Acta agriculturae Slovenica, 119/3, 1–6, Ljubljana 2023 doi:10.14720/aas.2023.119.3.14714 Original research article / izvirni znanstveni članek Results of testing of the efficacy of sublethal concentrations of bacterial- chemical insecticides combinations against cabbage moth larvae Hrant TERLEMEZYAN 1 , Masis SARGSYAN 1 , Harutyun HARUTYUNYAN 1 , Noushig ZARIKIAN 2, 3 , Sona SARGSYAN 1 , Gabriel KARAPETYAN 1 , Habetnak MKRTCHYAN 1 Received June 26, 2023; accepted September 14, 2023. Delo je prispelo 26. junija 2023, sprejeto 14. septembra 2023 1 Research Centre of Risk Assessment and Analysis in Food Safety Area, Y erevan, Armenia 2 Department of Experimental Zoology, Scientific Center of Zoology and Hydroecology of NAS RA, Y erevan, Armenia 3 Corresponding author, e-mail nzarikian@gmail.com The experiments of sublethal concentrations of bacterial- chemical insecticides against cabbage moth larvae Abstract: Using chemical pesticides has adverse effects on the environment and humans. Bacterial preparations may pro- vide an alternative to chemical pesticides. The study aims to test different combinations of sublethal concentrations of bacterial and chemical preparations against cabbage moth larvae. During 2020-2022 different combinations of sublethal concentrations of bacterial (Lepidocide) and chemical (Arrivo, Voliam Flexi, Proclaim Fit) preparations were tested in labora- tory and field conditions, against cabbage moth young larvae (stage I-II). The combinations of insecticides with bacterial and chemical sublethal concentrations show high biological effi- ciency against the cabbage moth larvae. No statistical difference was found between the efficiency indicators of the combined and standard chemical (Arrivo, Voliam Flexi, Proclaim Fit) op- tions and the significance level was generally between 2.0 and 5.9 %, showing that the results of the scientific experiments are reliable. Key words: biological effectiveness, cabbage moth larvae, insecticides, laboratory and field tests, statistical analysis Poskusi s subletalnimi koncentracijami bakterijsko-kemij- skih insekticidov na gosenice kapusnega molja Izvleček: Uporaba kemijskih insekticidov ima škodljive učinke na okolje in ljudi. Pripravki iz bakterij so lahko alterna- tiva kemijskim pesticidom. Namen raziskave je bil preiskusiti različne kombinacije subletalnih koncentracij bakterijskih in kemijskih pripravkov proti gosenicam kapusnega molja. V letih 2020-2022 so bile v laboratoriju in poljskih razme- rah preiskušene različne kombinacije subletalnih koncentracij bakterijskih (Lepidocide) in kemijskih (Arrivo, Voliam Flexi, Proclaim Fit) pripravkov za zatiranje mladih gosenic kapusne- ga molja (razvojni štadij I-II). Kombinacije bakterijskih in kemijskih insekticidov v su- bletalnih koncentracijah so pokazale veliko biološko učinko- vitost na tretiranih gosenicah. V kazalnikih učinkovitosti ni bilo statistično značilne razlike med kombiniranimi pripravki in standardnimi kemijskimi insekticidi (Arrivo, Voliam Flexi, Proclaim Fit). Raven značilnosti je bila nasplošno med 2,0 in 5,9 %, kar kaže, da so izsledki poskusov zanesljivi. Ključne besede: biološka učinkovitost, gosenica kapu- snega molja, insekticidi, laboratorijski in poljski poskusi, sta- tistična analiza Acta agriculturae Slovenica, 119/3 – 2023 2 H. TERLEMEZYAN et al. 1 INTRODUCTION The soil and climatic conditions of Armavir region of the Republic of Armenia are favorable for the culti- vation of white-head cabbage (Brassica oleracea L. ssp. oleracea convar. capitata (L.) Alef f. alba). The increase of the yield of this plant is often hindered by the cabbage moth Plutella maculipennis (Curtis, 1832) which belongs to the Plutellidae family of the insect order Lepidoptera. The damage caused by its larvae reduces the yield and lowers the quality of the crop. Hatched larvae eat the parenchyma of the leaves, leaving the epidermis intact, resulting in the formation of areas covered with a thin membrane, called “windows” (Avetyan & Marjanyan, 1976), and the more mature lar- vae open through holes on the leaves. The damage be- comes more dangerous when they feed on the young leaves forming the head of the plant (Safaryan, 1968; Terlemezyan, 1996; Philips et al., 2014; Andreeva et al., 2021). Besides the white-head cabbage, phytophagous lar- vae also damage other economic importance crucifer- ous plants, for example cauliflower, broccoli, rapeseed, etc. (Tsedeler, 1931; Harcourt, 1957; Terlemezyan, 1996; Churikova & Silaev, 2010; Shpanev, 2015; Kholod & Korenyuk, 2016; Tuleeva & Sarmanova, 2019). Therefore, it is extremely important to implement effective, environ- mentally safe control measures against harmful larvae. In the integrated pest control system, the preference is given to the use of bacterial preparations based on Bacillus thuringiensis Berliner, 1915 (Bt) species, which have high biological efficiency against leaf-eating harm- ful insects and, unlike chemical preparations, are safe for humans, warm-blooded animals, entomophages and fish. (Talekar & Shelton, 1993; Belyaev & Nozdrenko, 2004; Ivantsova, 2004; Sarantseva & Bobreshova, 2006; Sargsyan, 2013; Fathipour & Mirhosseini, 2017; Semer- enko, 2019; Zakharova et al, 2022). Currently, the implementation of economically justified control of phytophagous larvae through com- binations of sublethal concentrations (used in small quantities) of bacterial and chemical insecticides is also emphasized (Mesropyan, 2011; Avagyan, 2012; Chapan- yan, 2022). Based on the above, we aimed to test different com- binations of sublethal concentrations of bacterial and chemical preparations against cabbage moth larvae in laboratory and field conditions. 2 MATERIALS AND METHODS The scientific experiments were carried out during 2020-2022, in the laboratory conditions at the Scientific Center for Risk Assessment and Analysis of Food Safety and cabbage plantations of Nalbandian community of Armavir region. The research materials were: the young cab- bage moth larvae (stage I-II), the cabbage plant (variety: Slava), the commercial bacterial lepidocide preparations KA 3000 IU mg -1 in the powder for liquid suspension: the usage rate is 1.0 kg ha -1 (Russian Federation), chemi- cal preparations: 25 % concentrated emulsion Arrivo: the usage rate is 0.3 l ha -1 (FMC, USA), 30 % concentrated suspension Voliam Flexi: the usage rate is 0.3 l ha -1 , and 45 % water-soluble granules of Proclaim fit: the usage rate is 0.1 l ha -1 (Syngenta, Switzerland). All the above-mentioned preparations are al- lowed to be used against harmful insects in the Republic of Armenia. Cabbage plantations, where the number of moth larvae was at the threshold of economic damage of a specified pest (that is: 2-5 larvae per plant), when 10 % or more of the plants in the experimental site are occupied by them (Polyakov, 1984), were selected as ex- perimental sites. The biological effectiveness of insecticides com- bined with sublethal concentrations (Lepidocide + Ar- rivo, Lepidocide + Voliam Flexi, Lepidocide + Proclaim Fit) was determined according to the methodological manual (Methodological guidelines for testing biologi- cal products for plant protection from pests’ diseases and weeds, 1973). The lethal concentrations of 3 (in case of lepiocide: 0.33 kg ha -1 ) and 10 dilutions (in case of Arrivo and Voliam Flexi: 0.03 l ha -1 , in case of Proclaim Fit: 0.01 l ha -1 ) of bacterial (lepidocide) and chemical (Arrivo, Voliam Flexi and Proclaim Fit) insecticides, respectively, were combined. The samples sprayed with different solvents (Lepidocide: the usage rate is 1.0 kg ha -1 , Arrivo: the us- age rate is 0.3 l ha -1 , Voliam Flexi: the usage rate is 0.3 l ha -1 , Proclaim Fit: the usage rate is 0.1 l ha -1 ) were taken from the plantations naturally inhabited by moth larvae. During small-scale and production experi- ments, cabbage plants grown under laboratory condi- tions (in camps) and artificially inhabited by moths were sprayed with a hand-held sprayer full of working fluid, using backpack AO - 2 and motorized K-14 sprayers. The working fluid consumption was 400 l ha -1 . In small-scale experiments, the size of the experimental area for each (sampled separately and experimentally combined) op- tion was 100 m², as for large-scale spraying, it was 0.2 ha. Each option included in the experiments had 3 replicates. In laboratory conditions, 30 larvae were in- cluded in each option (10 larvae in each replicate), and Acta agriculturae Slovenica, 119/3 – 2023 3 Results of testing of the efficacy of sublethal concentrations of bacterial-chemical insecticides combinations against cabbage moth larvae in two-year small-scale and production experiments, the number of phytophagous larvae was generally between 51 and 70, and 55 and 77, in certain cases. The numbers of alive and dead larvae in the experimental plots were counted before spraying (base- line), and 3, 5 and 7 days after spraying, also before the mating phase. In laboratory conditions when experimenting the options with the sub-threshold concentrations, the mi- crobiological isolation of Bacillus thuringinsis var. kursta- ki Bulla et al. 1979 pathogens which are the basis for the production of the sprayed commercial lepidocide bacte- rial preparations, were isolated according to the meth- odological manual (Netrusov et al., 2005). The statistical analysis of the results of the scientific experiments was carried out according to the protocol presented by (Ashmarin and Vorobyev, 1962; Bernstein, 1968). 3 RESULTS AND DISCUSSION According to the results of scientific experiments carried out in laboratory conditions in 2020, it was proved that the combinations of standard lepidocide bacterial (3 dilutions of the lethal concentration) and di- luted lethal chemical (Arrivo, Voliam Flexi and Proclaim Fit) concentrations (10 dilutions of the lethal concentra- tion) have shown a high biological efficiency against phy- tophagous larvae (stage I-II) just in 7 days after spraying, generally ranging from 93.3 % to 96.7 %. The indicators of biological efficiency of the sample options for the same recording period were also high, ranging from 93.3 to 100 %. No mortality of phytophagous larvae was observed on the sprayed sample, during the observation period. The high rates of biological efficiency recorded in laboratory conditions made it possible, as well, to test the insecticides individually (standard/sample options) and in combination with sublethal concentrations (experi- mental options) against the cabbage moth larvae under field conditions (field and production experiments). According to the results of the partial (small-scale) research, it was demonstrated that even 7 days after spraying, the indicators of biological efficiency of com- bined options, such as Lepidocide + Arrivo, Lepidocide + Voliam Flexi, Lepidocide + Proclaim Fit, were still high, generally ranging from 91.5 % to 94.3 % (Table 1). As it is presented in Table 1, Lepidocide (sample), Arrivo (sample), Voliam Flexi (sample) and Proclaim Fit (sample) options have also demonstrated high biological efficacy (overall 85.7 % - 96.1 %). The pattern of high biological efficiency in small- scale experiments demonstrated by individual and sub- lethal concentrations of insecticides against the cabbage moth larvae was maintained during production experi- ments conducted in 2021-2022 (Table 2). According to the two-year data from Table 2, the in- dicators of biological efficiency (7 days after spraying) of the standard lepidocide were 82.4 % and 85.4 %. As for the combined options of sublethal concentrations, such as Lepidocide + Arrivo, Lepidocide + Voliam Flexi, and Lepidocide + Proclaim Fit, those were 89.1 % and 90.1 %, 92.2% and 93.0 %, and 91.3 % and 91.5 %, respectively. The indicators of biological efficiency recorded for all standard (sample) chemical insecticides were between 86.3 % and 95.2 % for the same period of observation. Moreover, the above-mentioned indicators recorded on the 7 th day were constant for all tested options before the mating period. From the data in Tables 1 and 2, it is clear that the indicators of biological efficiency recorded in the experi- ments conducted 3 and 5 days after spraying were rela- tively low compared to those recorded on the 7th day, Table 1: The indicators of biological effectiveness of standard (sample) and combined insecticides against cabbage moth larvae (stage I-II) (small-scale experiments, Nalbandyan, 2020) Options The number of larvae on the plant 20 option, quantity Biological efficiency according to accounting days, % 3 5 7 Lepidocide + Arrivo 59 57.6 78.0 91.5 Lepidocide +Voliam Flexi 53 62.3 84.9 94.3 Lepidocide + Proclaim Fit 67 56.7 80.6 92.5 Lepidocide (Sample) 70 51.4 77.1 85.7 Arrivo (Sample) 58 67.2 84.5 89.7 Voliam Flexi (Sample) 51 78.4 88.2 96.1 Proclaim Fit (Sample) 62 62.9 87.1 93.5 Acta agriculturae Slovenica, 119/3 – 2023 4 H. TERLEMEZYAN et al. which is apparently due to the specificity of the mecha- nism of action of insecticides on larvae. Compared to the water-spraying practices, when the experimental options, i.e., the combined bacterial and chemical sublethal concentrations, were applied, the cabbage larvae gradually refused to feed on plants. Moreover, no response to contact or any other mechani- cal stimuli was observed, which, eventually, contributed and led to larval death. The bodies of dead larvae, com- pared to healthy larvae, have become grey and have re- duced in size. Microbiological studies have confirmed that the gut cavity and decayed tissues of dead moth larvae were full of vegetative cells of the Bacillus thuringiensis pathogen, as well as insecticidal spore-crystal components. Using the Student’s t-test criteria, it was proved (Ta- ble 3) that the two-year indicators of biological efficiency of the experimental options, when the lepidocide was combined with sublethal concentrations of insecticides, significantly exceeded those of the standard lepidocide samples, because in the first case with p = 0.95 and n = 3, the student’s t-test scores, generally ranging from 3.601 to 7.095, were higher than the tabulated Student’s t-test score of 3.182. It was also statistically confirmed that there was no significant difference between the indica- tors of biological effectiveness recorded in the combined versions, on the one hand, and in the standard individual options of Arrivo, Voliam Flexi and Proclaim Fit, on the other hand (with p = 0.95 and n = 3, the calculated two- year average scores of the student’s t-tests were between 0.056 and 1.756, which were less than its table (3.182) index). In the two-year production studies, the statistical error was generally ranging from 2.0 % to 5.9 %, con- firming that the results of the scientific experiments are reliable (Table 4). 4 CONCLUSIONS Based on the results of the experiments, we came to a conclusion that the combinations of insecticides with bacterial and chemical sublethal concentrations show high biological efficiency against the cabbage moth lar- vae. The efficiency indicators for the latter are statistically different from those of the standard bacterial lepidocide. However, no statistical difference was found between the efficiency indicators of the combined and standard chemical (Arrivo, Voliam Flexi, Proclaim Fit) options. The statistical error indicators prove that the results of the scientific experiments are accurate. Table 2: The indicators of biological effectiveness of standard (sample) and combined insecticides against cabbage moth larvae (stage I-II) by years (production experiments, Nalbandian, 2020) Options The number of larvae on the plant 20 option, quantity Biological efficiency according to accounting days, % 3 5 7 During 2021 Lepidocide + Arrivo 55 56.4 76.4 89.1 Lepidocide + Voliam Flexi 64 60.9 84.4 92.2 Lepidocide + Proclaim Fit 59 50.8 78.0 91.5 Lepidocide (Sample) 55 49.1 76.4 85.4 Arrivo (Sample) 73 64.4 83.6 86.3 Voliam Flexi (Sample) 61 77.0 85.2 95.1 Proclaim Fit (Sample) 62 61.3 85.5 93.5 During 2022 Lepidocide + Arrivo 71 54.9 77.5 90.1 Lepidocide + Voliam Flexi 57 61.4 82.4 93.0 Lepidocide + Proclaim Fit 69 53.6 79.7 91.3 Lepidocide (Sample) 74 50.0 75.7 82.4 Arrivo (Sample) 77 66.2 81.8 88.3 Voliam Flexi (Sample) 63 76.2 87.3 95.2 Proclaim Fit (Sample) 70 60.0 84.3 91.4 Acta agriculturae Slovenica, 119/3 – 2023 5 Results of testing of the efficacy of sublethal concentrations of bacterial-chemical insecticides combinations against cabbage moth larvae Table 3: The comparative assessment of indicators of biological efficiency recorded in experimental and standard (sample) options during production experiments verified by Student‘s t test criteria (by years) Options  Indicators of biological efficiency 7 days after spraying, % Student’s t test scores Indicators of biological efficiency 7 days after spraying, % Student’s t test scores During 2021 During 2022 Lepidocide + Arrivo 89.1 3.601*1.756 90.1 4.424*1.208 Lepidocide + Voliam Flexi 92.2 4.687**1.756 93.0 7.095**1.535 Lepidocide + Proclaim Fit 91.5 4.643***1.628 91.3 4.537***0.056 Lepidocide (Sample) 85.4 - 82.4 - Arrivo (Sample) 86.3 - 88.3 - Voliam Flexi (Sample) 95.1 - 95.2 - Proclaim Fit (Sample) 93.5 - 91.4 - Note. * in the numerator: the combined experimental and lepidocide (sample) options, in the denominator: the comparative indicators of biologi- cal efficiency recorded in the experimental and Arrivo (sample) options, ** in the numerator: experimental and lepidocide (sample) options, in the denominator: the comparative indicators of the biological efficiency recorded in the experimental and Voliam Flexi (sample) options and *** in the numerator: the comparative indicators of biological efficiency recorded in the experimental and lepidocide (sample) options, in the denominator: the experimental and Proclaim Fit (sample) options Table 4: The statistical indicators of the average number of dead cabbage moth larvae (stages I-II) per replicate, 7 days after spray- ing, by years (production experiments) Options The average number of dead larvae per replicate, quantity Statistical indicators The squared deviation The coefficient of variation, % The average error The statistical error, % During 2021 Lepidocide + Arrivo 16.33 0.575 3.52 0.332 2.0 Lepidocide + Voliam Flexi 19.67 1.661 8.44 0.959 4.9 Lepidocide + Proclaim Fit 18.00 1.414 7.85 0.816 4.5 Lepidocide (Sample) 15.67 1.205 7.69 0.696 4.4 Arrivo (Sample) 21.00 1.633 7.78 0.943 4.5 Voliam Flexi (Sample) 19.33 1.737 8.99 1.003 5.2 Proclaim Fit (Sample) 19.33 1.009 5.22 0.583 3.0 During 2022 Lepidocide + Arrivo 21.33 1.741 8.16 1.005 4.7 Lepidocide + Voliam Flexi 17.67 1.199 6.79 0.692 3.9 Lepidocide + Proclaim Fit 21.00 2.160 10.29 1.247 5.9 Lepidocide (Sample) 20.33 1.739 8.55 1.004 4.9 Arrivo (Sample) 22.67 1.185 5.23 0.684 3.0 Voliam Flexi (Sample) 20.00 1.633 8.17 0.943 4.7 Proclaim Fit (Sample) 21.33 1.303 6.11 0.752 3.5 Acta agriculturae Slovenica, 119/3 – 2023 6 H. 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