Evaluation of Telenomus remus (Hymenoptera: Platygastridae) as a biocontrol agent of Spodoptera litura (Lepidoptera: Noctuidae) based on two-sex life table and functional response analyses
CABI Agriculture and Bioscience volume 4, Article number: 48 (2023)
Telenomus remus Nixon is an important egg parasitoid of Spodoptera spp. pests and, as such, has potential as a biological control agent. Spodoptera litura (Fabricius) is a significant pest of many economically important crops worldwide. This study was conducted to evaluate the demographic parameters and functional response of T. remus on the S. litura eggs.
T. remus can lay 186.90 eggs/female in the lifetime, adult preoviposition period was 0 days, total preoviposition period was 10.03 days, and the ratio of female and male offspring was 0.495 and 0.421, respectively. In addition, most females emerged from 24 h-old eggs, whereas most males emerged from 48 h-old eggs. The intrinsic rate of increase, finite rate of increase, net reproductive rate, mean generation time, and population doubling time were 0.3506 d–1 1.4199 d–1 92.45 offspring/individua, 12.91 days and 1.98 days, respectively. The net killing rate of T. remus on S. litura was 101.49 eggs/female, indicating the high capacity of T. remus to parasitize S. litura eggs. Moreover, the higher the egg density, the higher the parasitism rate by female T. remus, although there was a trend of parasitism stabilization at an egg density of 100, indicating a type II functional response curve for this parasitoid.
Overall, these findings suggest that T. remus can be efficiently reared on S. litura eggs and shows potential as biocontrol agent for this economically important pest species.
Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) is an insect pest worldwide (Yang et al. 2023; EPPO 2023), with more than 120 host plant species in 48 families, and causes severe economic losses in crop fields (Ravishankar and Venkatesha 2011; Toke, et al. 2016; Shekhawat et al. 2018). Each female can lay more than 2,000 eggs during her lifespan, laying 200–300 eggs in a single egg mass (Ahmad et al. 2013) that are usually covered by a layer of brown abdominal hair-like scales (Li et al. 2023). Thus, control and management of this pest are difficult because of its high fecundity, wide range of host plants (Ahmad et al. 2013), and increased resistance to insecticides (Sreelakshmi et al. 2018; 2019; Babu and Singh 2022). In most current pest control practice, synthetic insecticides are still the most common and effective emergency method for S. litura control. However, the adverse effects of synthetic insecticides are significant, such as ‘3R’ (residue, resistance, resurgence) problems, disruption of agroecosystems and killing of nontarget organisms (Ansari et al. 2018; Torres and Bueno 2018) and residual toxicity (Pavela and Sedlák, 2018). Therefore, it is vital to reduce synthetic insecticide use in agriculture. While, parasitoid wasps, offer excellent alternatives for controlling insect pests. Currently, more than 70 species of parasitoids of S. litura have been reported (Ranga Rao et al. 1993; Xie et al. 1999).
The efficiency of egg parasitoids as control agents against lepidopterous pests is widely recognized because of their action on early pest stages before any damage occurs to the crop (Parra and Coelho 2019; Zang et al. 2021). The egg parasitoid Telenomus remus (Nixon) (Hymenoptera: Scelionidae) is an excellent biological agent not only because of its high fecundity, but also its effective action on layers of Spodoptera eggs, even parasitizing eggs located in the inner layers of the egg mass (Hou et al. 2022; Li et al. 2023). Furthermore, its high dispersal (Pomari-Fernandes et al. 2018) and host search capacities (Pomari et al. 2013) support its use in the field. Thus, T. remus is widely used in the control of Spodoptera spp. It is a parasitoid wasp native to Peninsular Malaysia and Papua New Guinea (Wengrat et al. 2021) and has been released against various pest species of Spodoptera (Pomari et al. 2012; Bueno et al. 2010; Ferrer 2001; 2021). Telenomus remus was widely released in Venezuela during the 1990s to control Spodoptera frugiperda (J. E. Smith) in corn fields (Ferrer 2001) and remains the main measure of integrated pest management (IPM) to control this pest (Ferrer 2021). Its release achieved a control effect of up to 90% and resulted in an overall reduction in insecticide use of 49%–80% against S. frugiperda eggs (Hernández et al. 1989; Ferrer 2021). Recently, it was reported that T. remus has established natural populations independent of field release in Brazil (Wengrat et al. 2021). In Ghana, 72–100% of Spodoptera egg masses were parasitized in the minor rainy season, compared with 33% during major rainy season (Agboyi et al. 2021). Telenomus remus was also considered the egg parasitoid most effective against S. frugiperda in its overwintering area in China (Zhao et al. 2023), with a field parasitism rate > 80% (Zhao et al. 2019).
Although T. remus can parasitize a variety of Spodoptera spp. (Wojcik et al. 1976; Jalali et al. 1987; Wu et al. 2021), most of research has focused on S. frugiperda (Colmenarez et al. 2022). However, S. litura is also an important natural host of T. remus in India, and its eggs were used for the mass-rearing of this parasitoid before being replaced by alternative hosts Agrotis biconica Kollar and Corcyra cephalonica (Stainton) (Joshi et al. 1976; Gupta and Pawar 1985; Kumar et al. 1986; Gautum and Gupta 1994). This is because alternative hosts can significantly reduce production costs, enabling the economically viable mass-rearing of parasitoids (Queiroz et al. 2017; da Silva et al. 2022). Improvements in the artificial diet of S. litura (Cao et al. 2014; Sun et al. 2015), which made its mass-rearing easier and cheaper, subsequently significantly reduced the production cost of parasitoids reared using this species (Chen et al. 2021). Thus, using S. litura eggs as a host for mass-rearing T. remus is a viable approach. Another important reason is that the alternative host C. cephalonica cannot be used to rear Chinese strain T. remus (Dai et al. 2019; Chen et al. 2021), whereas eggs of S. litura are suitable for mass-rearing T. remus (Chen et al. 2021; Wu et al. 2021), including the use of cold-stored S. litura eggs (Chen et al. 2022a). The effects of the age and generation of T. remus on its mass-rearing on S. litura eggs have also been previously evaluated (Chen et al. 2022b, 2023). However, the peak emergence time of male and female parasitoid offspring, and the prediction of the population of T. remus reared/parasitized on the S. litura have not been reported.
Life tables are a useful tool for researching population ecology as well as pest management because they can accurately reflect the population parameters of the target organisms, such as their survival, development, longevity, and fecundity (Chi and Liu 1985; Chi et al. 2022a). Compared with traditional life tables, the age-stage, two-sex life table integrates data from both age stages and both sexes, which makes the demographic parameters more accurate (AmirMaafi et al. 2022; Chi et al. 2019, 2022a, b). Therefore, age-stage, two-sex life tables are widely used in many studies involving population and community ecology, including pest management, pesticide resistance, predator–prey relationships, biological control, mass-rearing and harvesting of insects, and plant resistance (Gul et al. 2019; Saeed et al. 2021; Ren et al. 2022; Ullah et al. 2022; Zhu et al. 2022).
Studies on the interaction of natural enemies and their hosts improve understanding of the predation/parasitism dynamics of natural enemies, which can be helpful for formulating IPM programs (Carneiro et al. 2010). Functional response models are important tools to evaluate this interaction. All functional response curves proposed by Holling (1959) stabilize at a certain predation/parasitism rate level, which is related to the maximum number of prey/host attacked per time unit. Three different types (I, II, and III) of functional response can be obtained through mathematic models, represented by discrete curves (Holling 1959). The type II curve is more often related to systems involving arthropods, including predatory and parasitoid insects (Cave and Gaylor 1989). The main characteristic of the type II functional response is a gradual increase in the number of prey consumed up to a density at which the consumption rate stabilizes (Hassel 1978; Hassel et al. 1997). The type II equation was used to build the functional response curves of T. remus against S. frugiperda eggs (Carneiro et al. 2010).
In this study, we systematically investigated the parasitism, emergence, longevity, and developmental time of T. remus on S. litura eggs. The resulting demographic parameters generated were analyzed by using age-stage, two-sex life table theory using TWOSEX-MSChart and Cousume (Chi 2021a,b). Moreover, the functional response of T. remus against S. litura eggs was also evaluated, in terms of the effect of different egg densities of S. litura on parasitism by T. remus. Whereas a cubic logistic regression model was firstly used to screen the most appropriate functional response model fits for T. remus attacking S. litura. Such information, in order to provide relevant basis for biological control S. litura utilization of T. remus.
Materials and methods
A colony of T. remus was collected from the experimental station of South China Agricultural University, Guangzhou, Guangdong Province, China and then reared under laboratory conditions at 28 ± 1 ℃, relative humidity (RH) 75% ± 5%, and a 14 h light:10 h dark photoperiod for more than 20 generations using S. litura as the hosts. The same laboratory conditions were used for all experiments described below.
The S. litura colony had also been collected from the experimental station of South China Agricultural University and then reared in Guangxi Key Laboratory of Biology for Crop Diseases and Insect Pests, Nanning, China, for more than 2 years. An artificial diet, described by Shu et al. (2015), was used to rear S. litura larvae, using the laboratory conditions described above.
Performance of T. remus reared from S. litura eggs
Life table study
To investigate the development time and sex ratio of offspring parasitoids, one pair of adult T. remus newly emerged from S. litura eggs were collected and transferred into a glass tube (1.0 cm diameter × 10.0 cm height) and allowed to mate for 24 h; the tube also contained 1-day-old S. litura egg masses (each containing 100–150 eggs) and filter paper strips contained 30% honey solution. The tube was covered with gauze (100 mesh) to allow air exchange. After 24 h, the parasitized egg masses were transferred to a new test tube and numbered accordingly. The test was repeated ten times. When S. litura larvae hatched, they were removed from egg masses with a brush so that they were unable to feed on the remaining eggs. The developmental duration and sex ratio were observed and recorded daily until no more parasitoids emerged. For all eggs without emergence holes, a stereomicroscope (Motic, SMZ-168 BP, Hong Kong, China) was used to check and count the presence or absence of recognizable parasitoid cadavers.
In a parallel experiment, the daily egg production of offspring parasitoids were investigated. One male and one female parasitoid (< 6 h old, and unmated) were then matched in a glass tube (1.0 cm diameter × 10.0 cm height) containing egg masses (≈100 eggs) and provided with a few drops (0.1–0.2 mL) of 30% honey water as food. After 24 h, another ≈100 eggs were placed in the test tube. This cycle was repeated until the female wasp had died. The survival time of female wasp was then recorded. If the male wasp died before the female, its survival time was recorded and it was replaced, ensuring that a male wasp was present until the female had died. The level of parasitism (i.e., the number of black eggs), number of emerged parasitoids, and sex ratio of offspring were observed and recorded daily. The experiment was repeated 15 times. The developmental duration (matched cohort) and daily fecundity (initial cohort) of the female parasitoids were matched by a bootstrap-match based on the life table method as described by Amir-Maafi et al (2022).
Emergence time of T. remus
In a parallel experiment, the emergence times of male and female adult T. remus were investigated. A pair of newly emerged adult wasps (< 6 h old) were randomly collected and transferred to a glass tube (1.0 cm diameter × 10.0 cm height) and allowed to mate for 24 h; 30% honey solution was provided as a source of food. The male wasp was then removed from the glass tube and an egg mass (≈100 eggs) and a few drops of 30% honey solution were added; the female wasp was allowed to oviposit eggs for 24 h. Then, the female was removed and the parasitized eggs were left in the glass tube, which was covered with gauze. This experiment was repeated ten times. The emerged adult offspring were recorded at 6-h intervals until no further adults emerged.
Effect of host egg age on parasitism by T. remus
To evaluate the influence of egg age on parasitism of T. remus, ≈100 S. litura eggs of different ages (24, 36, 48, 60, and 72 h) were provided to each T. remus female (mated for 24 h) for 24 h. Eggs of each age were placed in a glass tube (1.0 cm diameter × 10.0 cm height) containing a female wasp, and each egg age had ten replicates. The parasitism and sex ratio of T. remus adults hatching from eggs of different ages were then recorded.
Functional response of T. remus parasitizing S. litura eggs
Female adults of T. remus mated for 24 h were used in this experiment. Each female wasp was introduced into a glass (1.0 cm diameter × 10.0 cm height) tube, which contained an egg mass of a different density (20, 40, 60, 80, 100, 120, and 140 eggs), and a filter paper strip dipped in 30% honey solution. Each egg density was replicated eight times. After being left to lay eggs for 24 h, the female wasps were removed and discarded. The parasitized egg masses were labeled and the level of parasitism recorded. Newly hatched larvae were counted and withdrawn from the tubes with a brush so they that were not able to feed on parasitized eggs. Such observations were performed in the first 5 days after oviposition at 12-h intervals. Any parasitoids that emerged from the remaining eggs after this time were counted once they had died (Carneiro et al. 2010).
TWOSEX-MSChart (Chi 2021a) was used to analyse developmental duration, survival rate, longevity, fecundity (effective parasitism) and parasitism, and CONSUME-MSChart (Chi 2021b) was used to analyse the net killing rate (including effective and non-effective parasitism) data (Chi and Liu 1985; Chi 1988; Chi et al. 2020). The formulas and definitions used in this study are showed in Additional file 1: Table S1. The means, variances, and standard errors (SE) of the life table parameters were estimated with the bootstrap (B = 100,000) technique (Wang et al. 2016; Zhao et al. 2021). All life table graphs were created using SigmaPlot 12.5 (Systat Software, Inc., San Jose, CA, USA).
Data analyses were performed using the SPSS version 20 software package (SPSS Inc., Chicago, IL, USA). A Shapiro–Wilk test for normality was used to determine if datasets were normally distributed, and a Levene's test to determine homogeneity of variances. The Shapiro–Wilk test showed that the number of female and male offspring at different time intervals (first sets) and different hosts egg ages (second sets) were not normally distributed, and the Levene's test for homogeneity of variances showed none of the emergence time or hosts egg ages datasets variance were equal. Datasets had Poisson distributions and therefore this was selected in subsequent analyses. To test first and second sets of null hypotheses, a generalized linear model (GLM) (St-Pierre et al. 2018) was selected. Distribution of residual errors with a logarithm link function were selected. Similarly, when comparing the emergence numbers between females and males with respect to host egg age and time periods, a Poisson distribution was used in the GLM programs. Figures representing the emergence time and parasitism were generated using GraphPad Prism 9.0 (GraphPad Software, Inc., San Diego, CA, USA).
A logistic regression of the proportion of prey consumed (Ne/N0) as a function of initial density (N0) was used to determine the shape of the functional response. The type of functional response was determined by fitting data to Eq. 1 (Juliano 2001):
where (Ne/N0) is the proportion of a prey consumed, and P0, P1, P2, and P3 are the maximum likelihood estimates of the intercept, linear, quadratic and cubic coefficients estimated through the CATMOD procedure in SAS, respectively. The sign of P1 and P2 was used to distinguish the shape of the curves. When P1 < 0, the predator/parasitoid displays a type II functional response, indicating that the proportion of prey consumed declines monotonically with host density (De Clercq et al. 2000). When P1 > 0 and P2 < 0, the predator/parasitoid displays a type III functional response (Juliano 2001; Song et al. 2016). Given that our data fitted a type II functional response curve (Table 1), the equation for parasitoids utilized was Eq. 2:
where Na is the number of parasitized hosts, a′ is the parasitoid searching rate, Tt is the total time available for the parasitoid (24 h), N is the host density, and Th is the handling time.
Under the matched (female 94: male 80) and initial cohorts (female 15: male 15) of T. remus, key demographic parameters, such as the developmental time, adult longevity, total longevity, total preoviposition period (TPOP), adult preoviposition period (APOP), oviposition days, and fecundity, were analyzed (Table 2). Preadult duration of females, female offspring, and female longevity were 10.30 days, 0.495, and 8.68 days respectively, and males were 9.71 day, 0.421, and 7.24 days, respectively. With a total preadult duration of 10.03 days, and a preadult survival rate (sa) of 0.9158. With adult longevity and total longevity of 8.02 days and 17.37 days, respectively. The TPOP of T. remus was 10.03 days, which was the same as the preadult duration of females because the APOP was zero. Fecundity (F) and oviposition days (Od) of T. remus were 186.90 eggs/female and 7.303 days, respectively.
The age-stage survival rates (sxj) of T. remus on S. litura eggs showed that the adults began to emerge after 9 days, with obvious overlaps between the stages (Fig. 1a). Adult females of T. remus parasitized on S. litura eggs survived for 16 days, with sxj peaking at 49.47% at the age of 12 days. Peak sxj of male adults was 42.11% at the age of 12 days. Female adults had a longer longevity than that of male adults of T. remus reared on S. litura eggs (Fig. 1a).
The age-specific survival rate (lx), age-specific fecundity (mx), age-stage specific effective parasitism rate (fx2), and age-specific net maternity (lxmx) of T. remus on S. litura eggs are showed in Fig. 1b. The peak mx and lxmx of T. remus were 18.70 and 17.12 offspring/female, respectively. The peak fx2 of T. remus was 50 offspring/female at 9 days of age.
The life expectancy (exj) of a T. remus egg newly laid in S. litura eggs was 24 days. The highest exj of T. remus males and females was 9 days (Fig. 2a). The reproductive value (vxj) of T. remus peaked at 126.30 d–1 at 9 days of age (Fig. 2b).
The population demographic parameters of T. remus on the S. litura eggs are showed in Table 3. The gross reproduction rate (GRR), net reproductive rate (R0), intrinsic rate of increase (r), finite rate of increase (λ), mean generation time (T), and population doubling time (DT) of T. remus were 116.42, 92.47, 0.3506 d–1, 1.4199 d–1, 12.91 days, and 1.98 days, respectively.
Given that T. remus is an egg parasitoid, only female adult wasps can parasitize, and therefore kill, host eggs; thus, the age-specific S. litura eggs-killing rate (kx), age-specific net killing rate (qx), and cumulative killing rate (cx) were all zero before the adult stage (Fig. 3a). Peak kx of T. remus was 20.21 eggs per parasitoid, occurring by 12 days of age. Peak qx was also reached by 12 days of age (18.51 eggs/parasitoid) (Fig. 3a). Thus, with a starting population of ten T. remus eggs, after 30 days, the population reached 74,169 immature individuals, 204 male, and 304 female adults; by day 25, the total killing rate of T. remus reared on S. litura eggs was 11,816 eggs (Fig. 3b).
Parameters of T. remus parasitism and killing are showed in Table 4. The net non-effective parasitism rate (G0) was 15.26 offspring/female. The numbers of female and male offspring produced by T. remus on S. litura eggs were 146.38 and 43.59, respectively. The net killing rate (C0) of T. remus was 101.49 eggs per parasitoid. The stable killing rate (ψ), finite killing rate (ω), and transformation rate (Qp) of T. remus were 0.6541, 0.4606, and 1.0976, respectively.
The emergence of male and female parasitoids was observed over a 6-h period, with significant differences noted. Male parasitoids emerged in significantly greater numbers than females during the time intervals of 18:00–24:00 h and 0:00–06:00 h (Wald statistic 84.03 df 1, P < 0.001; Wald statistic 451.26, df 1, P < 0.001). Conversely, the number of female parasitoids was significantly higher than males between 06:00–12:00 h (Wald statistic 151.17, df 1, P < 0.001). However, no significant difference was observed between the number of female and male parasitoids emerging during 12:00–18:00 h (Wald statistic 1.50, df 1, P = 0.221). Male parasitoids showed a greater emergence pattern during the night (0:00–06:00 h; Wald statistic 360.66, df 3, P < 0.001), whereas female parasitoids emerged predominantly during the morning (06:00–12:00 h) (Wald statistic 341.79, df 3, P < 0.001) (Fig. 4a).
Parasitism on host eggs of different ages
The study revealed a significant difference in the emergence of male and female parasitoids across all egg ages tested. The results indicated that 24-h-old host eggs (Wald statistic 230.25, df 1, P < 0.001) produced more females than they did males, whereas 36-h, 48-h and 60-h-old host eggs (Wald statistic 53.58, df 1, P < 0.01; Wald statistic 35.34, df 1, P < 0.001; Wald statistic 5.10, df 1, P = 0.024) produced more males than females. However, there was no significant difference in the emergence of male and female parasitoids from 72-h-old host eggs (Wald statistic 2.50, df 1, P = 0.114). The results also demonstrated that T. remus produced the highest number of females on 24-h-old eggs (Wald statistic 476.00, df 3, P < 0.001), whereas the most males were generated on 48-h-old eggs (Wald statistic 305.37, df 3, P < 0.001) (Fig. 4b).
The results of logistic regression analysis (Table 1) indicated that the linear coefficient (P1) was negative for parasitism, indicating a type II functional response. The mean number of eggs parasitized by T. remus females increased with higher egg host densities, and stabilized at and beyond a density of 100 eggs (Fig. 5). Through disk equation fitting, the instantaneous attack rate (aʹ), handling time (Th), and maximum attack rates (T/Th) were obtained, with values of 0.9764, 0.0066 day, and 152.3 eggs/day, respectively. With the increase of host egg density, T. remus showed a decrease in its searching rate (Fig. 5).
The life table method is a useful tool for researching population ecology as well as pest management because it can accurately reflect the population parameters of the research organism, such as survival, development, longevity, and fecundity (Chi and Liu 1985; Chi et al. 2022a, b). The life table data showed that the T. remus performed well on eggs of S. litura, indicating that these eggs could be used to rear increased numbers of parasitoids, in turn controlling the pest itself. Our results were also supported by previous relevant studies (Chen et al. 2021, 2022b, 2023).
Previous studies have showed that some parasitoids can reproduce once they emerge, whereas others need extra nutrients and time to do so (Xu et al. 2015, 2018; Zhao et al. 2021). Telenomus remus belongs to the latter group of parasitoids because APOP = 0. Generally, parasitism decreased with the increase in female parasitoid age, and female longevity was also limited; thus, the release time (age) of parasitoids becomes important. Some studies showed that 3-day- and 4-day-old parasitoids had higher parasitism performance on all age eggs compared with 1-day- and 2-day-old parasitoids (Chen et al 2022b), but the total parasitism during the oviposition period was not evaluated. Theoretically, the earlier the release (exposing), the higher the total parasitism would be. In the current study, a total of 186.90 S. litura eggs were parasitized by a female T. remus during her lifetime, and 70% of eggs were laid during the first 5 days (Fig. 2b), although the age of T. remus virgin females did not affect the parasitism of S. frugiperda eggs (Queiroz et al. 2019). The shorter the longevity of the female, the more APOP should be considered when releasing the parasitoids. The female longevity of T. remus reared on S. litura eggs was 8.68 days (Table 2), which is relatively longer than that of T. remus reared on S. frugiperda eggs (8.3 days), but shorter than that of T. remus reared on eggs of different generations of C. cephalonica (13.1–15.3 days) (Pomari-Fernandes et al. 2015).
Usually, a higher fecundity or faster development rate (lower TPOP) will generate a higher intrinsic rate of increase (r) (Hu et al. 2014), and vice versa. Our results showed a lower fecundity and longer development time of T. remus on S. litura eggs (186.90 eggs/female and 10.03 days, respectively) (Table 2) compared with those reared on S. frugiperda eggs (214.4 eggs/female and 9.0 days, respectively) (Bueno et al. 2014) when the parental generation was reared on their respective primary hosts under the same temperature (28 ℃). However, a higher fecundity of T. remus was observed when reared on S. litura eggs than reared on S. frugiperda eggs (174.44 eggs/female) (Chen et al. 2023).
Similar development rates were obtained in another study, in which the development time of T. remus was 13.3 days on S. litura eggs and 12.2 days on S. frugiperda eggs at 26 ℃ (Li et al. 2023). The longer development time might result from the lower experimental temperature used. However, the fecundity results from different studies vary; for example, 173.5 and 145.8 eggs/female were reported using a field strain and a laboratory-reared strain of T. remus reared on S. frugiperda eggs, respectively (Naranjo-Guevara et al. 2020), and 140.8 eggs/female was reported by Pomari-Fernandes et al. (2015). Chen et al. (2021) showed that the fecundity of T. remus was ≈150 eggs/female on S. litura eggs among different photoperiods, a slightly longer (≈1 day) development time was recorded for T. remus on S. litura eggs compared with those reared on S. frugiperda eggs. In the current study, the r of T. remus reared on S. litura eggs (0.3506 day–1) (Table 2) was lower than that reported by Chen et al. (2021) (0.354 ~ 0.463 day–1 among different photoperiods). In our study, a short T and DT were found for T. remus reared on S. litura eggs (12.91 days and 1.98 days, respectively); thus, the population growth rate was fast, similar to the results of Chen et al. (2023). This result was also been confirmed by a population projection (Fig. 4b).
The parasitic behavior of female parasitoids plays a crucial role in insect pest control, making the determination of the sex ratio a pivotal factor for population dynamics and effective pest management. Numerous studies have identified a range of influential factors, including host quality, host density, female age, and strain differences (Carneiro et al. 2010; Giunti et al. 2015; Chen et al. 2021). In our study, we observed that the proportion of female T. remus reared on S. litura eggs (Nf/N) was 0.495. This finding deviated from the results reported by Li et al. (2023) (> 0.78, across different host ages) and Wu et al. (2021) (> 0.9), while it closely resembled the outcome reported by Huo et al. (2019) (0.451). This variability in the sex ratio of T. remus on S. litura eggs underscores the adaptability and flexibility of this wasp's sex ratio strategy. For instance, Chen et al. (2021) documented that the sex ratio of T. remus reared on S. litura eggs exhibited a decreasing trend as the parasitoid:host egg ratio increased. In contrast, our research highlights the significant impact of egg age on the sex ratio of T. remus (see Fig. 1b). This variation is likely due to changes in nutrient content and chemical defense substances within the eggs as they age (Vinson 2010).
In the context of pest control effectiveness, the net killing rate (C0) provides a comprehensive measure that accounts for both effective and non-effective parasitism (Zang et al. 2023). Non-effective parasitism, while not contributing to population growth, plays a crucial role in limiting pest population growth. In our study, the net non-effective parasitism rate (G0) of T. remus on S. litura eggs was 15.26, surpassing the values reported for Anastatus spp. on Caligula japonica Moore eggs (0.56–9.11) (Zang et al. 2023). This aligns with our life table results, which indicated a preadult survival rate (sa) of 0.9158 (< 1) (Table 2). Consistently, our findings are supported by emergence rates below 100%, in line with other studies (Wu et al. 2021; Li et al. 2023).
Functional response is an important tool for studying basic aspects of parasitoid–host interactions, with search rates and handling times being particularly important because they can both contribute to the impact of parasitoids on host population dynamics. Previous work reported that T. remus spends 40.6 s handling an S. frugiperda egg (Carneiro et al. 2010), and 37 s on an S. littoralis egg (Schwartz and Gerling 1974), which is significantly lower than that spent on S. litura eggs reported by our study (57.0 s/egg). The shorter time required for host recognition and handling means that parasitoids can parasitize more hosts per unit time. Thus, based on the differences in handing time, S. littoralis and S. frugiperda appear to be suitable for rearing of, and control by, T. remus. The way in which females handle host eggs and the time they take to do so are directly related to the number of parasitized eggs. The daily mean parasitism rate of T. remus on S. frugiperda (Carneiro et al. 2010) was significantly higher than that of S. litura (Fig. 5), regardless of host density. However, a higher search rate was recorded at the lowest S. litura density (20 eggs:1 parasitoid) (Fig. 5), whereas a higher search rates was found on both low (25 eggs:1 parasitoid) and medium densities (100 eggs:1 parasitoid) of S. frugiperda eggs (Carneiro et al. 2010). A similar result reported that a lower host:parasitoid ratio (14–20:1) was optimal for rearing T. remus on S. litura eggs (Chen et al. 2021), which was concordant with our study. Our results suggest that the optimal parasitoid-host density was 20:1 for mass rearing or field release (Fig. 5). However, a study showed that an egg:parasitoid ratio of 30:1 and 50:1 achieved the highest rates of parasitism and emergence of T. remus reared on S. litura eggs (Xie et al. 2021). Thus, functional response studies can provide data for reference decisions related to mass-rearing and field release that depend on density effects.
In the past, T. remus was used as a potential dominant parasitoid of S. frugiperda. However, our study found, as a natural host of T. remus, S. litura eggs are suitable for the mass-rearing of this wasp for field release to control this pest, as supported by two-sex life table and functional response data analyses. These findings are helpful to broaden the understanding of T. remus against Spodoptera spp.
The datasets are available from the corresponding author on reasonable request.
Agboyi LK, Layodé BFR, Fening KO, Beseh P, Clottey VA, Day R, Kenis M, Babendreier D. Assessing the potential of inoculative field releases of Telenomus remus to control Spodoptera frugiperda in Ghana. InSects. 2021;12:665. https://doi.org/10.3390/insects12080665.
Ahmad M, Ghaffar A, Rafiq M. Host plants of leaf worm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in Pakistan. Asian J Agric Biol. 2013;1(1):23–8.
Amir-Maafi M, Chi H, Chen ZZ, Xu YY. Innovative bootstrap-match technique for life table set up. Entomol Gen. 2022;42(4):597–609.
Ansari S, Waheed S, Ali U, Jones KC, Sweetman AJ, Halsall C, Malik RN. Assessing residual status and spatial variation of current-use pesticides under the influence of environmental factors in major cash crop growing areas of Pakistan. Chemosphere. 2018;212:486–96.
Babu SR, Singh B. Resistance in Spodoptera litura (F.) to insecticides and detoxification enzymes. Ind J Entomol. 2022;61:1–5. https://doi.org/10.55446/IJE.2022.519.
Bueno RCOF, Carneiro TR, Bueno AF, Pratissoli D, Fernandes OA, Vieira SS. Parasitism capacity of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) eggs. Braz Arch Biol Techn. 2010;53:1339. https://doi.org/10.1590/S1516-89132010000100017.
Bueno RCOF, Bueno ADF, Xavier MFDC, Carvalho MM. Telenomus remus (Hymenoptera: Platygastridae) parasitism on eggs of Anticarsia gemmatalis (Lepidoptera: Eribidae) compared with its natural host Spodoptera frugiperda (Lepidoptera: Noctuidae). Ann Entomol Soc Am. 2014;107(4):799–808.
Cao LJ, Yang F, Tang SY, Chen M. Development of an artificial diet for three lepidopteran insects. Chin J Appl Entomol. 2014;51(5):1376–86.
Carneiro TR, Fernandes OA, Cruz I, Bueno RCOF. Functional response of Telenomus remus Nixon (Hymenoptera, Scelionidae) to Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae) eggs: effect of female age. Rev Bras Entomol. 2010;54:692–6.
Cave RD, Gaylor MJ. Functional response of Telenomus reynoldsi (Hym: Scelionidae) at five constant temperatures and in an artificial plant arena. Entomophaga. 1989;34:3–10.
Chen WB, Li YY, Wang MQ, Mao JJ, Zhang LS. Evaluating the potential of using Spodoptera litura eggs for mass-rearing Telenomus remus, a promising egg parasitoid of Spodoptera frugiperda. InSects. 2021;12(5):384–384.
Chen WB, Zhang HZ, Jing XY, Li YY, Wang MQ, Mao JJ, Weng QF, Nie R, Zhang LS. Cold storage of Spodoptera litura eggs and Telenomus remus adults for improving mass-rearing efficiency. J Appl Entomol. 2022a;146(5):626–35.
Chen WB, Wang MQ, Li YY, Mao JJ, Zhang LS. Providing aged parasitoids can enhance the mass-rearing efficiency of Telenomus remus, a dominant egg parasitoid of Spodoptera frugiperda, on Spodoptera litura eggs. J Pest Sci. 2022b. https://doi.org/10.1007/s10340-022-01579-0.
Chen WB, Liu H, Chen B, Chen JJ, Wang MQ, Shen ZJ, Li YY, Mao JJ, Zhang LS. Quality assessment of Telenomus remus successively reared on Spodoptera litura eggs for 30 generations. Pest Manag Sci. 2023. https://doi.org/10.1002/ps.7466.
Chi H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol. 1988;17(1):26–34.
Chi H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. 2021a. http://220.127.116.11/Ecology/.
Chi H. CONSUME-MSChart: a computer program for consumption rate analysis based on the age stage, two-sex life table. 2021b. http://18.104.22.168/Ecology/.
Chi H, Liu H. Two new methods for the study of insect population ecology. Bull Inst Zool. 1985;24(2):225–40.
Chi H, Fu JW, You MS. Age-stage, two-sex life table and its application in population ecology and integrated pest management. Acta Entomol Sinica. 2019;62:255–62.
Chi H, You MS, Atlıhan R, Smith CL, Kavousi A, Özgökçe MS, Güncan A, Tuan SJ, Fu JW, Xu YY, Zheng FQ, Ye BH, Chu D, Yu Y, Gharekhani G, Saska P, Gotoh T, Schneider MI, Bussaman P, Gökçe A, Liu TX. Age-Stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen. 2020;40(2):102–23.
Chi H, Güncan A, Kavousi A, Gharakhani G, Atlihan R, Özgökçe MS, Shirazi J, AmirMaafi M, Maroufpoor M, Roya T. TWOSEX-MSChart: the key tool for life table research and education. Entomol Gen. 2022a;42(6):845–9.
Chi H, Kara H, Özgökçe MS, Atlihan R, Güncan A, Rişvanlı MR. Innovative application of set theory, Cartesian product, and multinomial theorem in demographic research. Entomol Gen. 2022b;42(6):863–74.
Colmenarez YC, Babendreier D, Ferrer WFR, Vásquez-Freytez CL, de Freitas BA. The use of Telenomus remus (Nixon, 1937) (Hymenoptera: Scelionidae) in the management of Spodoptera spp.: potential, challenges and major benefits. CABI Agric Biosci. 2022;3(1):5. https://doi.org/10.1186/S43170-021-00071-6.
da Silva CB, de Carvalho VR, de Andrade Bomfim JP, da Silva NNP, de Oliveira RC. Influence of factitious hosts on the morphometry and diversity of endosymbionts of the egg parasitoid Telenomus remus: insights for applied biological control. Phytoparasitica. 2023;51(1):77–88.
Dai P, Sun JW, Chen YM, Bao HP, Zhang LS, Nkunika POY, Zang LS. Discovery of three egg parasitoid species for the control of Spodoptera frugiperda (Smith). J Jilin Agric Univ. 2019;41(5):505–9.
De Clercq P, Mohaghegh J, Tirry L. Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biol Control. 2000;18(1):65–70. https://doi.org/10.1006/bcon.1999.0808.
EPPO (European and Mediterranean Plant Protection Organization). EPPO Global Database. https://gd.eppo.int/taxon/PRODLI/. Accessed 21 Feb 2023.
Ferrer F. Biological control of agricultural insect pests in Venezuela; advances, achievements, and future perspectives. Biocontrol News Inf. 2001;22(3):67–74.
Ferrer F. Biological control of agricultural pests in Venezuela: historical achievements of Servicio Biológico (SERVBIO). Rev Ambient. 2021;55(1):327–44.
Gautum RD, Gupta T. Mass-multiplication of the cutworm, Agrotis spinifera (Hübner). Ann Agric Res. 1994;15:64–9.
Giunti G, Canale A, Messing R, Donati HE, Stefanini C, Michaud JP, Benelli G. Parasitoid learning: current knowledge and implications for biological control. Biol Control. 2015;90:208–19.
Gul H, Ullah F, Biondi A, Desneux N, Qian D, Gao XW, Song DL. Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia Odoriphaga. Entomol Gen. 2019;39(2):81–92.
Gupta M, Pawar AD. Multiplication of Telenomus remus Nixon on Spodoptera litura (Fabricius) reared on artificial diet. J Adv Zool. 1985;6(1):13–7.
Hassel MP. The dynamic of arthropod predator-prey systems. Princeton: Princeton University Press. 1978;13(11):237.
Hassel MP, Lawton JH, Beddington JR. Sigmoid functional responses by invertebrate predator and parasitoids. J Anim Ecol. 1997;46:249–62.
Hernández D, Ferrer F, Linares B. Introducción de Telenomus remus Nixon (Hym: Scelionidae) para controlar Spodoptera año (Lep: Noctuidae) en Yaritagua. Venezuela Agron Trop. 1989;39(4–6):199–205.
Holling CS. Some characteristics of simple types of predation and parasitism. Can Entomol. 1959;91(7):385–98.
Hou YY, Yue M, Xu W, Desneux N, Nkunika POY, Bao HP, Zang LS. Spodoptera frugiperda egg mass scale thickness modulates Trichogramma parasitoid performance. Entomol Gen. 2022;42(4):589–96.
Hu LX, He ZS, Zhang XG. Age-stage two-sex life tables of the experimental population of Problepsis superans (Lepidoptera: Geometridae) on three igustrum species. Acta Entomol Sinica. 2014;57(12):1408–17.
Huo LX, Zhou JC, Ning SF, Zhao Q, Zhang LX, Zhang ZT, Zhang LS, Dong H. Biological characteristics of Telenomus remus against Spodoptera frugiperda and Spodoptera litura eggs. Plant pro. 2019;45:60–4.
Jalali SK, Singh SP, Ballal CR, Kumar P. Evaluation of different insect eggs for rearing of egg parasite, Telenomus remus Nixon (Hymenoptera: Scelionidae). J Biol Control. 1987;1(2):138–40.
Joshi BG, Ramaprasad G, Sitaramaiah S, Sathyanarayana CVV. Some observations on Telenomus remus Nixon, an egg parasite of the tobacco caterpillar, Spodoptera litura (F.). Tob Res. 1976;2:17–20.
Juliano SA. Non-linear curve fitting: predation and functional response curves. In: Schneider SM, Gurevitch J, editors. Design and analysis of ecological experiments. New York: Oxford University Press; 2001. p. 178–96.
Kumar DA, Pawar AD, Divakar BJ. Mass multiplication of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Corcyra cephalonica Stainton (Lepidoptera: Galleridae). J Adv Zool. 1986;7(1):21–3.
Li TH, Ma Y, Hou YY, Nkunika POY, Desneux N, Zang LS. Variation in egg mass scale thickness of three Spodoptera species and its effects on egg parasitoid performance. J Pest Sci. 2023. https://doi.org/10.1007/s10340-023-01608-6.
Naranjo-Guevara N, Santos LAOD, Barbosa NCCP, Castro ACMC, Fernandes OA. Long-term mass rearing impacts performance of the egg parasitoid Telenomus remus (Hymenoptera: Platygastridae). J Entomol Sci. 2020;55(1):69–86.
Parra JRP, Coelho A. Applied biological control in Brazil: from laboratory assays to field application. J Insect Sci. 2019;19(2):1–6.
Pavela R, Sedlák P. Post-application temperature as a factor influencing the insecticidal activity of essential oil from Thymus vulgaris. Ind Crop Prod. 2018;113:46–9.
Pomari AF, Bueno AF, Bueno RCOF, Menezes ADO. Biological characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Ann Entomol Soc Am. 2012;105(1):73–81.
Pomari AF, Bueno AF, Bueno RCOF, Menezes ADO. Telenomus remus Nixon egg parasitization of three species of Spodoptera under different temperatures. Neotrop Entomol. 2013;42:399–406.
Pomari-Fernandes A, Bueno AF, Queiroz AP, De Bortoli SA. Biological parameters and parasitism capacity of Telenomus remus Nixon (Hymenoptera: Platygastridae) reared on natural and factitious hosts for successive generations. Afr J Agric Res. 2015;10:3225–33.
Pomari-Fernandes A, Bueno AF, De Bortoli SA, Favetti BM. Dispersal capacity of the egg parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae) in maize and soybean crops. Biol Control. 2018;126:158–68.
Queiroz APD, Bueno AF, Pomari-Fernandes A, Grande MLM, Bortolotto OC, da Silva DM. Quality control of Telenomus remus (Hymenoptera: Platygastridae) reared on the factitious host Corcyra cephalonica (Lepidoptera: Pyralidae) for successive generations. Bull Entomol Res. 2017;107(6):791–8.
Queiroz APD, Favetti BM, Luski PG, Gonalves J, Neves PMOJ, Bueno ADF. Telenomus remus (hymenoptera: platygastridae) parasitism on Spodoptera frugiperda (lepidoptera: noctuidae) eggs: different parasitoid and host egg ages. Semin Cienc Agrar. 2019;40:2933. https://doi.org/10.5433/1679-0359.2019v40n6supl2p2933.
Ranga Rao GV, Wightman JA, Ranga Rao DV. World review of the natural enemies and diseases of Spodoptera litura (F.) (Lepidoptera: Noctuidae). Int J Trop Insect Sci. 1993;14:273–84.
Ravishankar BS, Venkatesha MG. Effect of host plants on the virulence of nuclear polyhedrosis virus screened against Spodoptera litura (p.) (Lepidoptera: Noctuidae). Crop Res. 2011;42(1–3):289–95.
Ren XY, Huang J, Li XW, Zhang JM, Zhang ZJ, Chen LM, Hafeez M, Zhou SX, Lu YB. Frozen lepidopteran larvae as promising alternative factitious prey for rearing of Orius species. Entomol Gen. 2022;42(6):959–66.
Saeed R, Abbas N, Hafez AM. Biological fitness costs in emamectin benzoate-resistant strains of Dysdercus koenigii. Entomol Gen. 2021;41(3):267–78.
Schwartz A, Gerling D. Adult biology of Telenomus remus (Hymenoptera: Scelionidae) under laboratory conditions. Entomophaga. 1974;19:482–92.
Shekhawat SS, Ansari MS, Basri M. Effect of host plants on life table parameters of Spodoptera litura. Ind J Pure Appl Biosci. 2018;6(2):324–32.
Shu Y, Zhou J, Lu K, Li K, Zhou Q. Response of the common cutworm Spodoptera litura to lead stress: changes in sex ratio, Pb accumulations, midgut 886 cell ultrastructure. Chemosphere. 2015;139:441–51.
Song ZW, Zheng Y, Zhang BX, Li DS. Prey consumption and functional response of Neoseiulus californicus and Neoseiulus longispinosus (Acari: Phytoseiidae) on Tetranychus urticae and Tetranychus kanzawai (Acari: Tetranychidae). Syst Appl Acarol. 2016;21:936–46.
Sreelakshmi P, Mathew TB, Josephrajkumar A, Paul A. Synergist induced susceptibility of tobacco caterpillar, Spodoptera litura (Fabricius) from Kerala, India exposed to conventional insecticides. Phytoparasitica. 2018;46(1):97–104.
Sreelakshmi P, Mathew TB, Umamaheswaran K, Josephrajkumar A. Modulation in activity profiles in insecticide-resistant population of tobacco caterpillar, Spodoptera Litura (Fabricius). Curr Sci. 2019;116(4):664–9.
St-Pierre AP, Shikon V, Schneider DC. Count data in biology—data transformation or model reformation? Ecol Evol. 2018;8(6):3077–85. https://doi.org/10.1002/ece3.3807.
Sun G, Liu SW, Chang XH, Luo YM, Li KK, Song YQ. Study on effect of an improved artificial rearing technique for Spodoptera litura Fabricius. Shandong Agr Sci. 2015;47:104–6.
Toke NR, Purohit MS, Ghetiya LV. Influence of host plants on the susceptibility of Spodoptera litura (Fabricius) to certain insecticides. Trends Biosci. 2016;8(9):2330–4.
Torres JB, Bueno AF. Conservation biological control using selective insecticides: a valuable tool for IPM. Biol Control. 2018;126:53–64.
Ullah F, Gul H, Hafeez M, Güncan A, Tariq K, Desneux N, Zhao ZH, Li ZH. Impact of temperature stress on demographic traits and population projection of Bactrocera dorsalis. Entomol Gen. 2022;42(6):949–57.
Vinson SB. Nutritional ecology of insect egg parasitoids. In: Cônsoli FL, Parra JRP, Zucchi RA, editors. Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, New York. 2010;(9):25–55.
Wang SY, Chi H, Liu TX. Demography and parasitic effectiveness of Aphelinus asychisreared from Sitobion avenaeas a biological control agent of Myzus persicae reared on chili pepper and cabbage. Biol Control. 2016;92:111–9.
Wengrat APGS, Coelho Junior A, Parra JRP, Takahashi TA, Foerster LA, Corrêa AS, Zucchi RA. Integrative taxonomy and phylogeography of Telenomus remus (Scelionidae), with the first record of natural parasitism of Spodoptera spp. in Brazil. Sci Rep. 2021;11:14110. https://doi.org/10.1038/s41598-021-93510-3.
Wojcik B, Whitcomb WH, Habeck DH. Host range testing of Telenomus remus (Hymenoptera: Scelionidae). Fla Entomol. 1976;59:195–8.
Wu ZM, Zhan YG, Ke CL, Li WJ, Wang ZJ, Feng GY, Gao X, Wu GX, Xie YH. Screening of host species for the mass rearing of Telenomus remus Nixon (Hymenoptera: Platygastridae). Chin J Biol Control. 2021;37(6):1140–5.
Xie JJ, Hu MY, Xu ZF. Natural enemies and biological control of Spodoptera litura Fabricius. Nat Enemies inSects. 1999;21(2):82–92.
Xie YH, Wang CY, Chen YQ, Shi PL, Zhan YG, Wang ZJ, Wu ZM, Wu GX, Shi AM. A Preliminary study of mass rearing Telenomus remus Nixon on Spodoptera litura. Chin J Biol Control. 2021;37(6):1146–51.
Xu HY, Yang NW, Wan FH. Female reproductive system and ovary development of two parasitoids of tobacco whitefly. Sci Technol Rev. 2015;33(7):79–83.
Xu HY, Yang NW, Chi H, Ren GD, Wan FH. Comparison of demographic fitness and biocontrol effectiveness of two parasitoids, Encarsia sophia and Eretmocerus hayati (Hymenoptera: Aphelinidae), against Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Manag Sci. 2018;74(9):2116–24.
Yang HH, Li JQ, Ma S, Yao WC, Chen YW, Wakil AE, Dewer Y, Zhu XY, Sun L, Zhang YN. RNAi-mediated silencing of SlitPer disrupts sexpheromone communication behavior in Spodoptera litura. Pest Manag Sci. 2023. https://doi.org/10.1002/ps.7593.
Zang LS, Wang S, Zhang F, Desneux N. Biological control with Trichogramma in China: history, present status, and perspectives. Annu Rev Entomol. 2021;66:463–84.
Zang ZY, Chen YM, Xu W, Zang LS. Evidence of two-sex life table analysis supporting Anastatus japonicus, a more effective biological control agent of Caligula japonica compared with other two Anastatus species. Biol Control. 2023;180: 105188. https://doi.org/10.1016/j.biocontrol.2023.105188.
Zhao X, Zhu KH, Zhang ZT, He KL, Zhang LS, Zhou JC, Dong H. Preliminary evalation of the control efficacy of Telenomus remus against Spodoptera frugiperda in field conditions. Plant pro. 2019;46:74–7.
Zhao Y, Zhao CL, Yang X, Chi H, Dai P, Desneux N, Benellie G, Zang LS. Yacon as an alternative host plant for Encarsia formosa mass-rearing: validating amultinomial theorem for bootstrap technique. Pest Manag Sci. 2021;77(5):2324–36.
Zhao HX, Xian XQ, Yang NW, Zhang YJ, Liu H, Wan F, Guo JY, Liu WX. Insights from the biogeographic approach for biocontrol of invasive alien pests: estimating the ecological niche overlap of three egg parasitoids against Spodoptera frugiperda in China. Sci Total Environ. 2023;862: 160785. https://doi.org/10.1016/j.scitotenv.2022.160785.
Zhu YF, Tan XM, Qi FJ, Teng ZW, Fan YJ, Shang MQ, Lu ZZ, Wan FH, Zhou HX. The host shift of Bactrocera dorsalis: early warning of the risk of damage to the fruit industry in northern China. Entomol Gen. 2022;42(5):691–9.
This work is supported by the Natural Science Foundation of Guangxi (NO. 2019GXNSFBA245004). The authors are thankful to acknowledge the comments of the anonymous reviewers.
Ethics approval and consent to participate
Consent for publication
The authors declared that they have no competing interest in connection with the evaluated manuscript.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Shen, Z., Liu, LH., Zang, LS. et al. Evaluation of Telenomus remus (Hymenoptera: Platygastridae) as a biocontrol agent of Spodoptera litura (Lepidoptera: Noctuidae) based on two-sex life table and functional response analyses. CABI Agric Biosci 4, 48 (2023). https://doi.org/10.1186/s43170-023-00188-w