Side effect of some Neem products on natural enemies of Helicoverpa ( Trichogramma spp.) and Chrysoperla carnea

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Archives of Phytopathology and Plant Protection December 2006; 39(6): 445 – 455

Side effect of some Neem products on natural enemies of Helicoverpa (Trichogramma spp.) and Chrysoperla carnea

N. E. EL-WAKEIL1,2, N. M. GAAFAR1,2, & S. VIDAL2 1

Pests & Plant Protection Department, National Research Centre, Cairo, Egypt, and 2Institute of Plant Pathology, George-August University, Goettingen, Germany (Received 30 July 2005)

Abstract The present work was conducted to evaluate the side effect of Neem products as natural insecticide on some of natural enemies of Helicoverpa armigera Hu¨b. (Trichogramma spp. and Chrysoperla sp.). The work is divided into laboratory and greenhouse experiments. The laboratory experiments dealt with the side effects of Neem products: NeemAzal-T/S, NeemAzal Blank, NeemAzal PC 05 and NeemAzal PC 05 Blank on Trichogramma spp. and C. carnea (Stephen). Neem concentrations: 2, 1, 0.5 and 0.25% were arranged in a completely randomized block design and each treatment was replicated at least six times. Parasitism and emergence rates of T. pretiosum (Riley) and T. minutum (Riley), and predation rates of C. carnea and its longevity were investigated. The greenhouse experiments dealt with the side effects of Neem products on parasitism rates of T. pretiosum and T. minutum on three different cotton cultivars. There were no serious side effects on parasitism and emergence rates of Trichogramma spp. and on efficiency of Chrysoperla. Similarly, Neem products achieved a good control of H. armigera in laboratory and greenhouse. Therefore, Neem products are recommended for controlling Helicoverpa, and are compatible with mass release of Trichogramma and Chrysoperla for organic cotton production. Future field experiments are suggested to further elucidate the effects of Neem on H. armigera and its natural enemies.

Keywords: Neem, Helicoverpa, Trichogramma, Chrysoperla, laboratory, greenhouse

Introduction Studying side effects of pesticides on beneficial arthropods is very important to test the suitable techniques and standard methods, which are urgently needed, for sound integrated pest managements (IPM; Kakakhel & Hassan 1998). Despite the sensitivity of insects of most orders to azadirachtin, Neem products are selective, as they do not harm important natural enemies of pests (Isman & Port 1990). They are also non-toxic to warm-blooded animals. Neem-seed extracts have, therefore, a considerable potential for integrated pest control measures (Schmutterer 1988). Neem has systemic activity, it is active at low concentrations and degrades rapidly in the environment (Schmutterer 1988, 1990). The side effect test revealed that NeemAzal-T/S is harmless to numerous natural enemies. The test was based on Correspondence: N. E. El-Wakeil, Pests and Plant Protection Department, National Research Centre, 31 El-Tharir Street, 12622 Dokki, Cairo, Egypt. Tel: þ202-734-0110. Fax: þ202-337-0931. E-mail: [email protected] ISSN 0323-5408 print/ISSN 1477-2906 online ª 2006 Taylor & Francis DOI: 10.1080/03235400500356160

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the evaluation of the survival of the larvae, their development and pupation, and the fecundity and fertility of the resulting adults (Natarajan 1990; Salem & Matter 1991; Kaethner 1991; Kienzle & Zebitz 1996; Vogt et al. 1997). The results of laboratory experiments conducted to study the effect of Neem formulations compared with insecticides on Trichogramma species, based on the rate of parasitization and emergence of adults from parasitized eggs, revealed that Neem products were safer compared with insecticides (Klemm & Schmutterer 1993; Lakshmi et al. 1997; Zhang MinLing 1997; Dodan & Roshan 1999; Markandeya & Divakar 1999; Thakur & Pawar 2000; Prabal & Parameswaran 2001). Raguraman & Singh (1999) tested Neem seed oil at concentrations of 5.0, 2.5, 1.2, 0.6 and 0.3% for oviposition deterrence, feeding deterrence, toxicity, sterility and insect growth regulator effects against T. chilonis Ishii. Neem seed oil at 0.3% deterred oviposition (parasitization) by the parasitoid. Neem seed oil also deterred feeding at or above 1.2% concentration. In feeding toxicity tests, Neem seed oil at 5% concentration caused 50% mortality to both males and females. Schuster & Stansly (2000) tested Azatin EC on two species of green lacewings; they found that the Neem product was not toxic to eggs, larvae and adults, topically or residually. On the other hand, NeemAzal-T/S (formulation dried residues on glass panes) was harmful to larvae of the lacewing C. carnea (Stephen) causing mortality and difficulties with moulting (Hermann et al. 1997; Schmutterer 1997; Srinivasan & Babu 2000). The longevity of treated adults by some Neem products ranged between 18.66 and 20.66 days, while it was 23.66 days in controls. Fecundity was also affected slightly by all Neem products (599.66 – 741.66 eggs) as against 874.66 eggs in controls (Karuppuchamy et al. 1998; Deole et al. 2000). The results of using parasitoids and predators in integrated pest management of H. armigera in cotton fields to investigate egg parasitism, and toxicity of insecticides to parasitoids and predators, revealed that egg parasitism in the laboratory by T. chilonis were 75.6% (Raja et al. 1998). Nimbecidine (Neem product) tested against T. chilonis and C. carnea resulted in zero mortality. The integrated pest management components (T. chilonis, C. carnea and nimbecidine) gave good control of H. armigera (Reddy & Manjunatha 2000). Therefore, we will study the side effects of Neem products on: . parasitism rates of T. pretiosum (Riley) and T. minutum (Riley) in the laboratory and greenhouse; . emergence rates of T. pretiosum and T. minutum in the laboratory; . on predation rates and longevity of C. carnea in the laboratory.

Material and methods Insects The Helicoverpa eggs used throughout this study were obtained from a culture in the laboratory. Larvae were reared on a modified diet according to Shorey & Hala (1965), at a regime of 278C, 70%RH and a photoperiod of 16:8 (L:D). Trichogramma pretiosum and T. minutum were provided by the Institute of Biological control (BBA), Darmstadt, and were reared on Sitotroga eggs. The stock of C. carnea was ordered ¨ RE Bio-protect Company (Germany), and maintained in a climatic cabinet at from O 25 + 28C, 70%RH and 16:8 h L:D).

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Plants Three different cotton cultivars (Giza 89, Giza 86 and Alex 4) were cultivated in a controlled greenhouse for use in the greenhouse experiments. Neem products NeemAzal-T/S, NeemAzal blank, NeemAzal PC 05 and NeemAzal PC 05 blank were provided by Trifolio – M GmbH (Germany). Four concentrations were used: 2, 1, 0.5 and 0.25%. Effect of Neem products on parasitism of Trichogramma spp. on Helicoverpa eggs in the laboratory. The purpose of this study was to investigate whether Trichogramma parasitoids could parasitize treated eggs if the farmer sprayed the Neem products before releasing the Trichogramma. Twenty Helicoverpa eggs were sprayed with different concentrations of Neem product and left for 20 min to dry. After that, they were exposed to Trichogramma species (20 parasitoid females per 20 Helicoverpa eggs) into 40-ml glass vials. After 4 – 6 days, the black eggs were recorded to calculate parasitism rates. Replications were six vials for each Neem concentration. Emergence rates of Trichogramma spp. from treated parasitized eggs in the laboratory. The purpose of this study was to investigate whether Trichogramma wasps could emerge from treated eggs if the farmers sprayed the Neem products after parasitization by Trichogramma occurs. Ten parasitized Helicoverpa eggs were sprayed with four different concentrations of Neem products and left for 20 – 30 min to dry, then put into 40-ml glass vials. After 4 – 5 days, the emerged parasitoids were counted to calculate the emergence rates. This was replicated six times for each concentration. Parasitism of Trichogramma spp. on Helicoverpa eggs on three cotton cultivars. Ten Helicoverpa eggs were sprayed with four different concentrations of each Neem product, left to dry, then attached onto the first, third and fifth leaves on the cotton plants. These plants were placed in wood cages in the greenhouse, then exposed to Trichogramma spp. at a ratio of two parasitoid females to each host egg. After 24 h, these eggs were collected and incubated at 278C, RH 70% and L:D 16:8. After 4 – 5 days, the black eggs were counted to calculate the parasitism rates. Three plants were used as replications for each cotton cultivar per treatment. Predation rates of Chrysoperla on Helicoverpa egg in the laboratory. Ten treated Helicoverpa eggs were sprayed with four different concentrations of Neem products. After drying, the treated eggs were put into 50-ml glass vials with Chrysoperla larva to study effect of Neem on predation rates on Helicoverpa eggs. The Helicoverpa eggs were examined daily, the number of eggs consumed was calculated and enough new treated eggs added to maintain the Chrysoperla larvae until pupation. Six vials were used for each Neem concentration. Effect of Neem products on the longevity of Chrysoperla larvae instars. Longevity of each three larval instars of Chrysoperla was calculated in each treatment, to test effects of Neem products on development of Chrysoperla larvae. Statistical analysis Statistical analyses were conducted using analysis of variance (ANOVA), and following with Tukey test to compare means of treatments with control, significant differences were noticed

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for p 5 0.05 for all trials using Program SYSTAT 8 (Wilkinson et al. 1998). The percentage data were arcsine transformed prior to analysis. Results Effect of Neem products on parasitism of Trichogramma spp. on Helicoverpa eggs in the laboratory NeemAzal-T/S reduced parasitism rates of T. pretiosum by 50, 60, 66.7 and 80% at concentrations of 2, 1, 0.5 and 0.25%, respectively (Figure 1A). NeemAzal PC 05 reduced parasitism rates to 66.7, 70.8, 71.7 and 83.3%, respectively, on subsequent concentrations, while parasitism rates were reduced in NeemAzal Blank concentrations to 70, 75.8, 86.7 and 95%. There was no obvious effect on parasitism rates with NeemAzal PC05 Blank; the latter reduced the parasitism rates to 88.3, 91.8, 95.8 and 96.7%, while parasitism rates were 100% at control. The effect of Neem on T. minutum is in similar to T. pretiosum, as shown in Figure 1B. NeemAzal-T/S had a similar effect on parasitism rates of T. minutum on H. armigera eggs; parasitism rates were reduced to 40, 43.3, 51.7 and 80% (2, 1, 0.5 and 0.25% concentrations). NeemAzal PC 05 reduced the parasitism rates to 55, 75, 77.5 and 90.8% on four consequent concentrations, respectively, while NeemAzal Blank reduced the parasitism rates by 70, 84.2, 90.8 and 95.8%. Parasitism rates in NeemAzal PC05 Blank treatment were reduced to 92.5, 77.4, 95.7 and 97.5% at four concentrations, compared with 98.3% at control (Figure 1B). Emergence of Trichogramma spp. from treated parasitized eggs in the laboratory In Figure 2A the results indicated that the emergence rates of T. pretiosum from parasitized Helicoverpa eggs treated with NeemAzal-T/S were 78.3, 90, 93.3 and 100% for 2, 1, 0.5 and 0.25% concentrations, respectively. NeemAzal PC 05 reduced the emergence rates to 80, 90, 91.7 and 100% at the same concentrations. While both blanks had the least effect on emergence rates, they were 80, 91.7, 100 and 100% in NeemAzal Blank, and 95, 95, 100 and 100% in NeemAzal PC05 Blank at succeeding concentrations compared with 100% at control. The emergence rates of T. minutum from parasitized Helicoverpa eggs treated with NeemAzal-T/S were 65, 80, 83.3 and 93.3% for 2, 1, 0.5 and 0.25% concentrations, respectively, as shown in Figure 2B. NeemAzal PC 05 reduced the emergence rates to 78.3, 81.7, 88.3 and 96.7% at the same concentrations. Emergence rates in NeemAzal Blank treatment were 80, 86.7, 90 and 90%, and in NeemAzal PC05 Blank were 83.3, 88.3, 93.3 and 100% at subsequent concentrations compared with 100% in the control (Figure 2B). Parasitism rates of T. pretiosum on Helicoverpa eggs on three cotton cultivars The results indicated that NeemAzal-T/S reduced the parasitism rates to 50, 48.9, 71.1 and 73.3% at 2, 1, 0.5, 0.25% concentrations, respectively, on Giza 89 cultivar (Figure 3A). On Giza 86 cultivar parasitism rates were reduced to 48.8, 51.1, 53.3 and 83.3%, and on cultivar Alex 4 they were 42.2, 53.3, 54.4 and 87.7% compared with 96.6, 93.3 and 97.7% on control plants for succeeding cotton cultivars (Giza 89, Giza 86 and Alex 4). NeemAzal PC 05 reduced the parasitism rates to 70, 67.8, 70 and 80% on Giza 89 cultivar, to 65.3, 58.9, 80 and 78.8% on Giza 86 cultivar, and to 84.4, 64.4, 82.2 and 88.8% on Alex 4 cultivar on concentrations of 2, 1, 0.5 and 0.25%, respectively. Neem blanks had less effect on T. pretiosum. NeemAzal Blank reduced the parasitism rates to 81.1% on Giza 89, 80.7% on Giza 86 and 84.4% on Alex 4. NeemAzal PC05 Blank reduced the parasitism rates to 93.3% on Giza 89, 90% on Giza 86 and 97.7% on

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Figure 1. Effect of Neem products on parasitism rates of Trichogramma species on H. armigera eggs in the laboratory.

Alex 4, compared with 95.6, 93.3 and 98.7%, respectively, on control plants for succeeding cotton cultivars Giza 89, Giza 86 and Alex 4 (Figure 3A). Parasitism rates of T. minutum on Helicoverpa eggs on three cotton cultivars The results indicated that NeemAzal-T/S had reduced the parasitism rates, to 40, 55.4, 77.8 and 81.3% at concentrations of 2,1, 0.5, 0.25%, respectively (Figure 3B) on Giza 89 cultivar respectively, while parasitism rates were reduced to 43.3, 55.5, 61.1 and 76.6% on Giza 86, and 58.8, 68.8, 78.8 and 87.7% on Alex 4 cultivar, compared with 93.3, 92.2 and 93.3% on control plants for successive cotton cultivars Giza 89, Giza 86 and Alex 4. NeemAzal PC 05

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Figure 2. Effect of Neem products on emergence rates of Trichogramma species from parasitized H. armigera eggs.

reduced the parasitism rates to 82.2, 82.2, 74.4 and 83.3% on Giza 89, 80, 78.8, 81.1 and 75.5% on Giza 86, and 90, 85.5, 85.5 and 86.6% on Alex 4 at concentrations of 2, 1, 0.5 and 0.25%, respectively. Neem blanks had less effect on T. minutum. NeemAzal Blank reduced the parasitism rates to 74.4% on Giza 89, 75.5% on Giza 86 and 84.4% on Alex 4. Parasitism rates were reduced by NeemAzal PC05 Blank to 86.7% on Giza 89, reduced to 82.2% on Giza 86 and reduced to 87.7% on Alex 4, compared with 93.3, 92.2 and 93.3% on control plants of these cultivars Giza 89, Giza 86 and Alex 4 (Figure 3B). Effect of Neem products on efficiency of C. carnea larvae preying on Helicoverpa egg in the laboratory Data in Figure 4 revealed that the Neem products did not affect three larval instars of Chrysoperla. The Helicoverpa eggs consumed by Chrysoperla larvae differed between

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Figure 3. Effect of Neem products on parasitism rates of Trichogramma species on H. armigera eggs in the greenhouse.

Neem products and concentrations, being less in high concentrations compared with low concentrations. On other hand, longevity in high concentrations was longer than low concentrations. The results indicated no significant difference in preyed eggs and also no side effect of Neem treatments compared with control. Effect of Neem products on the longevity of Chrysoperla larvae instars The results indicated that longevity increased with increasing Neem concentrations but the predation rates decreased with increasing them. Longevity of 1st larval instar of C. carnea was 5, 5, 4.8 and 4.5 days treated by NeemAzal-T/S at 2, 1, 0.5 and 0.25% concentrations. Longevity in NeemAzal PC 05 was 4.4, 4.2, 4.1 and 4.1 days at succeeding concentrations. Longevity in NeemAzal Blank treatment was shorter; it was 4 days at all concentrations, and 4, 3.5, 3.5 and 3.2 days in NeemAzal PC05 Blank at succeeding concentrations compared with 3 days at control (Table I). Longevity of the 2nd instar of C. carnea was 4, 3.8, 3.8 and 3.9 days treated by NeemAzal-T/S at 2, 1, 0.5 and 0.25% concentrations, respectively. It was 4.4, 4.4, 4.3 and 4.1 d in NeemAzal PC 05 at succeeding concentrations, and in NeemAzal Blank treatment it was 4.2, 4, 3.6 and 3.5 days at the four concentrations. It was 3.8, 4.3, 3.7 and 4 days at subsequent concentrations in NeemAzal PC05 Blank treatment, compared with 3.4 days at control (Table I). The third larval instar is the longest; it is consider an effective predacious instar. Longevity of 3rd instar of C. carnea was 12, 12, 12.2 and 11.6 days treated by NeemAzal-T/S at 2, 1, 0.5 and 0.25% concentrations, while in NeemAzal PC 05, it was 11.6, 11.4, 11.4 and 11.2 days at succeeding concentrations, Longevity in NeemAzal Blank was shorter—10.8, 11, 10.9

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Figure 4. Effect of Neem products on the efficiency of C. carnea larvae in preying on H. armigera eggs in the laboratory.

Table I. Effect of Neem products on longevity of C. carnea larvae instars. Neem concentrations

1st larval instar (days)

2nd larval instar (days)

3rd larval instar (days)

Whole larval stage (days)

NeemAzal T/S

2% 1% 0.5% 0.25% Control

5.0 5.0 4.8 4.5 3.0

4.0 3.8 3.8 3.9 3.4

12.0 12.0 12.2 11.6 10.6

21.0 20.8 20.8 20.0 17.0

NeemAzal Blank

2% 1% 0.5% 0.25% Control

4.0 4.0 4.0 4.0 3.0

4.2 4.0 3.6 3.5 3.4

10.8 11.0 10.9 11.0 10.6

19.0 19.0 18.5 18.5 17.0

NeemAzal PC 05

2% 1% 0.5% 0.25% Control

4.4 4.2 4.1 4.1 3.0

4.4 4.4 4.3 4.1 3.4

11.6 11.4 11.4 11.2 10.6

20.4 20.0 19.8 19.4 17.0

NeemAzal PC05 Blank

2% 1% 0.5% 0.25% Control

4.0 3.5 3.5 3.2 3.0

3.8 4.3 3.7 4.0 3.4

10.8 11.0 10.9 9.8 10.6

18.0 18.0 17.8 17.0 17

Neem Products

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and 11 days at the four concentrations. Longevity in NeemAzal PC05 Blank treatment was the shortest at 10.2, 10.2, 10.6 and 9.8 days at succeeding concentrations, compared with 10.6 days in the control (Table I). Longevity of the whole larval stage of C. carnea was 21, 20.8, 20.8 and 20 days treated by NeemAzal-T/S on at 2, 1, 0.5 and 0.25% concentrations, while for NeemAzal PC 05 it was 20.4, 20, 19.8 and 19.4 days at succeeding concentrations, Longevity in NeemAzal Blank was shorter, being 19, 19, 18.5 and 18. days at the four concentrations, while it was 18, 18, 17.8 and 17 days in NeemAzal PC05 Blank at succeeding concentrations, compared with 17 days in the control (Table I). Discussion The results indicated that there is an effect of Neem products on parasitism rates of T. pretiosum and T. minutum at 2% concentration. These results correspond with those of Khorkhordin & Mironova (1996) and Maheshkumar et al. (2000), who found only slight effect of Neem formulations at high concentrations on the degree of parasitism and adult emergence of the egg parasite T. japonicum. The results also corresponded with those of Raja et al. (1998) and Thakur & Pawar (2000); their results revealed that Neem-based pesticides and biopesticides are slightly toxic to egg parasitoid. It would be effective to use Neem products in careful concentrations in IMP programmes, combined with tested natural enemies species, which have displayed level of resistance to this biopesticides. The results indicated that Neem products had no serious effects on emergence rates of T. pretiosum and T. minutum from treated Helicoverpa eggs. These finding concur with those of Markandeya & Divakar (1999) who reported that emergence of T. chilonis from the parasitized eggs was not affected. Treating host eggs with the Neem formulation any time after parasitization did not affect emergence of the parasitoid. This confirms that using Neem products can be used safely with natural enemies. Parasitism rates in the greenhouse experiment indicated that the effect of tested Neem products on T. pretiosum and T. minutum did not affect the efficiency of Trichogramma in controlling H. armigera, except at 2% concentration. Our results correspond with those of Raguraman & Singh (1999); Reddy & Manjunatha (2000) and Maheshkumar et al. (2000) confirming that there is only a slight effect of Neem products at high concentrations on the parasitism rates of Trichogramma species and that crops produced the highest yield in the treated plots. It is possible to use Neem products in an IMP programme in combination with Trichogramma to keep cotton production organic. Therefore, future experiments are suggested to further elucidate the effects of Neem on H. armigera and Trichogramma in the field. The results suggest that Neem products have no deleterious effect on predacious efficiency of C. carnea under laboratory conditions, These findings agree with the results obtained by Kienzle & Zebitz (1996) and Vogt et al. (1997) and Hermann et al. (1997), who reported no negative effect of NeemAzal T/s and NeemAzal-F on C. carnea efficacy. The only side effect of Neem products was on the longevity of larval instars of Chrysoperla. These results are similar to those of Srinivasan & Babu (2000) who found that longevity of treated C. carnea was affected by Neem products compared with control. It would be useful to use Neem products with C. carnea to control H. armigera to maintain organic cotton production to protect the environment from the side effects of pesticides. In conclusion, the Neem products tested on Trichogramma species and C. carnea showed slightly harmful activity in high concentrations. Thus, according to its short persistence,

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Neem formulations in moderate concentrations could be considered a promising active ingredient to use in IPM programmes, and are more compatible with Trichogramma species and C. carnea than synthetic insecticides. In fact, most of the chemicals tested by other researchers had a long residual toxicity in these biocontrol agents (Kakakhel & Hassan 1998; Deole et al. 2000). Therefore, considering that laboratory conditions are very strict and that in field conditions less toxic effects are foreseeable, the use of Neem formulations would seem to be advisable. However, a short delay between the treatment and the introduction of the biocontrol agents is suggested for the successful combination of the use of Neem and of Trichogramma species and C. carnea. Acknowledgements My thanks go to Dr Kleeberg for providing us the Neem products for this study, and also to all those who contributed in any way to this work, but are not mentioned here. References Deole SA, Bodhade SN, Mahajan LB, Deotale VY, Sharnagat BK. 2000. Residual toxicity of some pesticides used in cotton pest management against a chrysopid, Chrysoperla carnea. J Soils Crops 10:279 – 281. Dodan DS, Roshan L. 1999. Integrated management of neck blast and stem borer in scented rice. Haryana Agric Univ J Res 29:47 – 49. Hermann P, Zebitz CPW, Kienzle J. 1997. Effects of different NeemAzal- formulations on larvae of Chrysoperla carnea in laboratory and semi-field. In Kleeberg, Zebitz, editors. Practice oriented results on use and production of neem-ingredients and pheromones. Proceedings of the 5th Workshop, Wetzlar, Germany, 1996 22 – 25 January, 183 – 188. Isman MZ, Port GR. 1990. Systemic action of neem seed substances against Pieris brassicae. Entomol Exp Appl 54:297 – 300. Kaethner M. 1991. No side effects of neem on the aphidophagous predators Chrysoperla carnea and Coccinella septempunctata. Anz Schaed Pflanz Umwel 64:97 – 99. Kakakhel SA, Hassan SA. 1998. The side effects of pesticides on the egg parasitoid Trichogramma cacoeciae Marchal, acute dose response. Pesticides and beneficial organisms. IOBC Bull 21:61 – 69. Karuppuchamy P, Balasubramanian G, Babu PCS. 1998. Seasonal incidence and management of aphid, Aphis punicae on pomegranate. Madras Agric J 85:224 – 226. Khorkhordin EG, Mironova MK. 1996. Effects of NeemAzal on beneficial insects. In Kleeberg, Hummel, editors. Practice oriented results on use and production of Neem ingredients and pheromones IV. pp 157 – 163. Kienzle J, Zebitz CPW. 1996. Impact of NeemAzal on the arthropods fauna in an organic apple orchard. In Kleeberg, Hummel, editors. Practice oriented results on use and production of Neem ingredients and pheromones IV. pp 165 – 169. Klemm U, Schmutterer H. 1993. Effects of neem preparations on Plutella xylostella L. and its natural enemies of the genus Trichogramma. Zeit Pflanzenkrankheit schutz 100:113 – 128. Lakshmi VJ, Katti G, Krishnaiah NV, Lingaiah T. 1997. Laboratory evaluation of commercial neem formulations vis-a-vis insecticides against egg parasitoid, Trichogramma japonicum. J Biol control 11:29 – 32. Maheshkumar K, Krishnaiah NV, Lingaiah T, Paslu IC, Krishnaiah K. 2000. Effects of some commercial neem-based insecticides against Nilaparvata lugens, Sogatella furcifera and Nephotettix virescens. In Kleeberg, Zebitz, editors. Practice oriented results on use and production of neem ingredients and pheromones IX. Germany pp 23 – 33. Markandeya V, Divakar BJ. 1999. Effect of a neem formulation on four bioagents. Plant Prot Bull (Faridabad) 51:28 – 29. Natarajan K. 1990. Natural enemies of Bemisia tabaci Gennadius and effect of insecticides on their activity. J Biol control 4:86 – 88. Prabal S, Parameswaran S. 2001. Contact toxicity of chemical and bio-pesticides against Cnaphalocrocis medinalis guenee and Trichogramma chilonis Ishii. J Appl Zool Res 12:86 – 87. Raguraman S, Singh RP. 1999. Biological effects of neem (Azadirachta indica) seed oil on an egg parasitoid, Trichogramma chilonis. J Econ Entomol 92:1274 – 1280.

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