivity against H. theivora: A field trial was conducted in (Sep - Oct 2005) at North Bengal university experimental station in Darjeeling, India to evaluate the efficacy of different azadirachtin concentrations (300, 1500, 3000, 10,000 and 50,000 ppm) at different dilutions (1:200, 1:300, 1:500, 1:1000 and 1:1500) against H. theivora along with untreated control. TV1 and TV9 (100 x 65 cm space) mixed plots were chosen for the current study by following Randomized Block Design with three replications. Each plot in the experiment was separated by two buffer rows of non-experimental tea. 100 bushes per replication were considered for each treatment of different dilutions of azadirachtin concentrations. Plots with heavy infestation of H. theivora were chosen for this study. After selection of the plots, pretreatment count was taken in the respective plots and two rounds of foliar spray were given at 15 days interval with hand operated Knapsak 400 litres/ha. Post treatment observations were taken for four weeks after treatment.

3 Bioefficacy of Neem formulations combined with reduced dosages of insecticides against H. theivora in tea: Randomized block design field trials were laid out at North Bengal university experimental station in Darjeeling, India to study the bioefficacy of Neemazal F 5 EC alone and in combination with monocrotophos and endosulfan at different dilutions against H.theivora. The control plot was treated with water spray. The treatments were applied at fortnightly interval with Knapsak 400 litres/ha. Pre and post observations were made at weekly interval for four weeks. Infestation of H.theivora was assessed on the basis of collection of infested and uninfested shoots from each replicate of the treatment. After that per cent infestation and per cent reduction were calculated by using the following formulae: Infested shoots/replicate Per cent infestation = x 100 Total No. of shoots/replicate Pretreatment Post treatment per cent infestation per cent infestation Per cent reduction = x 100 Pretreatment per cent infestation Results Relative insecticidal value of azadirachtin concentration and Bioefficacy of Neem formulations against H. theivora The bioactivity of different azadirachtin concentrations (300, 1500, 3000, 10,000 and 50,000 ppm) at different dilutions (1:200, 1:300, 1:500, 1:1000 and 1:1500) under field conditions against H. theivora was noted and summarized in table 1. During first and second week after first spraying of different azadirachtin concentration the reduction of H. theivora was recorded at a minimum of 3.4 % to the maximum of 36.9 % at the respective dilutions. But after the second round of spray the per cent reduction in infestation was increased to the tune of 22.5 % % in all the dilutions during III and IV week (table 1). After completion of two rounds of foliar spraying of different azadirachtin concentrations per cent reduction ranged from , , , , and % at 1:1500, 1:1000, 1:500, 1:300 and 1:200 dilutions. Significant difference (p<0.05) was noticed between dilutions, azadirachtin concentration and its interactions (table 1). The percent reduction in H. theivora infestation was in ascending trend with respect to azadirachtin concentration as well as dilutions. At higher dilutions (1:1500) i.e. 300 and 1500 ppm azadirachtin concentration gave <30% reduction; and >30% - <43% reduction was registered at 3000, 10000, and ppm of azadirachtin concentration, whereas >50% - < 65% reduction was observed at a lower dilution (1:200) (table 1). Bioefficacy of neem formulations combined with deltamethrin and endosulfan against H. theivora in the Dooars condition First spray of TRA recommended doses i.e. 1:1600 and higher con. Than recommended dose i.e. dilutions 1:500 of neem formulations (Neemazal F 5 EC) gave % and % reduction in H. theivora population in I & II week respectively, which later increased to % and % in III & IV week respectively.

4 Table 1. Different Azadirachtin concentrations and their impact on infestation pattern of H. theivora Parent concentration of Azadirachtin Dilution of different azadiracht in content Per cent reduction in infestation over pre treatment in different week 1 st week 2 nd week 3 rd week 4 th week 300 PPM 1: *(10.63) 3.2(10.30) 22.5(28.32) 26.4(30.92) 1: (12.38) 4.1(11.68) 26.6(31.05) 29.5(32.90) 1: (16.22) 6.8(15.12) 29.4(32.83) 33.6(35.43) 1: (17.36) 7.4(15.79) 38.2(38.17) 39.5(38.94) 1: (17.05) 6.8(15.12) 41.4(40.05) 45.4(42.36) 1500 PPM 1: (19.19) 8.6(17.05) 26.5(30.98) 29.8(33.09) 1: (20.88) 10.9(19.28) 30.2(33.34) 34.6(36.03) 1: (22.30) 12.2(20.44) 34.6(36.03) 39.0(38.65) 1: (24.65) 12.6(20.79) 38.9(38.59) 41.4(40.05) 1: (24.95) 13.6(21.64) 44.2(41.67) 47.7(43.68) 3000 PPM 1: (24.27) 12.8(20.96) 28.5(32.27) 32.4(34.70) 1: (25.77) 14.1(22.06) 38.4(38.29) 42.6(40.74) 1: (27.56) 18.6(25.55) 42.6(40.74) 45.8(42.59) 1: (29.73) 19.4(26.13) 47.0(43.28) 50.6(45.34) 1: (31.82) 21.4(27.56) 50.2(45.11) 59.6(50.53) PPM 1: (25.77) 16.8(24.20) 35.0(36.27) 38.9(38.53) 1: (26.42) 19.2(25.99) 38.8(38.53) 46.4(42.94) 1: (29.73) 21.4(27.56) 44.4(41.78) 48.6(44.20) 1: (31.88) 23.4(28.93) 49.6(44.77) 57.2(49.14) 1: (33.09) 28.3(32.14) 54.6(47.64) 57.5(49.31) PPM 1: (30.79) 21.3(27.49) 40.5(39.52) 42.4(40.63) 1: (3.09) 24.6(29.73) 46.4(42.94) 45.4(42.36) 1: (34.70) 29.3(32.77) 51.4(45.80) 56.6(48.79) 1: (37.35) 31.6(34.20) 56.2(48.56) 60.8(51.30) 1: (37.41) 33.2(35.24) 59.4(50.42) 65.4(53.91) CD (0.05)

5 CV (%) CD Critical Difference (p<0.05); CV Coefficient of Variation; Data within the parentheses are angular transformed values, which were used for analysis. * Average of the three replications The following spray with endosulfan at recommended doses brought in a reduction of % in I & II week and % in III & IV week Deltamethrin resulted in reduction of H. theivora population by % in I & II week and % in III & IV week (table 2). Neemazal + 1: :2000 1: :3000 dose caused population reduction to the tune of % and % in I & II week and % and % in III & IV week respectively. When neemazal combined with 1:600+1:400 1:600+1:600 doses were applied the H. theivora infestation was reduced to the tune of % and % in I & II week and % and % in III-IV week respectively (table 2). The combination treatments, therefore recorded a significant reduction of H. theivora incidence compared to use of neem alone. It was also noted that with the reduced dose of insecticides in combination with neem formulations gave significant control of H. theivora population (table 2). Table 2. Effect of Neem formulations with different doses of insecticides on H. theivora Treatment Dilution Per cent reduction in infestation over pre treatment in different week Endosulfan 1: * (29.60) Deltamethrin 1: (47.43) Neemazal 1: (34.60) Neemazal 1: (25.52) Neemazal + Endosulfan Neemazal + Endosulfan Neemazal + Deltamethrin Neemazal + Deltamethrin 1:600+1: (53.25) 1:600+1: (46.59) 1:600+1: (71.89) 1:600+1: (60.47) Control Water spray 4.2 (13.96) 1 st week 2 nd week 3 rd week 4 th week 5.2 (13.03) 23.7 (31.52) 29.3 (32.74) 24.1 (28.56) 48.5 (44.12) 44.4 (41.79) 85.4 (67.56) 63.1 (52.69) 1.4 (3.95) 9.6 (19.05) 64.7 (52.09) 51.4 (43.37) 43.1 (43.62) 62.5 (50.24) 60.1 (50.37) 89.5 (70.89) 75.2 (57.04) (23.10) 12.8 (20.77) 37.3 (37.57) 56.6 (48.80) 24.1 (29.53) 56.5 (48.76) 54.5 (47.56) 93.5 (75.38) 70.5 (51.11) (-26.62) CD (p = 0.05) CV (%)

6 CD Critical Difference (p<0.05); CV Coefficient of Variation; Data within the parentheses are angular transformed values, which were used for analysis. * Average of the three replications Discussion The present study hints at a possible relationship between bioactivity of different azadirachtin concentrations and pest (H. theivora) damage. Among five different concentrations only 50,000 ppm resulted in the maximum (65%) control of H. theivora at higher dilutions (1:200). As H. theivora is having the sucking type of mouth parts selective and reduced ingestion toxicologically active compounds may be the reason for a lesser control. This observation can be well validated with the findings of Lowery and Isman 8 and Martinez-Carvalho 11. Schmutterer 21 concluded that a foliar spray application of most commercial Neem formulations persists 5-7 days under field conditions or possibly a little longer due to some systemic effects, and the present result corroborate the foregoing observation, and possibly that is why a reduction in infestation of H. theivora after about a week of the first spray was evident. Even though breakdown of azadirachtin occurs in UV light, its metabolites may still have bioactivity 2. Dihydroazadirachtin, a compound obtained by hydrogenation of the C-22, 23 double bond of the hydroxy-furan fragment of azadirachtin, currently shows promise as a more stable compound for better field persistence 14. In this study, different azadirachtin contents were tested against H. theivora and significant variations were obtained between azadirachtin concentration and bioactivity. Concentrated extracts of Azadirachtin ranged from 1.4% to 20.9%, whereas the azadirachtin concentrations in the neem oils tested by Isman et al. 5 ranged from 0.2% to 0.4%. Results of Isman et al. 5 hint that neem oils containing azadirachtin at levels of 2000 ppm or greater have sufficient bioactivity for their utilization in the preparation of neem based insecticides. In the present trial bioactivity of azadirachtin 5% (50000 ppm) against H. theivora suggested that azadirachtin concentration should constitute a useful quality-control criterion for the acceptability of neem oil as a precursor for a formulating botanical insecticide. The market for neem-based pesticides will increase, as the farmers become aware of benefits and also due importers insistence on residues. Several stringent measures had been taken by CIB and tea board who approve only 5% azadirachtin formulations (50000 ppm) as pesticide. The current study also revealed the fact that azadirachtin concentration is the determining factor in terms of its bioactivity, i.e., in controlling the pest. The bioactivity of azadirachtin concentrations may vary from insect to insect. In tea, using of 5% azadirachtin is ideal for getting desired control of 60-65% of H. theivora at 1:200. Combining biorotational products with synthetic pesticides often help to minimize the application rate of conventional active ingredients and still retain their benefits such as long residual activity. Recent studies by Rahaman et al. 15 reported that neem formulations combined with reduced dosages of acaricides and insecticides are found effective against Oligonychus coffeae and Scirtothrips dorsalis in tea. Miller 12, Sarode et al. 19 and Lindquist 7 have found similar result. Comparative assessment of nimbicidine in combination with or without endosulfan on the growth, development and histomorphology of Helicoverpa armigera, Spodoptera litura and Gangara thyrsis, revealed that more pronounced effects takes place in combination treatments than individual treatments 16. Sarode et al. 19 conducted laboratory experiment to workout relative toxicity of neem seed extract in combination with reduced doses of endosulfan, monocrotophos, quinalphos, carbaryl and fenvalerate against H. armigera and found that combination treatments registered higher kill than treatment of neem seed extract. The combination of neemazal 5 EC (1:600) with deltamethrin (1:2000) was superior to other combinations in terms of controlling the Helopeltis population. Similarly, endosulfan in combination with neemazal also registered desirable percent reduction at full dose. These studies illustrated that biorational insecticides especially neem, alone or at reduced rates in combination with synthetic insecticides, could play a vital role in a tea pest management program. Therefore, the following integrated pest management practices must be followed for combating problem of Helopeltis infestation so that it does not assume unmanageable proportions:

7 1. After infestation remove all the infested shoots to rejuvenate the shoot growth as well as to remove the laden eggs before spraying. 2. In severe infestation LOS (level of skiff) operation should be followed to minimize the infestation of the next generation. 3. Shade status neither should be overshaded nor unshaded. 4. Alternate hosts must be eliminated [Guava (Psidium guajava), oak (Quercus spp.), melastoma (Melastoma sp.), Thoroughwort (Eupatorium sp.), fragrant thoroughwort (Eupatorium odoratum), Dayflower (Commelina spp.), Sesbania (Sesbania cannibina), Jackfruit (Artrocarpus heterophylla), Bortengeshi (Oxalis acetocello), Ornamental jasmine (Gardenia jesminoid), Mulberry (Morus alba), Kadam (Enthocephalus cadamba), Jamun ( Eugenia jambolana), Boal (Ehretia acuminata), Mikania (Mikania micrantha), Acacia moniliformis and Premna latifolia)]. 5. By following proper monitoring detect the H. theivora at an early stage and manually collect the adults (Morning h h; Evening h h) by the trained labour force. 6. Unpruned sections must be monitored regularly during December-February and proper care should be taken to kill the residual population. 7. At most care need to be adopted in skiffed and pruned sections during bud breaking (March April) which are prone to H. theivora attack. 8. Underperformance of spraying equipments should be avoided. 9. Selection and usage of chemicals, assurance of the quality, required spraying fluid, and trained man power for overall good coverage. 10. Under dense tea bush population care must be taken for good and uniform coverage of chemicals. 11. Incompatible chemicals must be avoided in tank-mix formulations in severely affected sections. 12. Recommended dose of chemicals should be followed and avoid sub- and supra- lethal doses to minimize the chances of susceptibility change in H. theivora populations. 13. Avoid spraying during hot sunny days which degrade the chemical activity, cause phytotoxicity, and no direct contact with insects. Hence prefer early morning and late afternoon. 14. With prior knowledge about H. theivora infestation pattern, mark the infested bushes in the early stage and go for spot application to check the pest as well as to reduce the chemical load instead of blanket application. 15. Conserve and preserve the natural enemies present in the natural tea ecosystem by minimizing the load of chemicals for their natural regulation. References 1. Anonymous: Note on European Tea Committee Surveillance of Pesticides in origin Teas. Report of Pesticide Residue European Tea Committee Surveillance (2004). 2. Ascher KRS, Nonconventional insecticidal effects of pesticides available from the Neem tree, Azadirachta indica. Arch. Insect Biochem. Physiol., 1993; 22: Bora S, Gurusubramanian G, Relative toxicity of some commonly used insecticides against adults of Helopeltis theivora Waterhouse (Miridae: Hemiptrra) collected from Jorhat area tea Plantations, South Assam, India. Resist. Pest Manag Newsl. 2007; 17(1): Flavia AC, Silva DA, Martinez S, Effect of neem seed oil aqueous solutions on survival and development of the predator Cycloneda sanguinea (L.) (Coleoptera: Coccinellidae). Neotrop. Entomol 2004; 33 (6): Isman MB, Koul O, Luczynski A, Kaminski J, Insecticidal and antifeedant bioactivities of Neem oils and their relationship to azadirachtin content. J. Argi. Food Chem 1990; 38: Jacobson M Focus on phytochemical pesticides, Volume 1, The Neem Tree. CRC Press, Boca Raton, FL, 1998; 178.

8 7. Lindquist, R.: Thrips Cocktail for the Year Floriculture. Available at: http.// www. osu. edu/ archive/apr00/cocktail.html,1-5 Accessed Sept. 20, Lowery DT, Isman MB, Toxicity of neem to natural enemies of aphids. Phytoparasitica 1995; 23: Martinez SS, Van Emden HF, Growth disruption, abnormalities and mortality of Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) caused by azadirachtin. Neotrop. Entomol 2001; 30: Martinez S S, O nim - Azadirachta indica - natureza, usos múltiplos, produção. Londrina, IAPAR, 2002; Martinez-Carvalho S, Effects of sublethal concentrations of azadirachtin on the development of Spodoptera littoralis. Tese de doutorado, University of Reading, 1996; Miller F, Tank-mixing insecticides can reduce rates. Ground maintenance, grounds. Available at. http.// www. mag.com/mag/ grounds_maintenance _tankmixing_ insecticides_ reduce: 1997; 1-3. Accessed Sept. 20, Mordue AJ, Nisbet AJ, Azadirachtin from the neem tree Azadirachta indica: Its actions against insects. An. Soc. Entomol. Brasil 2000; 29: Mordue AJ, Blackwell A, Azadirachtin: an update. J. Insect Phys 1993; 39: Rahman A, Sarmah M, Gurusubramanian G, et al. Bioefficacy of Neem formulations combined with reduced dosages of acaricides and insecticides against Oligonychus coffeae Nietner and Scirtothrips dorsalis Hood in tea. J. Plant Crops 2007; 35(1): Ramarethinam S, Marimuthu S, Murugesan NV, et al. Effect of a neem oil formulation on the growth, development and histomorphology of some lepidopteran pest (Helicoverpa armigera H.; Spodoptera litura F.; and Gangara thyrsis). Pestology 2000; 24 (10): Rembold H, Effect on viruses and organisms growth and metamorphosis. Schmutterer H. ed. The neem tree, Weinheim, VHC, 1995; Roy S., Mukhopadhyay A., Gurusubramanian G, et al. Susceptibility status of Helopeltis theivora Warerhouse (Heteroptera: Miridae) to the commonly applied insecticides in the tea plantation of the Sub-Himalayan Dooars area of North Bengal India. Resistance Pest Manage Newsl 2008; 18(1): Sarode SV, Jatkar NS, Sonalkar VU, et al. Bioefficacy of neem seed extract combined with reduced dosages of insecticides against Helicoverpa armigera (Hubner). Pesticide Res J 2000; 12(2): Saxena RC, Neem seed derivatives for management of rice insect pest- a review of recent studies. In: Schmutterer H, Ascher KRS, eds. Proceeding of the Third International Neem Conference, Nairob, Kenya, GTZ, Eschborn. 1997; Schmutterer H, Properties and potential of natural pesticides from the Neem tree, Azadirachta indica. Ann Rev Entomol 1990; 35: Schmutterer H, The neem tree: Source of unique natural products for integrated pest management, medicine, industry and other purposes. VCH, Weinheim, 1995; 696.