Introduction

The phytophagous, 28-spoted, epilachna beetle, Epilachna vigintioctopunctata Fab. (Coleopetra: Coccinellidae), is very important and widely distributed pest in South and East Asia, Australia, America, and the East Indies (Nakamura, 1976; Richards, 1983; Rajagopal and Trivedi, 1989). They are polyphagous and most destructive pest over several economic crops in all over India and other countries (Abbas et al., 1988; Abdullah et al., 2003; Anam et al., 2006; Rahaman et al., 2008; Abdullah, 2009). The host plants range of E. vigintioctopunctata in the Southeast Asian region include solanaceous (brinjal, Potato, tomato, black nightshade), cucurbitaceous (teasel gourd, ribbed gourd, sweet gourd) and leguminous (long-podded cowpea, snake bean) plants (Nakamura et al., 1988; Rajagopal and Trivedi, 1989; Dhamdhere et al., 1990; Shirai and Katakura, 1999; Khan et al., 2000; Sharma and Sexena, 2012; Naz et al., 2012).Among the most preferred host plants, eggplant, Solanum melongena (Solanaceae) and teasel gourd, Momordica cochinchinensis (Cucurbitaceae) are widely cultivated summer vegetable crop of Indian subcontinent (Abdullah et al., 2003; Tandon and Sirohi, 2009; Khan et al., 2011).Black nightshade, Solanum nigrum (Solanaceae), is a fairly common herb found in disturbed habitats and it can be a serious agricultural weed when it competes with crops (Abdullah, 2009). In general farmers have to cope with a range of pests like epilachna beetle (Epilachna vigintioctopunctata, E. dodegastigma, E. indica), shoot borer (Leucinodes orbonalis), whitefly (Bemisia tabaci), red pumpkin beetle (Aulacophora foveicollis) and have been found to affect the growth of this vegetable crops and the weed (Abdullah et al., 2003; Abdullah, 2009; Abe and Matsuda, 2005; Khan et al., 2011).

Usually, to control the pest outbreaks, growers are often forced to apply chemical pesticides (Rahaman and Prodhan, 2007) but the sustainability of this strategy is in question because their applications do not provide effective control. There are several reports regarding their life cycle and control by using some insecticides, biorationals, botanicals etc.(Das et al., 2002; Liu et al.,2003; Karunaratne and Arukwatta, 2009; Sharma and Sexena, 2012; Rajagopal and Trivedi, 1989; Abbas and Nakamura, 1985; Otsu et al., 2003) but their host preference in terms of their feeding dynamics, survivability and population parameters on the three host plants are unknown.The present study will give the basic knowledge about their nutritional ecology and population dynamics including different demographic parameters on different host plants for developing sustainable agricultural tactics towards integrated pest management (IPM) during the crop cultivation.

1 Result

1.1 Phytochemicals

The biochemical constituents of the three host plants, S. melongena, S. nigrum and M. cochinchinensis, are presented in Table 1. The primary metabolites i.e., total carbohydrates, proteins and lipids including amino acids content was higher in S. melongena leaves (94.947±1.444, 10.470±0.110, 9.400±0.216 and 1.857±0.049 µg/mg dry wt., respectively) and varied significantly with S. nigrum and M. cochinchinensis leaves (F_2,6= 154.885, 15.257, 47.209 and 26.753, respectively, P< 0.005) (Table 1). The moisture content were higher in S. nigrum (79.333±0.561%) relative to the other hosts and significantly differed (F_2,6=45.692, P>0.0001)(Table 1). Among the secondary metabolites, total phenolics, flavonoids, tannin, saponin and phytate concentrations were higher in M. cochinchinensis (10.177±0.180, 8.233±0.203, 7.843±0.067, 11.620±0.061 and 7.470±0.112 µg/mg dry wt., respectively) and varied significantly with S. nigrum and S. melongena (F_2,6= 115.697, 16.851, 239.295, 162.685 and 192.103, respectively, P< 0.005) (Table 1). On the other hand, alkanes and fatty acids contents were highest in S. melongena (0.680±0.023 and 0.570±0.026, µg/mg dry wt., respectively) relative to S. nigrum and M. cochinchinensis with highly significant differences (F_2,6=29.115 and 16.363, respectively, P< 0.005) (Table 1). Thus, the nutritional factors (primary metabolites including moisture content) relative to the anti-nutritional factors (Secondary metabolites) in S. melongena leaves were always higher followed by S. nigrum and M. cochinchinensis leaves.

1.2 Feeding dynamics

The life cycle and food utilization indices of this epilachna beetle, E. vigintioctopunctata were investigated in the laboratory condition by providing three host leaves separately and showed four distinct stages with four larval instars (i.e., egg, larva, pupa, and adult) (Supplementary material: Figure 1). Adult beetles are spherical and pale brown in colour with 28 black spots on their elytra. Yellowish cigar shaped eggs are laid in masses attached to ventral surface of leaves in batches of 20-35 eggs. Grubs (larvae) are yellowish with spines all over the body. The larvae pupate on the abaxial leaf surface and they are yellow with the anterior devoid of spines. As both, adult and larval stages feed on the epidermal tissues of leaves by scrapping the green matter (chlorophyll) (Supplementary material: Figure 2), the food utilization indices were relevant only for these stages which lead to the variation in overalllife history along with their population parameters.

The developmental duration of the different stages of E. vigintioctopunctata on S. melongena was shorter than S. nigrum and M. cochinchinensis but the adult longevity was always longer on S. melongena. Food utilization efficiency measures of the all four instars and their adults of E. vigintioctopunctata are given in tables 2-6. All the larval instars displayed higher value of food utilization indices (GR, CR, RGR, CI, ER, HCR, AD, ECI, ECD and HUE) when reared on S. melongena leaves followed by S. Nigrum and M. cochinchinensis leaves and showed different pattern of significance (Table 2; Table 3; Table 4; Table 5). Whereas, the adults have higher value of food utilization indices (GR, CR, ER, and ECD on M. cochinchinensis, RGR, AD, ECI and HUE on S. melongena and CI and HCR on S. nigrum) with different pattern of significance (Table 6).Among the different feeding indices, CR, CI and HCR values were higher in third instars followed by gradually decrease in fourth, second, first instars and in adults (Table 2; Table 3; Table 4; Table 5; Table 6). The AD and HUE values were decreased in same pattern (fourth instar >adult>first instar >second instar >third instar) whereas the other indices (RGR, ER, ECI and ECD) represent different patterns (Table 2; Table 3; Table 4; Table 5; Table 6).

The accumulated survivability throughout the developmental stages were significantly (P< 0.05) greatest when the insects fed with S. melongena leaves instead of S. nigrum and M. cochinchinensis leaves (Table 7).The adult emergence was significantly higher (F_2,6=22.710, P< 0.005) on S. melongena leaves (48.860 ± 2.416%) relative to S. nigrum (43.598 ± 0.860%) and M. cochinchinensis (32.984 ± 1.436%) leaves (Table 7). The fecundity was always significantly higher (F_2,6=163.500, P< 0.0001) on S. melongenaleaves (140.667 ± 1.333 eggs/female) than S. nigrum (125.333 ± 1.764 eggs/female) and M. cochinchinensis (104.00 ± 1.155 eggs/female) (Figure 3). The growth index (GI) of E. Vigintioctopunctata was also higher on S. Melongena (3.624) than on S. nigrum and M. cochinchinensis (3.136 and 2.581, respectively) (Figure 4).

1.3 Population dynamics

The population dynamics of E. vigintioctopunctata was calculated on their three host plant leaves, S. melongena, S. nigrum and M. cochinchinensis, separately and showed different pattern with highly significant differences. The three cohorts containing 146, 128 and 106 eggs for S. melongena, S. nigrum and M. cochinchinensis, respectively were reared separately to construct the demographic data of E. vigintioctopunctata and they represent similar pattern of development with significant variations (P< 0.05). The proportion of surviving (lx) and average population alive in each stage (Lx) was also gradually decreased in the development of egg to adult stage on the three host plants (Table 8; Table 9; and Table 10) which was always significantly higher on S. melongena than S. nigrum and M. cochinchinensis. Life expectancy (ex) in egg and forth instar stages were higher on S. nigrum whereas in first, second, third instar and in pupal stages were higher on S. melongena leaves (Table 8; Table 9; and Table 10). The killing power (Kx) was almost always higher on M. cochinchinensis than the other host plants (Table 8; Table 9; and Table 10). Thus, the overall most vulnerable stage of E. vigintioctopunctata was found in egg and pupal stages on all the three host plants.

The GRR, R₀, r_m and λ of E. vigintioctopunctata on S. melongena (93.531, 16.630, 0.048 and 1.049, respectively) was significantly (P<0.001) higher than S. nigrum (72.828, 11.730, 0.042 and 1.042, respectively) and M. cochinchinensis (53, 5.594, 0.029 and 1.029, respectively) (Table 11). While, the T_c and DT of E. vigintioctopunctata on M. cochinchinensis was significantly (P<0.001) higher (60.3 and 24.275 days, respectively) than on S. nigrum (59.40 and 16.720 days, respectively) and S. melongena (59.10 and 14.573 days, respectively) (Table 11). Ultimately, the overall GS was higher on S. melongena (0.582) followed by S. nigrum (0.568) and M. cochinchinensis (0.550) which was the reflected reverse value of K (0.290, 0.308 and 0.376, respectively). Thus, the population growth parameters of E. vigintioctopunctata were optimum on S. melongena relative to S. nigrum and M. cochinchinensis in relation with their respective phytochemical regime.

2 Discussions

Host plant availability and quality in terms of their phytochemicals may play a vital role in pest feeding preference as well as population dynamics by affecting immature and adult performance (Applebaum, 1985; Slansky and Scriber, 1985; Dicke, 2000; Schoonhoven et al., 2005; Genc, 2006; Shobana et al., 2010; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014). Host-plant utilization is also influenced by the ability of insect to ingest, assimilate and convert food into their body tissues (Scriber and Slansky, 1981; Dadd, 1985; Nation, 2001). Thus, host plant quality during larval growth and development is a key determinant of adult longevity, fecundity, fertility and survivability (Awmack and Leather, 2002; Syed and Abro, 2003; Shobana et al., 2010; Roy and Barik, 2013; Roy, 2014; Roy, 2015a). Ultimately, shorter developmental time along with greater total reproduction of insects on a host indicate greater suitability of a host plant (Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014; Roy, 2015a).The primary metabolites (carbohydrates, proteins, lipids, amino acids including moisture content) are used for general vitality, growth and reproduction (Mattson, 1980; Dadd, 1985; Slansky and Scriber, 1985; Turunen, 1990; Harborne, 1994; Genc and Nation, 2004; Schoonhoven et al., 2005; Shobana et al., 2010). Whereas, the secondary metabolites govern the suitability of the substrate for herbivores host preference and acceptability (Harborne, 1994; Schoonhoven et al., 2005; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014; Roy, 2015a). Consumption of greater amount of secondary chemicals was also found to significantly reduce the adult longevity, fecundity, and retardation of larval growth (Harborne, 1994; Schoonhoven et al., 2005; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014) due to higher metabolic costs (Xue et al., 2010).

In the present study, all nutritional indices varied when E. vigintioctopunctata fed on S. melongena, S. nigrum and M. cochinchinensis leaves. The current data reveal that all the four larval instars and adults of E. vigintioctopunctata had higher GR on S. melongena leaves due to good nutritional quality relative to the secondary chemicals. The other feeding indices are also affected by the host phytochemicals in relation with efficiency of nutrient digestion or absorption in their metabolic process. Thus, all the instars including adults were efficiently converting S. melongena leaves followed by S. nigrum and M. cochinchinensis leaves into their biomass by homeostatic adjustment in consumption rates and other efficiency parameters of the insect for ideal growth and development (Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014).The food utilization indices ultimately influence developmental duration, adult longevity, fecundity and survival of E. vigintioctopunctata. High survival rates and shorter developmental timeof E. vigintioctopunctata on S. melongena indicates better nutritional quality of their leaves followed by S. nigrum and M. cochinchinensis (Slansky and Scriber, 1985; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014; Roy, 2015a). Therefore, it can be concluded that S. melongena leaves provides the best quality food to E. vigintioctopunctata (higher nutritional factors relative to the anti-nutritional secondary metabolites) followed by S. nigrum and M. cochinchinensis for their better nutritional ecology and population growth.

In ecological research, life table study is a central theme and used to calculate the vital statistics of pest population dynamics including comprehensive description of their survivorship, development, fecundity, mortality and life expectancy (Southwood, 1978; Carey, 2001; Sarfraz et al., 2007; Ali and Rizvi, 2008; Roy, 2015b; Dutta and Roy, 2016). It is widely useful technique in insect pest management, where developmental stages are discrete and mortality rates vary widely from one life stage to another (Kakde et al., 2014; Roy, 2015b; Dutta and Roy, 2016). There is a range of innet capacity for individual of a population (Gill et al., 1989; Roy, 2015b; Dutta and Roy, 2016) but the variation in available food quality (Kim and Lee, 2002; Liu et al., 2004; Yasar and Güngör, 2005; Win et al., 2011; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014; Roy, 2015a) along with environmental factors (Ellers-Kirk and Fleischer, 2006; Schowater, 2006; Ali and Rizvi, 2010) always influence the growth, reproduction, longevity and survival of that population. The effect of different food sources on population parameters were observed in Epilachna dodecastigma (Khan et al., 2000), E. sparsa (Abbas and Nakamura, 1985), Plutella xylostella (Sarfraz et al., 2007) and Diacrisia casignetum (Roy and Barik, 2013) on different host plants. Variation between the results of this study could be attributed to differences among nutritional and anti-nutritional factors present in the respective host leaves that directly affect potential and achieved herbivore development and fecundity (Awmack and Leather, 2002; Syed and Abro, 2003; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014; Roy, 2015a).

The overall accumulated survival rate of E. Vigintioctopunctata on S. melongena leaves was highest as compared with that on S. nigrum and M. cochinchinensis leaves and the result suggest type III survivourship curve like most insect species (Price, 1998; Schowalter, 2006; Roy, 2015b; Dutta and Roy, 2016). The GRR, R₀, r_m, T_c, DT and λ are fundamental ecological parameters to predict the pest population growth to evaluate the performance of an insect on different host plants as well as their resistance (Southwood and Henderson, 2000; Win et al., 2011; Roy, 2015b; Dutta and Roy, 2016). In the present study, GRR, R₀, r_m, and λ of E. vigintioctopunctata was significantly higher on S. melongena followed by S. nigrum and M. cochinchinensis leaves. Whereas, the T_c and DT was also significantly lower on S. melongena than on S. nigrum and M. cochinchinensis leaves. Thus, the population parameters of E. vigintioctopunctata on the three host leaves will help to assess the relative contribution made by the respective leaf constituents to the adult population pool. This knowledge of nutritional ecology along with the life table parameters of E. vigintioctopunctata can help one to understand their population dynamics for their proper management for sustainable agriculture of those crops.

In respect to the phytochemical regime, S. melongena leaves had the lowest antibiosis resistance against E. vigintioctopunctata and were the most favorable one relative to S. nigrum and M. cochinchinensis as indicated by the short developmental time (T_c and DT), which leads to reduce exposure of the insect to its natural enemies, and high survival of immature stages. By knowing such most vulnerable stages (egg and pupal stages) from the life table parameters, one can also make time based application of different control measures for proper management of that pest population. Ultimately, the Knowledge on their population growth as well as their nutritional ecology in relation with respective host leaf chemicals support the use of S. nigrum as an alternative host towards S. melongena and as a trap crop towards M. cochinchinensis to avoid or minimum invasion of this pest for sustainable agriculture.

3 Materials and Methods

3.1 Plant materials

The egg plant, S. melongena, teasel gourd, M. cochinchinensis and black nightshade, S. nigrum leaves (tender and mature) were collected randomly from the agricultural field near Chinsurah Rice Research Center, Hooghly (22°53' N, 88°23' E), West Bengal, India. Leaves were initially rinsed with distilled water and dried by paper toweling for phytochemical analysis.

3.2 Extraction and phytochemical estimation

The freshly harvested S. melongena, M. cochinchinensis and S. nigrum leaves were dipped in different solvents for extraction of different primary and secondary chemicals. Finally, the variability of the phytochemicals present in the three host plant  leaves were estimated by various biochemical analysis, such as total carbohydrates (DuBois et al., 1956), total proteins (Miller, 1959), total lipids (Folch et al., 1957), total amino acids (Moore and Stein, 1948; Roy et al., 2013), moisture(Banerjee and Haque, 1984; Roy and Barik, 2012), total phenols (Bray and Thorpe, 1953; Roy and Barik, 2012), total flavonoids (Zhishen et al., 1999), tannin (Trease and Evans, 1983), saponin (Trease and Evans, 1983), phytate (Reddy and Love, 1999), alkanes (Roy and Barik, 2012; Roy et al., 2012a), fatty acids (Roy et al., 2012b; Roy et al.,2013; Roy and Barik, 2014). Each biochemical analysis was repeated for three times and expressed in dry weight basis.

3.3 Insect rearing

The insects used in this study were collected by sweep netting from the respective host plants. The insects were maintained separately in 1 l glass jars, containing respective host leaves, and covered with fine-mesh nylon nets at 27 ± 1°C temperatures, 65 ± 10% relative humidity, and a 12L: 12D photoperiod in a BOD incubator. The F2 E. vigintioctopunctata were used for oviposition separately indifferent sterilized glass jars. Fresh leaves were given daily by replacing the previous one until eggs were laid by the test insects, and the eggs with each host-plant leaves were placed in new sterilized glass jars separately. To maintain natural condition of leaves, a moist piece of cotton was placed around the cut ends of leaf bearing twigs followed by wrapping with aluminum foil to prevent moisture loss. To study their life table parameters, the eggs were separated and checked daily until all eggs either hatched or collapsed, and the numbers of daily emerged larvae along with their survival and developmental time were recorded by daily monitoring. The larvae and adults were reared in sterilized glass jars containing 20 individuals on each kind of host leaves for study their feeding dynamics with five replicates for each host plants. Thus, the feeding dynamics along with different life table parameters of E. vigintioctopunctata were determined by a single generation with three cohorts for each kind of host leaves.

3.4 Food utilization

The weight gain of insects, the weight of food consumed and the weight of faeces produced were determined in a monopan microbalance (±0.001 mg). Third generation larvae of approximately same size were selected and weighed initially and were reared separately into separate sterilized glass jars. They were allowed to feeding on weighed quantity of three host leaves for 24 h and were reweighed. The fresh weight gain during the period of study was estimated by determining the differences in weight of larvae or adults. The quantity of the food consumed was estimated by determining the difference between the dry weight of diet remaining at the end of each experiment and total dry weight of diet initially provided.  All the values were expressed on dry weight basis through dry conversion values as described by Roy and Barik (2012 and 2013) and Roy (2014). Twenty individuals were used in each type of host leaves for each instars and adults with five replicates.

3.5 Food utilization indices

Food utilization indices (on dry weight basis) were calculated by the formulas of Waldbauer (1968) with slight modifications (Thangavelu and Phulon, 1983; Sétamou et al., 1999; Xue et al., 2010; Roy and Barik, 2012; Roy and Barik, 2013; Roy, 2014) to assess the feeding efficiencies of E. vigintioctopunctata as follows:

Growth rate (GR) = P/Q

Consumption rate (CR) = R/Q

Relative growth rate (RGR) = P/QS

Consumption index (CI) = R/QS

Egestion rate (ER) = T/QS

Host consumption rate (HCR) = CI+ER

Approximate digestibility (AD) (%) = 100 (R-T)/R

Efficiency of conversion of ingested food (ECI) (%) = 100P/R

Efficiency of conversion of digested food (ECD) (%) = 100P/(R-T)

Host utilization efficiency (HUE) (%) = 100 R/(R+T)

Hatchability (%) = 100A/B

Effective rate of rearing (ERR) (%) = 100C/D

Adult emergence (AE) (%) = 100E/C

Accumulated survivability (AS) (%) = N_b% XN_a% / 100

Growth index (GI) = AE%/H

Where, P: dry weight gain of insect; Q: duration of experimental period; R: dry weight of food eaten; S: mean dry weight of insect during time Q; T: dry weight of faeces produced; A: number of eggs hatched; B: number of eggs laid by per female; N_a: number of larvae in beginning of instar; N_b: number of larvae in succeeding instar; C: number of cocoons harvested; D: number of last instar larvae reached pupation; E: number of beetles emerged; H: Duration of immature period.

3.6 Life table parameters

The construction of life table includes several parameters which were calculated with the formulae of Carey (1993), Krebs (1994) and Price (1998). These parameters include probability of survival from birth to age x (lx),proportion dying each age (dx), mortality (qx), survival rate (sx) per day per age class from egg to adult stages. Using these parameters, the following statistics like, average population alive in each stage (Lx), life expectancy (ex), exponential mortality or killing power (kx), total generation mortality (K), generation survival (GS), gross reproductive rate (GRR), net reproductive rate (R₀), mean generation time (T_c), doubling time (DT), intrinsic rate of population increase (r_m) and finite rate of population increase (λ) were also computed, using Carey’s formulae(Carey, 1993).

3.7 Statistical analysis

All the data on food utilization indices and life table parameters of E. vigintioctopunctata of the three host leaves along with their phytochemical regime were analyzed using one way ANOVA (Zar, 1999). All the statistical analysis was performed using the statistical program SPSS v. 13.0 (SPSS, 2004).

Author’s contributions

NR designed the whole study including sample collection, chemical analysis, index calculation, data analysis and drafts the manuscript with the help of institutional support.

Acknowledgments

The financial assistance provided by the University Grants Commission [F. No. PSW-025/13-14], New Delhi, Government of India is gratefully acknowledged.

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