Impact of temperature and soybean genotypes on biology of tobacco caterpillar and its mortality assessment with chitin synthesis inhibitors under in vitro condition

Introduction

Soybean (Glycine max L. Merril), belongs to the family Leguminaceae and subfamily Papilionoideae, is an important two dimensional crop grown in tropical, subtropical and temperate climates. The cultivated soybean originated from China and was introduced in India during the tenth century AD through Himalayan routes (Agarwal et al., 2013) [1] . It is an ideal crop for small and marginal farmers with high nutritional value and significantly contributed to "Yellow Revolution" in India. It contains 42% protein, 20% oil, lycin and vitamins A, B and D (Ramesh Babu et al., 2018) [2] . For vegetarians, it is known as "Poor Man's Meat". It has innumerable possibilities of not only improving agriculture but also supporting industries and good source of medicinal value, thus it is considered as "Miracle Bean" or "Golden Bean" or "Wonder Crop" of the 20 th century (Fattah et al., 2020). India ranks 4 th in area and 5 th in production of soybean in the world after United States of America, Brazil, Argentina and China (Longchar et al. 2018) [4] . In Indian scenario, Madhya Pradesh alone contributes more than 50% in total area and production of soybean; hence this state is usually referred as "Soya State" (Ahirwar et al. 2013) [5] . The low productivity of soybean both at national and state level is attributed to abiotic and biotic stresses like drought, weeds, insect pests and diseases. Among these, insect pests often pose a serious threat to soybean production, quantitatively and qualitatively. Soybean is reported to be attacked by more than 380 species of insects in many parts of the world. About 150 insects pests cause damage to soybean in various parts of Madhya Pradesh, out of them a dozen of them cause serious damage to the crop from sowing to harvest (Ahirwar et al. 2013) [5] . Among them, tobacco caterpillar, Spodoptera litura Fab. (Lepidoptera: Noctuidae) is a most destructive and serious defoliator throughout the ecological situation. In recent years, S. litura regularly occurred as a devastating pest of field crops due to its nocturnal habit, migration ability of adult insect over longer distances, wide host range and also characteristics to survive in the soil during cold spells without undergoing diapauses (Karmakar and Pal, 2017) [6] . In Madhya Pradesh, S. litura is a regular and serious pest, it damages soybean from mid-August to October in Kharif and from November to March in Rabi season. It feeds on foliage, flowers and pods causing significant yield losses (Azmi et al. (2017) [7] . Sudden rise in temperature and sunshine hours would decide the outbreak of S. litura in soybean. During, 2008 outbreak of S. litura in soybean caused widespread losses in Vidarbha and Marathwada region of Maharashtra (Kawre et al., 2019) [8] . Sundar et al., (2018) [9] has further emphasized that climate change affects the activity of S. litura and caused 40% defoliation. It alters the interaction between host -insect relationship, under such conditions some of the cultivars resistant to specific pest, may become susceptible (Sangle et al., 2015) [10] . Billy reported that in central India a 3 ºC rise in surface air temperature, abandons out the positive effects of doubling of CO 2 concentration, which results in reduction in the soybean productivity to the extent of 50%. The fourth assessment report of Inter Governmental Panel on Climate Change indicated that the annual average temperature of the earth is likely to increase by 1 ºC by 2025 and by 3 ºC towards the end of the century. Effect of temperature change on herbivorous insects directly affects the insect physiology and behavior or indirectly by influencing the host plant abundance and quality (Karuppaiah and Sujayanad, 2012) [11] . According to Srinivasa Rao et al., (2014) [12] temperature is the single most significant climatic factor influencing the metabolism, development, reproduction and survival of the insects. Fand et al., (2015) [13] reported S. litura incidence will increase in soybean areas like Madhya Pradesh, Maharashtra and Rajasthan due to increased temperature under future climatic condition. Therefore, to manage S. litura efficiently, there is a need to study the effect of change in temperature on the biology of the pest on its host plants. The last four decades have witnessed a massive transition in the development of insecticide resistance in S. litura. The first case of insecticide resistance in S. litura was documented against BHC in areas around Jaipur and Ajmer (Bhatia, 1986) [14] . Hence, S. litura has the distinction of being first ever lepidopteran pest in India and second agricultural pest to develop insecticide resistance. Field collected populations of S. litura showed resistant to cypermethrin, deltamethrin, chlorpyrifos and profenofos (Ahmed et al., 2005) [15] . Problems like resurgence, residue, secondary pest outbreak and environmental safety emerged due to neuroactive insecticides in pest management. Therefore, in the present context ecofriendly management strategies are required for this notorious pest. The insect growth regulators (IGR's) are a group of modern pesticides which may play desirable role in integrated pest management. IGR's are a group of chemical substance that inhibits the lifecycle of an insect by dispensing the moulting processes (Deep et al., 2018) [17] . IGR's include compounds such as chitin synthesis inhibitors (CSI's), juvenile hormone mimics and ecdysone agonists. The CSI's further consist of various compounds acting on the immature stages of insects by inhibiting the chitin formation, thereby causing abnormal endocuticular deposition and abortive moulting (Ahmad and Gull, 2017) [18] . Lufenuron specifically acts on the incorporation of N-acetyl glucosamine in the integument, resulting in the formation of abnormal new cuticle and death of the insect (Islam et al, 2015) [15] . Novaluron is a relatively new benzoylphenyl urea group with low mammalian toxicity and it acts by ingestion and contact against lepidopteran insects (Hamadah et al, 2015) [20] .

Materials and Methods

Initiation and multiplication of S. litura culture Initially the S. litura egg masses were collected from the unsprayed soybean field of Breeder Seed Production farm, JNKVV and kept in petridishes with tender leaves for enabling the young larvae to feed immediately after hatching and to prevent Mortality of larvae. The rearing space was increased regularly using more number of plastic trays (8 x 4 inch) from third instar onwards to avoid cannibalism and crowding of larvae. For pupation, sixth instar larvae were transferred to the beakers half filled with moist sterile sand. Male and female pupae were separated as proposed by Li et al (2014) [21] . A pair of emerged adults were released in each plastic container along with cotton swab dipped in 10% honey solution (Plate 5). As proposed by Farahani et al (2011) [22] the F 1 offsprings obtained were maintained on the tested genotypes for two successive generations before they were used in the experiment. Thus the nucleus culture from third generation F 3, adults were used for further investigation. The glasswares used in the experiment was thoroughly washed in detergents, treated with 2% formalin and then dried in an oven at 30 o C for 8 hours to check microbial contamination in the insect culture as per the methodology suggested by Sharma and Singh (2018) [23] .

Procurement of soybean seeds

Seeds of soybean genotypes (JS-335, JS 97-52, JS22-09 and JS20-116) were obtained from Soybean Breeder; All India Coordinated Research Project on Soybean, Department of Plant Breeding & Genetics, College of Agriculture, JNKVV, Jabalpur, MP. The seeds were stored in air tight containers for further use as and when required for study (Plate 3).

Raising of test genotypes

Four different genotypes of soybean which were included in the study as main treatment (JS-335, JS 97-52, JS 22-09 and JS 20-116) were grown in suitable soil and compost mixture in 20 cm diameter plastic pots in green house following the recommended package of practices but without any insecticidal spray (Plate 4). Trifoliate leaves from 20-25 days old crop were used for the study as proposed by Farahani et al (2011) [22] .

Design of temperature regimes

On the basis of last forty years temperature data of kharif season in Jabalpur (M.P) the mean range was computed which was further into three temperature regimes (viz., 20±2, 25±2 and 30±2 °C) were considered as sub treatments.

Materials used

The following materials were used to conduct the studies on the biological parameters: 32 mega pixel camera, aluminum foil, BOD, camel hair brush (zero size), cotton swab, digital electronic balance, forceps, glass beakers, laminated graph paper, marker, measuring scale, muslin cloth, ocular micro meter, paraffin paper, plastic containers for oviposition, plastic petri dishes (15" diameter), plastic pots, plastic trays, refrigerator, rubber bands, soybean cultivars / genotypes, stereomicroscope, students microscope and thermo hygrometer,

Method of observation

Soybean genotypes comprising of four treatments were replicated three times and kept at 20±2 °C, 25±2 o C and 30±2 °C temperature regimes at constant RH 65±5% with 14:10 light / dark cycle as per methodology suggested by Thakur et al (2017) [24] .

Eggs: 100 eggs were examined on the four genotypes kept at three different temperature regimes. The data on hatching percentage and incubation periods were recorded.

Incubation period: It was calculated from the time of egg laying to the time of hatching.

Hatching percentage: It was calculated from the data on number of eggs hatched out of total number of eggs under observation.

Larval stage

Thirty newly hatched neonates were released @ ten larvae per treatment per replication which were provided with fresh leaves of tested genotypes as food material. The number and duration of different larval instar was determined by the moulting process with casting off head capsule and exuviae. Number of instars and instar wise survival, larval duration were also recorded on all the selected genotypes at subsequent temperature.

Pupa

Observations on pupal percentage, pupal duration were recorded within 24 hours of pupation as suggested by Swetha et al. (2017) [35] .

Adult stage Adult emergence:

The number of adults emerged out from the total pupae were recorded. Female and male moth as showed in plate-14 Total life cycle: The time period from egg laying to adult emergence was taken as the total life cycle. The individual duration of egg, larvae, pupae and adults were summed to obtain the total developmental duration and were figured out with all the tested genotypes at different temperature.

Chitin synthesis inhibitors

Studies on efficacy of three chitin synthesis inhibitors were carried out on second instar tobacco caterpillar the details of which are mentioned below:

Preparation of Stock solution

The test doses of diflubenzuron, novaluron and lufenuron were measured with micropipette and transferred into 100ml volumetric flask separately and distilled water was added to make the volume up to 100 ml. The flask having one percent of the active ingredients of chitin synthesis inhibitors were taken as stock solution. These stock solutions were kept in refrigerator at 4 °C and removed an hour before use as to bring the solution to room temperature.

Bioassay study against S. litura on 2 nd instar larvae Leaf dip bioassay method was carried out against 2 nd instar larvae of S. litura as per the methodology suggested by Khatun et al (2017) [26] . Trifoliate castor leaves were dipped in aqueous solution of different concentration of tested chitin synthesis inhibitors for 10 seconds with gentle agitation and dried on tissue paper. The starved defecated third instar larvae were released on the treated soybean leaves which were placed in petriplates having a moist filter paper to avoid desiccation. In case of control, larvae were treated with distilled water. Ten third instar larvae were used in each treatment, replicated thrice and incubated at 27±1 ºC, 65±5% relative humidity and photophase of 14:10 hours.

Observation recorded

Assessment of larval mortality was observed at 72 hrs after treatment and was continued upto their mortality as proposed by Kranthi (2005) [27] and Guptha and Guptha (2014) [28] . a. Malformed and shrinked larvae were considered as dead b. Larvae which did not moult or pupate were considered as dead. c. Pupae from which no adults emerged and those appeared as withered away, were also taken as dead. [33] on soybean.

Results and Discussion

However, fecundity in the present findings on JS-335 genotype (2440 eggs/female at 25 °C) is slightly higher than the findings of Fand et al (2015) [13] on JS-335 soybean genotype, as they reported maximum and minimum fecundity (1234.9 and 492.3 eggs / female, respectively) was recorded at 25 and 20 ºC, respectively. Under similar conditions of suitable food and temperature, such variations are related to genetic variation from different geographic locations or biotypes related to the insect (Murua et al, 2008) [29] .

Incubation period

Among the genotypes, longest incubation period was observed on JS97-52 (6.22 days) which was at par with JS20-116 (6.11 days) and were significantly shortest on JS-335 (3.89 days). Among the temperature regimes, the mean incubation period significantly decreased with increase in temperature. The present findings corroborates the findings of Devi and Jha (2017) [30] , Thakur et al (2017) [24] as they also reported that the incubation period was inversely correlated with temperature on different host crops viz., sunflower, jute and tomato, respectively.

Hatchability

The highest hatching was noticed on JS-335 (88.04%) which was significantly superior then the rest of the genotypes. The lowest hatchability was observed on JS97-52 (63.65%) which was statistically at par with JS20-116 (67.90%). However, among the tested temperature the highest hatching was observed at 25±2 °C (80.71%) followed by at 30±2 °C (75.76%) and lowest at 20±2 °C (63.97%), respectively. The present findings confirms the findings of Shukla and Patel (2011) [31] , Thakur et al (2017) [24] and Ramaiah and Maheshwari (2018) [32] , as they also reported that the most favourable temperature was 27±1 °C and 25±2 °C, as hatching of eggs was maximum i.e. 97.84, 89.60±3.29 and 87.25 ± 7.42% on jute , banana and castor crops, respectively. The slight deviations in the hatchability that exist might be attributed to host plants used as larval food.

Total larval duration

Among genotypes it was observed to be shortest on JS-335 (15.89 days). While it was recorded longest on JS97-52 (24.89 days). Among temperature regimes, it significantly decreased with increase in temperature, being 27.58, 20.08 and 14.92 days which were observed at 20±2 °C, 25±2 °C and 30±2 °C, respectively. The present findings are in conformity with the findings of Fand et al (2015) [13] ,

Gayathri et al (2016) [3] and Thakur et al (2017) [24] as they also reported that the total larval duration was negatively correlated with temperature being 25.42±1.51

Total larval survival

The mean total larval survival showed significant difference among genotypes and it was minimum on JS97-52 (55.56%), while it was maximum on JS-335 (87.78%). The total larval survival significantly increased with increase in temperature, being 61.67, 63.33 and 79.17% at 20±2 °C, 25±2 °C and 30±2 °C, respectively. while it was maximum on JS-335 (96.67%) at 30±2 °C. The present findings are in accordance with the findings of Fand et al (2015) [13] as they also claimed that the S. litura larval survival was lowest and highest at 20 °C and 30 °C temperatures, respectively when reared on different crops.

Pupation

Highest pupation was noticed on JS-335 (88.92%) which was significantly superior than the rest of the genotypes and lowest on JS97-52 (70.59%). Among the tested temperature, significantly highest pupation was observed at 25±2 °C (85.87%) and lowest at higher temperature 30±2 °C (71.00%). The present findings corroborates the findings of Fand et al (2015) [13] , Thakur et al (2017) [24] as they also reported that the highest pupation was observed at 25±2 °C on soybean, jute and castor, respectively.

Pupal duration

Pupal duration was significantly shortest on JS-335 (7.33 days), while longest duration was recorded on JS97-52 (13.00 days). Among temperature regimes, it significantly decreased with increase in temperature, being 13.33, 11.25 and 7.17 days at 20±2 °C, 25±2 °C and 30±2 °C, respectively. The present findings are in accordance with the findings of Fand et al (2015) [13] and Gayathri et al (2016) [33] , as they also reported similar trend, being 16±0.13, 12±0.12 and 7.6±0.16 days at 20±2 °C, 25±2 °C and 30±2 °C, respectively on soybean crop

Adult emergence

Among genotypes the highest adult emergence was noticed on JS-335 (90.88%) which was significantly superior then the rest of the genotypes and lowest on JS97-52 (59.26%). Among the tested temperature, significantly highest adult emergence was observed at 25±2 °C (80.28%) followed by 30±2 °C (73.53%) and lowest at 20±2 °C (65.60%), but they differed significantly from each other. The present findings slightly deviated with the findings of Thakur et al (2017) [24] , as they also reported the adult emergence was positively correlated with temperature from 18±1 °C to 27±1 °C, being 76.20 to 90.05%, later it decreased to 72.30% at 33±1 °C on jute crop. [33,30,24] . Factors other than temperature viz. genetic differences, sex, food, humidity, photoperiod, geographic origin and number of instars can change the developmental duration. Female moth lived longer than the male moth also confirm the findings of Farahani et al. (2011) [22] and Fand et al (2015) [13] .

Total life span

Chitin synthesis inhibitors

In the present investigation at 24 and 48 hours after treatment, none of the treatments exhibited mortality of S. litura 2 nd instar larvae. The larval mortality was first observed at 72 hrs after treatment. Similar findings have been reported by Islam et al (2015) [19] .

days after treatment

At 3 days after treatment, significantly maximum larval mortality was recorded in Lufenuron 100 ppm (56.67%), which was superior over all the remaining treatments. The next best treatment was novaluron 200 ppm (46.67%), followed by diflubenzuron 300 ppm (40.00%) and lufenuron 50 ppm (33.33%). The latter two treatments were at par with each other. Minimum larval mortality was observed in diflubenzuron 75 ppm (13.33%)

days after treatment

At 5 days after treatment, significantly maximum larval mortality was recorded in Lufenuron 100 ppm (85.00%), which was superior over all the remaining treatments. The next best treatment was novaluron 200 ppm (75.55%), followed by diflubenzuron 300 ppm (66.67%) and lufenuron 50 ppm (65.07%). Lowest larval mortality was observed in diflubenzuron 75 ppm (6.29%).

days after treatment

At 7 days after treatment, significantly highest larval mortality of 100.00% was recorded in Lufenuron 100 ppm and novaluron 200 ppm and were superior over all the remaining treatments. The next best treatment was diflubenzuron 300 ppm (88.89%), which was at par with lufenuron 50 ppm (83.33%).

In the present study Lufenuron at higher concentration (100 ppm) was found to be highly effective as it recorded maximum larval mortality at 3 days after treatment (DAT) followed by Novaluron and Diflubenzuron @ 200 and 300 ppm, respectively. The present findings confirm the findings of Radhika et al (2002) as they also reported that the order of toxicity of Chitin synthesis inhibitor was Lufenuron> Novaluron >Diflubenzuron at 72 hrs after application and the order of efficacy was same at 5 days and 7 DAT. The present findings are in accordance with the findings of Islam et al (2015) [19] , as they also reported maximum larval mortality (100%) which was attained by the application of higher concentration of Lufenuron @ 75 ppm after 3 days of treatment. The present findings contradicts the findings of as they reported Novaluron was highly effective than lufenuron and diflubenzuron. Such differences in the order of toxicity might be due to variation in the doses, larval stages and application methods that they have incorporated in the investigation (Islam et al, 2015) [19] .

Conclusion

The study highlights the significant influence of genotype and temperature on the reproductive and developmental parameters of female moths. JS-335 genotype consistently outperformed others in terms of fecundity, hatching, pupation, and adult emergence, especially at the ambient temperature of 25±2 °C, which was most favorable for these parameters. Conversely, JS97-52 exhibited the lowest values across most metrics. Temperature played a crucial role, with higher fecundity, shorter developmental durations, and increased survival rates observed at higher temperatures.

The study also validated the efficacy of Lufenuron as a potent chitin synthesis inhibitor, showing maximum larval mortality, especially at higher concentrations.

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