Indian Journal of Experimental Biology Vol. 57, June 2019, pp. 443-449

Safety assessment of selected biopesticides and botanicals on spp. (: ) in fields

Sudhendu Sharma* & Naveen Aggarwal

Department of Entomology, Punjab Agricultural University, Ludhiana-141 004, Punjab, India

Received 12 February 2017; revised 04 September 2018

A biological alternative to pesticides in agriculture is an important subject as it promotes environmental health. Unlike synthetic persticides, they do not harm other beneficial and natural enemies of pests. Here, we studied the influence of five biopesticides/botanicals [Dipel WP (Bacillus thuringiensis var. kurstaki), Myco-Jaal 10% SC (Beauvaria bassiana), entomopathogenic nematode (EPN), Steinernema feltiae), Neem azal 1% (10000 ppm azadirachtin) and Karanj oil 2% (20000 ppm karanjin)] on adult emergence and the parasitisation efficiency of Trichogramma spp. in basmati rice. Our results revealed that all the biopesticides/botanicals tested at varied doses against adult emergence of the Trichogramma spp were harmless to slightly harmful, though negative relationship between dose and the emergence was observed. Neem azal 1% @ 5.0 mL/L and karanj oil 2% @ 20.0 mL/L affected the adult emergence of Trichogramma chilonis and T. japonicum negatively. The parasitization efficiency of the surviving individuals was not affected in all the treatments. However, exposure of 2-fold doses of biopesticides i.e., neem azal 1% @ 10.0 mL/L and karanj oil 2% @ 40.0 mL/L, significantly disrupted the adult emergence of T. chilonis and T. japonicum though, the surviving individuals showed the same oviposition ability resulting in successful parasitism. The order of toxicity of different biopesticides/botanicals against Trichogrammatids was Neem azal 1% > Karanj oil 2% > Dipel WP > EPN > Myco-Jaal 10% SC.

Keywords: Basmati rice, Biological pest control, Biopesticides, Botanicals, Endoparasitoids, EPN, IPM, Karanj oil, Neem azal, Pest control, Trichogramma, Wasps

Among the rice cultivars, aromatic rice, basmati holds a In many agroecosystems, sustainable pest unique niche due to its distinct aroma and flavour. India management is exercised through biological control. produces more than 70% of the total world aromatic Hymenopteran wasps in the genus Trichogramma rice. The country exported 4.06 mT of basmati rice, (Trichogrammatidae) has widely been used for worth 4.17 billion US dollars, during the year 2017-18 management of Lepidopteran pests under numerous (APEDA, 2018)1. Synthetic pesticides affect non-target biological systems4. Egg parasitism by Trichogramma insect species and also drastically disrupt natural pest chilonis Ishii and Trichogramma japonicum Ashmead control2. Excess application of these pesticides results in has been significantly effective in the biological pesticide residues. On the other hand, increasing global suppression of yellow stemborer, Scirpophaga demand of food safety has stimulated research on risks incertulas and leaffolder, Cnaphalocrocis medinalis associated with consumption of food toxins. Therefore, in rice5-8. Biopesticides based on Bacillus food rejection or acceptance across international borders thuringiensis Berliner have been used against is being regulated by national and international food stemborer and leaffolder in rice, which have reduced regulations. Basmati rice exports to the US had been the population of these pests9,10. Similarly, botanical plunged in recent past as many Indian firms faced pesticides, present an important alternative to rejection for higher pesticide residues, threatening multi- minimize the use of or replace the synthetic 3 billion rice export industry . This has led to increased pesticides. However, influence of these biopesticides awareness of ecologically safe produce, and encouraged on the natural enemy population, particularly Tricho- organic farming. grammatids, is little known. Thus, in the present —————— study, we investigated the disruptive effect of these *Correspondence: Phone: +91 9780010958 (Mob.) biopesticides/botanicals on these natural enemies so E-mail: [email protected] as to avoid the harmful ones. 444 INDIAN J EXP BIOL, JUNE 2019

Materials and Methods Treatment protocol

Insect rearing Effect on adult emergence The cultures of test insects, T. chilonis and The experiment was conducted in semi-field T. japonicum were mass maintained on laboratory conditions wherein basmati rice plants of variety Pusa host, Corcyra cephalonica Stainton (Lepidoptera: Basmati 1121 were raised in pots at Entomological Pyralidae) in the Biocontrol Laboratory at Department Research Farm, Punjab Agricultural University, of Entomology, Punjab Agricultural University, Ludhiana. Tricho-cards with counted number (approx. Ludhiana, India. The eggs of C. cephalonica were 100) of T. chilonis and T. japonicum parasitized Corcyra used as host for mass production of these eggs were stapled to these potted plants. During 2012 Trichogrammatids. Bold white sorghum grains meant crop season, each of the biopesticide/botanical was for human consumption were procured. The required applied in three different dosages. In all, there were 16 quantity of sorghum was milled to 3-4 pieces of each treatments and the experiment was replicated thrice. The grain and heat sterilized in oven at 100ºC for 30 min. biopesticides, namely Dipel WP (Bacillus thuringiensis To prevent bacterial infestation, streptomycin var. kurstaki) and @ Myco-Jaal 10% SC (Beauvaria sulphate was added to the crushed sorghum at the rate bassiana) each @ 4.0, 6.0 and 8.0 g/L, of 0.2 g/Kg and mixed thoroughly. Corcyra rearing entomopathogenic nematode Steinernema feltiae @ 4.0, boxes each containing 2.5 kg of milled sorghum were 6.0 and 8.0 million IJs (infective juveniles) per litre; and charged with Corcyra eggs @ 0.5 cc/box. These botanicals, namely neem azal 1% (10000 ppm boxes were kept on iron racks (90 cm length × 45 cm azadirachtin) @ 3.0, 4.0 and 5.0 mL/L, karanj oil 2% breadth × 180 cm height) in rearing laboratory at (20000 ppm karanjin) @ 10.0, 15.0 and 20 mL/L water 27±2°C and 70±5% humidity. On 40th day, moths were sprayed up to runoff on the stapled trichocards. For started emerging and these were collected daily and the untreated control treatment, normal water was transferred to the specially designed oviposition sprayed. The cards were removed after spray and cages. The fresh eggs of C. cephalonica were brought to the biocontrol laboratory to observe the collected and treated with UV rays for 45 min to emergence of parasitoids. These surviving parasitoids prevent hatching. These eggs were glued to cards of were further observed for their parasitization efficiency. 15×10 cm and were exposed to adult female During 2013 crop season, again the basmati rice Trichogramma in the ratio of 8:1 for 24 h at 27±1°C plants of variety Pusa Basmati 1121 were raised in pots and 65 ± 5% humidity. at the same location and Tricho-cards with counted number of parasitized Corcyra eggs were stapled to Biopesticides/botanicals In all, five biopesticide formulations (three these potted plants. The procedure for the spray and microbials and two plant based) at different doses observance of emergence of parasitoids was similar to were tested for their efficacy. These biopesticides the previous year. However, during 2013, the were selected because of their potential use in pest biopesticides/botanicals were applied at the highest test management in paddy under organic farming dose and double dose of first year’s treatment doses i.e. conditions. The formulations, their active ingredients Dipel WP @ and Myco-Jaal 10% SC each @ 8.0 and and producers are listed in Table 1. 16.0 g/L, entomopathogenic nematode S. feltiae @ 8.0 and 16.0 million IJs/L; and Neem azal 1% @ 5.0 and Table 1—Formulations tested against 10.0 mL/L, and Karanj oil 2% @ 20.0 and 40.0 mL/L Trichogramma chilonis and T. japonicum water. In all, there were 11 treatments including Formulation Active ingredient Producer untreated control and the experiment was replicated Dipel WP Bacillus thuringiensis var. Valent BioSciences thrice. The response of the test insects to toxicant Kurstaki (32 g a.i./Kg) Corporation, USA exposure was classified using the IOBC toxicity ratings Myco-Jaal Beauvaria bassiana Pest Control (India) wherein for extended laboratory, semi-field studies, the 10% SC (1×1010 conidia/mL) Pvt. Ltd, India scale runs from 1= harmless (<25% mortality), Entomo- Steinernema National Bureau of pathogenic feltiae Agricultural Insect 2= slightly harmful (25-50%), 3= moderately harmful 11 nematode Resources, India (51-75%) to 4= harmful (>75%) . Neem azal Azadirachtin E.I.D.-Parry (India) 1% (10000 ppm) Ltd., India Effect on parasitization efficiency Karanj oil Karanjin Parker India Group, The experiment to assess the parasitization 2% (20000 ppm) India efficiency of the surviving individuals following SHARMA & AGGARWAL ASSESSMENT OF BIOPESTICIDES/BOTANICALS TO TRICHOGRAMMA 445

application of different biopesticides/botanicals was varied in their toxicities to the egg parasitoids, conducted in the Biocontrol Laboratory at 27±1ºC and T. chilonis and T. japonicum. Among the different 65±5% humidity in Department of Entomology, treatments, the adult emergence of T. chilonis varied Punjab Agricultural University, Ludhiana during 2012 from 79.38 to 88.64% and that mortality ranged from and 2013. The experiment was replicated thrice on the 11.36 to 20.62% (Table 2). Out of 16 treatments, surviving individuals to work out their parasitization botanicals affected the adult emergence causing efficiency. mortality to a higher extent than that of biopesticides. Neem azal 1% @ 5.0 mL/L water affected the adult Statistical analysis emergence of T. chilonis most (79.38% emergence) The effects of five selected biopesticides/botanicals resulting in 20.62% mortality (F=5.34; df15,32; on the per cent adult emergence, adult mortality and P <0.0001). Maximum adult emergence (88.64%) was per cent parasitism of the egg parasitoids T. chilonis recorded in untreated control resulting in minimum and T. japonicum were subjected to a one-way mortality (11.36%). karanj oil 2% @ 20.0 mL/L analysis of variance (ANOVA) test. The percentage (80.23%) and neem azal 1% @ 4.0 mL/L (80.31%) proportions were subjected to arcsine angular also affected the adult emergence wherein mortality transformation before analysis to separate treatment percentage was 19.77 and 19.69, respectively in the means. The results were expressed as mean ± standard two treatments. Among the biopesticide treatments, error followed by Duncan’s test. Dipel WP affected the adult emergence most when applied @ 8.0 g/L (81.49%) and 6.0 g/L (82.13%). Results Whereas, Myco-Jaal 10% SC @ 4.0 mL/L was least

Effect on adult emergence and mortality disruptive to adult emergence (87.73%) resulting in The results of the study conducted during 2012 mortality to the extent of 12.27%. This was followed demonstrated that different biopesticides/botanicals by karanj oil 2% @ 10.0 mL/L (87.21% emergence;

Table 2—Effect of biopesticides/botanicals on adult emergence (in %) of Trichogramma chilonis and T. japonicum Treatment Dose/L 2012 2013 water T. chilonis T. japonicum T. chilonis T. japonicum Adult Mortality Adult Mortality Adult Mortality Adult Mortality emergence emergence emergence emergence Dipel WP 4.0 g 85.31±1.84abc 14.69±1.84abc 76.77±1.09abc 23.23±1.09abc - - - - 6.0 g 82.13±1.54ab 17.87±1.54ab 74.39±1.22ab 25.61±1.22ab - - - - 8.0 g 81.49±1.39ab 18.51±1.39ab 72.87±1.42ab 27.13±1.42ab 85.04±1.38bc 14.96±1.38bc 78.42±1.34b 21.58±1.34b 16.0 g - - - - 81.82±1.93b 18.18±1.93b 76.63±1.07b 23.37±1.07b Myco-Jaal 4.0 mL 87.73±1.73bc 12.27±1.73bc 76.42±1.13abc 23.58±1.13abc - - - - 10% SC 6.0 mL 86.12±1.08bc 13.88±1.08bc 77.77±0.89bc 22.23±0.89bc - - - - 8.0 mL 83.40±1.08ab 16.60±1.08ab 76.54±0.72abc 23.46±0.72abc 84.72±1.18bc 15.28±1.18bc 79.18±0.71b 20.82±0.71b 16.0 mL - - - - 80.87±1.53b 19.13±1.53b 78.08±1.44b 21.92±1.44b EPN 4.0 million 86.96 13.04 79.17 20.83 - - - - IJs ±1.00bc ±1.00bc ±0.37bc ±0.37bc 6.0 million 85.19 14.81 76.68 23.32 - - - - IJs ±1.09abc ±1.09abc ±1.01abc ±1.01abc 8.0 million 82.43 17.57 73.26 26.74 86.77 13.23 78.43 21.57 IJs ±0.81ab ±0.81ab ±1.84ab ±1.84ab ±1.34c ±1.34c ±1.79b ±1.79b 16.0 - - - - 83.48 16.52 75.88 24.12 million IJs ±1.20bc ±1.20bc ±2.01b ±2.01b Neem azal 3.0 mL 82.15±0.72ab 17.85±0.72ab 74.49±0.89ab 25.51±0.89ab - - - - 1% 4.0 mL 80.31±1.55a 19.69±1.55a 73.69±1.17ab 26.31±1.17ab - - - - 5.0 mL 79.38±0.75bc 20.62±0.75bc 70.58±0.84a 29.42±0.84a 80.58±2.18b 19.42±2.18b 74.66±1.03b 25.34±1.03b 10.0 mL - - - - 72.44±2.65a 27.56±2.65a 63.45±1.30a 36.55±1.30a Karanj oil 10.0 mL 87.21±0.56bc 12.79±0.56bc 77.22±0.70bc 22.78±0.70bc - - - - 2% 15.0 mL 84.65±1.27abc 15.35±1.27abc 74.49±0.96ab 25.51±0.96ab - - - - 20.0 mL 80.23±1.86ab 19.77±1.86ab 72.86±0.55ab 28.14±0.55ab 81.62±1.41b 18.38±1.41b 77.60±1.32b 22.40±1.32b 40.0 mL - - - - 77.36±1.26b 20.64±1.26b 69.28±1.22b 27.72±1.22b Control - 88.64±0.89bc 11.36±0.89bc 79.64±1.54bc 20.36±1.54bc 90.62±0.84c 9.38±0.84c 83.01±0.63c 16.99±0.63c F value 5.34 5.62 8.70 13.38 df 15,32 15,32 10,22 10,22 p value <0.0001 <0.0001 <0.0001 <0.0001 [Values are Mean ± SE. Means followed by the same letters within the column did not differ significantly (P <0.05; LSD test)] 446 INDIAN J EXP BIOL, JUNE 2019

12.79% mortality) and EPN @ 4.0 IJs/L (86.96% Our observations during the 2012 and 2013 on emergence; 13.04 mortality). In case of T. japonicum, mortality of parasitoids showed that the tested the adult emergence varied from 70.58 to 74.27% and biopesticides/botanicals had different adverse effect mortality varied from 20.36 to 29.42%. For the on adult emergence of the T. chilonis and biopesticide/botanicals, neem azal 1% @ 5.0 mL/L T. japonicum. The data on mortality responses of all affected the adult emergence most (70.58%) and biopesticide/botanical tested, could be classified as higher mortality (29.42%). It was followed by karanj per IOBC toxicity scales as harmless (Class 1) for the oil 2% @ 20.0 mL/L (72.86% emergence; 27.14% emergence of egg parasitoid, T. chilonis regardless to mortality) and Dipel WP @ 8.0 g/L (72.87% varied doses. But this statement did not hold true for emergence; 27.13% mortality). In addition to T. japonicum. Out of the tested biopesticides/botanicals, untreated control (79.64% emergence; 20.36% treatments like Dipel WP @ 6.0 and 8.0 g/L, EPN mortality), the application of EPN S. feltiae @ 4.0 S. feltiae @ 8.0 million IJs/L, all the three doses of million IJs/L water was least disruptive (79.17% neem azal 1% @ (3.0, 4.0 & 5.0 mL/L) and karanj oil emergence; 20.83% mortality). Myco-Jaal 10% SC 2% @ 15.0 and 20.0 mL/L were classified as slightly @ 4.0 mL/L (77.77% emergence; 22.23% mortality) harmful (class 2) as the mortality ranged from 25.51 and karanj oil 2% @ 10.0 mL/L (77.22% emergence; to 29.42% in these treatments. 22.78% mortality) were also less disruptive (F=5.62; df ; P <0.0001). During 2013, out of all biopesticide/botanical 15,32 treatments, neem azal 1% @ 10.0 mL/L could be During 2013, wherein biopesticides/botanicals classified as slightly harmful for T. chilonis were applied at highest test dose and double dose of emergence. Rest of the biopesticides/botanicals previous year’s treatment doses, neem azal 1% regardless to varied doses were classified as harmless @ 10.0 mL/L (72.44% emergence; 27.56% mortality) (Class 1). Mortality responses of T. japonicum to and karanj oil 2% @ 40.0 mL/L (77.36% emergence; neem azal 1% @ 5.0 and10.0 mL/L karanj oil 2% @ 22.64% mortality) disrupted the adult emergence of 40.0 mL/L render these treatments be classified as T. chilonis most in comparison to control (90.62% slightly harmful for the emergence of the parasitoid. emergence; 9.38% mortality) (F=8.70; df10,22; P <0.0001). The remaining treatments were classified as harmless. Myco-Jaal 10% SC @ 16.0 mL/L (80.87% emergence; 19.13% mortality) and karanj oil 2% @ 20.0 mL/L Effect on parasitization efficiency (81.62% emergence; 18.38% mortality) were also The parasitization efficiency of the surviving disruptive to the parasitoid (Table 2). Among the T. chilonis and T. japonicum adults that emerged from biopesticide/botanical treatments, EPN S. feltiae eggs treated with respective biopesticides/botanicals @ 8.0 million IJs/L water was least disruptive for 2012 and 2013 are presented in Table 3. The (86.77% emergence; 13.23% mortality). It was results did not differ significantly during 2012. The followed by Dipel WP @ 8.0 g/L (85.04% parasitization varied from 87.31 to 88.93% in case of emergence; 14.96% mortality) and Myco-Jaal 10% T. chilonis (F=0.75; df15,32; p=0.7181) and from 70.27 SC @ 8.0 mL/L (84.72% emergence; 15.28% to 74.27% for T. japonicum (F=1.15; df15,32; mortality). Similar pattern was observed in case of p=0.3562). The percentage of parasitization was not T. japonicum where treatments like Neem azal 1% significantly different across the different treatments @ 10.0 mL/L (63.45% emergence; 36.55% mortality) and it hold true for both the parasitoids. Similar and karanj oil 2% @ 40.0 mL/L (69.28% emergence; results was arrived at during 2013, wherein the 31.72% mortality) resulted in lowest emergence of surviving individuals emerged from the all the T. japonicum adults in comparison to emergence in biopesticides/botanicals treated eggs showed the same control treatment (83.01% emergence; 16.99% oviposition ability as that from untreated eggs mortality). Myco-Jaal 10% SC @ 8.0 mL/L was least resulting in successful parasitism. The parasitism of disruptive to the egg parasitoid (79.18% emergence; the laboratory reared Corcyra eggs by the surviving 20.82% mortality). It was followed by treatments like T. chilonis varied from 84.56 to 88.65% (F=2.04; Dipel WP @ 8.0 g/L (78.42% emergence; 21.58% df10,22; p=0.0786) and that by surviving T. japonicum -1 mortality) and EPN S. feltiae @ 8.0 million IJs L varied from 76.11 to 79.14% (F=0.74; df10,22; (78.43% emergence; 21.57% mortality) (F=13.38; p=0.6808) in different treatments which was par with df10,22; P <0.0001). each other. SHARMA & AGGARWAL ASSESSMENT OF BIOPESTICIDES/BOTANICALS TO TRICHOGRAMMA 447

Table 3 —Effect of biopesticides/botanicals on parasitization efficiency of Trichogramma chilonis and T. japonicum Treatment Dose/L water Parasitization of host eggs (%) 2012 2013 T. chilonis T. japonicum T. chilonis T. japonicum Dipel WP 4.0 g 87.80±0.23a 71.78±1.44a - - 6.0 g 88.07±0.61a 73.15±0.87a - - 8.0 g 88.81±0.60a 73.68±1.00a 88.01±0.65a 78.31±0.61a 16.0 g - - 86.93±0.84a 78.27±0.38a Myco-Jaal 10% SC 4.0 mL 87.96±0.22a 73.28±0.84a - - 6.0 mL 88.12±0.73a 72.55±0.34a - - 8.0 mL 87.31±0.28a 73.51±0.71a 87.46±0.59a 79.14±1.35a 16.0 mL - - 85.88±0.78a 78.36±1.26a EPN 4.0 million IJs 88.89±0.93a 71.65±0.95a - - 6.0 million IJs 88.70±1.19a 73.09±1.05a - - 8.0 million IJs 87.77±0.25a 71.84±0.84a 85.52±1.02a 77.41±1.09a 16..0 million IJs - - 86.33±0.89a 79.06±0.75a Neem azal 1% 3.0 mL 88.19±0.23a 73.20±0.88a - - 4.0 mL 87.98±0.56a 72.09±0.82a - - 5.0 mL 88.78±0.24a 73.75±0.33a 86.04±1.03a 78.02±0.62a 10.0 mL - - 85.32±0.89a 76.11±0.84a Karanj Oil 2% 10.0 mL 88.76±0.50a 72.33±0.79a - - 15.0 mL 88.40±0.45a 70.62±1.19a - - 20.0 mL 88.24±0.39a 71.87±1.26a 84.56±1.16a 77.70±1.17a 40.0 mL - - 85.73±1.01a 78.22±1.11a Control - 88.93±0.51a 74.27±0.53a 88.65±0.57a 78.50±0.83a F value 0.75 1.15 2.04 0.74 df 15,32 15,32 10,22 10,22 p value 0.7181 0.3562 0.0786 0.6808 [Values are Mean ± SE. Means followed by the same letters within the column did not differ significantly (P <0.05; LSD test)]

Discussion Trichogramma in the rice ecosystem. Studies Despite their ill effects, pesticides still remain as conducted to verify the disruptive influence of an integral part of pest management programmes. different biopesticides on adult emergence of Further, application of pesticides and releases of Trichogramma spp. in basmati rice revealed that all Trichogrammatids has historically been considered the biopesticides tested at varied doses were harmless incompatible12-15. Biopesticides of the microbial though negative relationship between dose and the origin, such as entomopathogenic bacteria, fungi and emergence was observed. However, higher doses of nematodes, with specificity to a target pest or a class treatments like neem azal 1% and karanj oil 2% of pests, offer an eco-friendly and effective alternative affected the adult emergence of T. chilonis and to pest problems. These can be used in integration T. japonicum negatively. Exposure of twofold doses of with bioagents aiming at complementary control of biopesticides revealed that treatments of neem azal 1% target pests16-19. Likewise, plant products having an @ 10.0 mL/L and karanj oil 2% @ 40.0 mL/L array of biologically active substances affecting the significantly disrupted the adult emergence of growth and development of the herbivores, play a T. chilonis and T. japonicum placing them into the significant role in the ecology and physiology of category of slightly harmful pesticides. Among the phytophagous insects. While these potential biopesticide treatments, Myco-Jaal 10% SC and EPN parasitoids are to be necessarily safeguarded from the S. feltiae were least disruptive to the adult toxic effect of pesticides, the safety of these biological emergence of the parasitoid. alternatives against the endoparasitoids also needs to The present study also demonstrated that be ensured. In the present study, we evaluated the parasitization efficiency of the surviving biopesticides/botanicals for influence, if any, on the individuals emerged from the all the endo-parasitoids Trichogramma chilonis and biopesticides/botanicals treated eggs was not T. japonicum in basmati rice field. affected and adults showed the same oviposition Our study outlines the compatibility of certain ability as that from untreated eggs. Laboratory biopesticides/botanicals with the released investigations carried out to assess the toxicity of 448 INDIAN J EXP BIOL, JUNE 2019

certain neem products and insecticides against 70-100% and also affected the emergence of adult parasitoids, T. chilonis and T. japonicum revealed that parasitoids. However, Bt formulations, namely Biolep the adult emergence and per cent parasitisation were and Bioasp were relatively safe for the parasitoids. greatly influenced by insecticides as compared to Sagheer et al.28 studied the synergistic effect of neem products which were relatively safer to these T. chilonis and biopesticides for the management of egg parasitoids20. Lyons et al.21 examined the effects C. medinalis. They reported that integration of of neem formulations on the reproduction and biopesticides (microbial+botanical) and egg parasitoid, survival of the egg parasitoid Trichogramma minutum T. chilonis for the sustainable management of leaf- Riley. Seed extracts having azadirachtin and a folder has enhanced the effectiveness of parasitoid. purified form of azadirachtin were tested at an operational dose and at 10 times the operational dose. Conclusion At azadirachtin @ 50 g/ha (operational dose), no The results of the present study suggests that significant effects were observed on survival biopesticides/botanicals viz., Dipel WP (Bacillus of parasitoid females. However, azadirachtin thuringiensis var. kurstaki) and Myco-Jaal 10% SC @ 500 g/ha, female survival after 1 day was (Beauvaria bassiana) @ 4.0 and 6.0 g/L; significantly reduced by Azatin EC and Neem EC. entomopathogenic nematode, Steinernema feltiae The studies also find support from Rao et al.22 who @ 4.0 and 6.0 million IJs (infective juveniles) per tested the toxicity of newer insecticides to egg litre; Neem azal 1% (10000 ppm azadirachtin) @ 3.0 parasitoid, T. chilonis and reported that neem and 4.0 mL/L, Karanj oil 2% (20000 ppm karanjin) formulations Neemgold at 0.015% recorded the @ 10.0 and 15.0 mL/L water are safe and such maximum parasitism (50.3%) of T. chilonis, followed by applications do not harm the endoparasitoids 0.3% Nivar with (40.3% parasitism). Trichogramma chilonis and T. japonicum. However, the same biopesticides at the dose 8.0 g/L, 8.0 million In the current study it was found that microbial IJs/L, 5.0 and 20 mL/L or above, respectively, based biopesticides including Bt were harmless to influenced the adult emergence of the endoparasitoids slightly harmful to the Trichogramma spp. This negatively. Hence, these biopesticides can be integrated corroborates with biosafety studies of N. rileyi against with utilization of Trichogramma spp. against the T. chilonis which suggested that at quite high 7 lepidopteran pests of rice, though the indiscriminate concentration of 2.4×10 of the biopesticide, the use of these ‘harmless’ biopesticides have to be parasitization (89.70%) was at par with untreated 23 24 avoided to eliminate the slightest chances of control (91.20%) . Pazini et al. while studying the disruptive influence on the released egg parasitoids. selectivity of pesticides on T. pretiosum revealed that the biopesticides Beauveria bassiana and M. anisopliae Conflict of Interest did not reduce the egg parasitiztion with a parasitism The authors declare that there is no conflict of reduction of no more than 10.0% and were classified interest regarding the publication of this paper. as harmless. Similar results were recorded by Amaro et al.25 who assessed the toxicity of entomopathogens References on adults of T. pretiosum and found B. bassiana and 1 APEDA, Agricultural and Processed Food Products Export M. anisopliae as harmless against the parasitoid. Development Authority. Available at: http://agriexchange. Momanyi et al.26 evaluated the toxicity of eight pest apeda.gov.in/product_profile/prodintro/Basmati_Rice.aspx (2018). control products commonly used in vegetable crops in 2 Crowder DW, Northfield TD, Strand MR & Snyder WE, Kenya, by exposing the adults of Trichogramma sp. Organic agriculture promotes evenness and natural pest nr. mwanzai and Trichogrammatoidea sp. nr. lutea to control. Nature, 466 (2010) 109. detached potted tomato leaves at different intervals 3 Sally M, United States finds Pesticide Residue in Basmati, Exports Plunge. Economic Times Bureau, July 1, 2013. after spraying. They reported that biologically derived 4 Bueno R, Bueno AD, Parra JRP, Vieira SS & de Oliveira LJ, products Dipel (Bt kurstaki) was harmless and had no Biological characteristics and parasitism capacity of persistent toxicity on both the trichogrammatid Trichogramma pretiosum Riley (Hymenoptera, Tricho- species. Similarly, Borah et al.27 studied the effect of grammatidae) on eggs of Spodoptera frugiperda (J.E. Smith) different insecticides on the parasitisation and (Lepidoptera, Noctuidae). Revta Bras Ent, 54 (2010) 322. 5 Aggarwal N, Sharma S & Jalali SK, On-farm impact of emergence of T. japonicum adults and reported that biocontrol technology against rice stem borer, Scircophaga chemical pesticides inhibited parasitism ranging from incertulas (Walker) and rice leaf folder Cnaphalocrocis SHARMA & AGGARWAL ASSESSMENT OF BIOPESTICIDES/BOTANICALS TO TRICHOGRAMMA 449

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