Introduction
The fall armyworm (FAW), Spodoptera frugiperda, formerly known as Laphygma frugiperda (Smith and Abbott), is a serious pest of maize native to tropical and subtropical regions of the Americas since 1797 (Goergen et al., Reference Goergen, Kumar, Sankung, Togola and Tamo2016; Rwomushana, Reference Rwomushana2019). However, in 2016, it invaded Africa and abruptly advanced throughout most African countries and later in Asia. In India, this alarming pest was detected first time in 2018 in Karnataka and has now been spread to almost all the maize-growing states (Sharanabasappa et al., Reference Sharanabasappa, Kalleshwaraswamy, Asokan, Mahadeva, Swamv, Maruthi, Pavithra, Hegde, Navi, Prabhu and Goergen2018). According to a preliminary calculation, FAW was expected to affect about 170,000 ha of maize crops in ten Indian states (Sangomla and Kukreti, Reference Sangomla and Kukreti2023). The prolificacy of S. frugiperda (egg masses usually contain hundreds of eggs) and its potentiality to emigrate long distances are the two peculiar traits that facilitated it to invade more than 80 countries worldwide (Wu et al., Reference Wu, Zhang, Liu, Cheng, Su, Sappington and Jiang2022).
FAW is known to infest more than 353 plants belonging to 76 different families; mostly under Poaceae followed by Asteraceae and Fabaceae (Montezano et al., Reference Montezano, Specht, Sosa-Gomez, Roque-Specht, Sousa-Silva, Paula-Moraes, Peterson and Hunt2018), implicating that polyphagy can enable it to develop or sustain populations outside of the primary cropping areas or cropping season imparting larger pest pressure. This wider host range of FAW in comparison to other congeneric species like Spodoptera cosmioides (Walker), Spodoptera eridania (Stoll), Spodoptera albula (Walker) and Spodoptera dolichos (Fabricius) (Montezano et al., Reference Montezano, Specht and Bbarros2014; Specht and Roque-Specht, Reference Specht and Roque-Specht2016) has entitled it to the distinction of an invasive species. Although FAW larvae have a decided preference for grasses such as maize and sorghum (its main hosts), various other crops including weeds are also attacked. Spodoptera frugiperda has been reported to feed in large numbers on the leaves, stems and reproductive parts of Solanum lycopersicum Mill. (Tietz, Reference Tietz1972), Capsicum annum L. (Casmuz et al., Reference Casmuz, Juarez, Socias, Murua, Prieto, Medina and Gastaminza2010), Brassica oleracea var. capitata L., Zingiber officinale Roscoe, Citrus sinensis L. Osbeck, Prunus persica L. Batsch, Fragaria ananassa Duchesne, Abelmoschus esculentus L. Moench, Solanum tuberosum L. etc. (Rwomushana, Reference Rwomushana2019). The potential of FAW to sustain on both crop and non-crop plants including weeds enables it to maintain the population year-round (Montezano et al., Reference Montezano, Specht, Sosa-Gomez, Roque-Specht, Sousa-Silva, Paula-Moraes, Peterson and Hunt2018).
India is a tropical country that favours rapid reproduction and multiplication of FAW. The peak activity period of FAW is from July to September in India, thus becoming a major threat to the Kharif maize crop. To escape excess rainfalls and higher incidence of insects in Kharif season, maize is also cultivated in Rabi season in different parts of the country. However, various studies have reported cold hardiness in stages of FAW resulting in damage to winter crops which in turn can empower FAW to sustain throughout the year (Zhang et al., Reference Zhang, Zhao, Wu, Li and Wu2021; Vatanparast and Park, Reference Vatanparast and Park2022; Qi et al., Reference Qi, Hong, Chen and Liang2024). Consequently, when Kharif maize is absent, FAW being a polyphagous pest may shift to crops in succession after Kharif maize or to other inter-crops. Maize–pea intercropping is widely practiced worldwide including India, due to the complementary use of N sources by intercropping with legumes (Aulakh, Reference Aulakh2020). However, information on the host susceptibility of S. frugiperda to companion plants like pea in the intercropping system and crops grown in succession is lacking. Such knowledge is requisite to assess the biotic potential of S. frugiperda on different crops at risk. Life tables provide comprehensive information on the insect population dynamics and their fitness by including all life-history parameters and reproduction of both sexes (Huang et al., Reference Huang, Chi and Smith2017; Chen et al., Reference Chen, Guo, Gao, He, Bai, Zhang and Wang2020). In this study, we assessed the life table data of FAW reared on pea and analysed the population fitness. Our research aimed to provide comprehensive knowledge about the FAW population growth and possible damage to pea with the objective of providing helpful information for the application of fruitful FAW management tactics in the newly FAW-invaded agricultural ecosystems.
Materials and methods
Insect
FAW larvae were field-collected in Experimental Farm, Department of Entomology Dr YS Parmar University and Forestry, Nauni, Solan, Himachal Pradesh, India (1275 m amsl; 31.28oN; 76.94oE), and reared in the laboratory at 25 ± 0.5°C, 70 ± 5% RH and 14L:10D photoperiod. The pest was raised on the respective host for one generation before being used in the experiments.
Host plant raising
Maize (Zea mays L. var. Early Composite) and pea (Pisum sativum var. sativum L. var. Azad P-1) plants were grown as per the standard package of practices at the experimental farm of the Department of Entomology. Due to the different growth cycles of plant species, 25-day-old maize and 35-day-old pea leaves were used to feed S. frugiperda larvae.
Larval feeding trials
The trials were performed in Biological Control Research Laboratory of the Department of Entomology, Dr YS Parmar University and Forestry, Nauni, Solan, Himachal Pradesh, India at 25 ± 0.5°C, 70 ± 5% RH and 14L:10D photoperiod. Newly emerged adults obtained from mass culture were paired and placed in separate plastic cylindrical containers covered with nylon mesh on one side (150 × 150). Ten egg masses (one from each container) laid on host leaves within 24 h period were randomly selected. Ten eggs were then randomly picked from each egg mass. The neonate larvae hatched from selected 100 eggs were reared individually on the test host plants in Petri plates (100 mm). Petri plates with fresh leaves were changed daily to ensure sufficient food for larvae. The larval development and survival were recorded until death, pupation or pupal emergence. Newly eclosed adults were kept in pairs in plastic cylindrical containers (1L) covered on one side with nylon mesh (150 × 150). All adults were fed daily with 30% (v/v) honey solution in cotton swabs. FAW adults that mated successfully included 20 pairs that were fed with maize, and 14 pairs that were fed with pea. Each pair was offered with host leaves as a substrate for oviposition. Observations on the duration of different developmental stages, adult longevity, pre-oviposition and oviposition periods, fecundity and sex ratio were recorded.
Life table analysis
Life tables of S. frugiperda reared on maize and pea leaves were constructed and analysed based on the age-stage, two-sex life table theory using the TWOSEX-MSChart program (Chi, Reference Chi2022b).
The age-stage survival rate (sxj, probability that a newly laid egg can survive to age x and stage j) and age-stage specific fecundity (fxj, number of eggs produced by female adult at age x) were computed. These parameters accurately illustrate the biological characteristics of S. frugiperda. The age-specific survival rate (lx) and age-specific fecundity (mx) were calculated as:
where m is the number of stages.
The gross reproductive rate (GRR) was calculated as:
The net reproductive rate (R 0), defined as the rate of multiplication of the population in a generation, represented in terms of number of offspring produced per generation was calculated as summation of the product of lx and mx, i.e.
The true intrinsic rate of increase (r) is the number of offspring produced by an individual in a day (offspring per individual per day) and was calculated by using the Lotka–Euler equation:
The mean generation time (T) is defined as the time period required by a population to increase to R 0-fold of its size as time approaches infinity and population settles down to a stable age-stage distribution and was calculated by:
The finite rate of increase (λ) is the rate of multiplication of population in a day (times per day) and was calculated as:
The doubling time (DT), the time required by a population to double its size, was calculated by the formula:
Age-stage-specific life expectancy (exj) is the time that an individual of age x and stage j is predicted to live. It was calculated by the formula:
where, s'iy = probability that an individual of age x and stage j can survive to age i and stage y assuming s'xj = 1.
Age-specific reproductive value (vxj), the contribution of an individual of age x and stage j to the future population, was calculated by the formula:
The life table parameters for the two host treatments were estimated using the bootstrap technique with 100,000 resampled data for calculating the means and standard error of population parameters. The differences in population parameters, development duration and reproductive values among host plants were compared using the paired bootstrap test in the program of TWOSEX-MSChart (P < 0.05).
Population projection of Spodoptera frugiperda
The life table data for S. frugiperda reared on maize and pea were used to project the population growth and its uncertainty to elucidate the predicted population size using the computer program TIMING-MSChart (Chi, Reference Chi2022a). The population growth for 200 days was projected for an initial population of ten eggs. The results of the 100,000 bootstrap sampling of the intrinsic rate of increase (r) obtained in the previous section were sorted to find the 2.5th and 97.5th percentiles of the sorted bootstrap samples. We then utilised the bootstrap life table samples that generated the 2.5th and 97.5th percentiles of the intrinsic rate of increase (r) to project the population growth. The results indicate the confidence interval of the population.
Results
Developmental biology, reproduction and life table of Spodoptera frugiperda
Spodoptera frugiperda successfully completed its life cycle by feeding on pea leaves. The developmental duration of each larval instar, prepupal and pupal stage of S. frugiperda fed on pea leaves was significantly longer than that on maize leaves (table 1). The female longevity, male longevity and adult preoviposition period (APOP) were significantly higher on maize than on pea. The mean fecundity of S. frugiperda on maize (1265.58 eggs per female) and pea (710.84 eggs per female) was significantly different (table 2). The survival rate from egg stage to adult female and male was 33 and 20% on maize, and 19 and 14% on pea, with a sex ratio of 1.65:1 and 1.36:1, respectively (table 2; fig. 1).
Developmental biology of Spodoptera frugiperda on maize and pea
Means in the row with different alphabetical superscript differ significantly by the paired bootstrap test (P < 0.05).
Population growth parameters of Spodoptera frugiperda on maize and pea
Means in the row with different alphabetical superscript differ significantly by the paired bootstrap test (P < 0.05).
Age-stage-specific survival rate (sxj) of the Spodoptera frugiperda reared on maize and pea.
The age-stage-specific survival rate (sxj) of S. frugiperda is shown in fig. 1. Due to the variation in developmental rates among individuals as well as between sexes, there was overlapping between different stages. The survival rate of the sixth larval instar and pupa was much higher on maize (61 and 57%, respectively) than on pea (45 and 39%, respectively). The number of eggs laid by adult female at age x is shown as fx in fig. 2. The fx of S. frugiperda fed on maize and pea increased initially before declining, and peaked on the 31st and 41st days, respectively. The curve of lx is a simplified version of the curves of sxj. The lx curve of S. frugiperda fed on maize significantly decreased from 35th day, and its survival rate decreased to zero by 43rd day, whereas the age-specific survival rate of S. frugiperda fed on pea leaves dropped rapidly from 42nd day, and by 48th day, it had dropped to zero (fig. 2).
Age-specific survival rate (lx), female age-specific fecundity (fx), age-specific fecundity of the total population (mx) and age-specific maternity (lxmx) of the Spodoptera frugiperda reared on maize and pea.
The age-stage-specific life expectancy (exj) explains the future expected life duration of an individual of age x and stage j (fig. 3). The life expectancies of newly laid eggs (e 01) were 25.01 and 23.04 days on maize and pea, respectively. The exj of adult females fell from 15.70 on maize to 11.11 days on pea, while the maximum exj of adult males, 15.74 days, was observed on maize, but decreased to 10.21 days on pea (fig. 3).
Age-stage-specific life expectancy (exj) of the Spodoptera frugiperda reared on maize and pea.
The reproductive value (vxj) shows the contribution of an individual of age x and stage j to the future population (fig. 4). After the emergence of adult females of S. frugiperda at 23 and 34 days on maize and pea, the vxj jumped to 280.79 and 330.06 eggs, respectively, while the peak vxj occurred at 29 days (728.41 eggs) and 38 days (514.88 eggs) on maize and pea, respectively. The duration of vxj of female adults was 16 days on maize whereas it was 12 days on pea (fig. 4).
Age-stage-specific reproductive value (vxj) of the Spodoptera frugiperda reared on maize and pea.
Population parameters of Spodoptera frugiperda
The population growth parameters of S. frugiperda were significantly influenced by the host plant. The net reproductive rate (R 0) of FAW reared on maize (417.64 offspring per individual) was significantly higher than that of FAW reared on pea (135.06 offspring per individual). Feeding on maize achieved higher values of intrinsic rate of increase (r), finite rate of increase (λ) than feeding on pea (table 2). Since the r and λ values on both crops were greater than 0 and 1, respectively, it implies that S. frugiperda can successfully sustain its population both on maize and pea. The λ values of the pea-fed populations and maize-fed populations of S. frugiperda indicate that the two populations grew continuously and geometrically at the rates of 1.13- and 1.21-fold per day, respectively. Contrarily, the mean generation time (T) of pea-fed populations (41.5 days) was 1.29 times that of maize-fed populations (31.14 days). The doubling time (DT) was significantly longer when FAW was fed on pea, while the gross reproductive rate (GRR) was significantly higher on maize (799.48 offspring per individual) than pea (455.2 offspring per individual) (table 2).
Population projection of Spodoptera frugiperda
The population projection showed that S. frugiperda reared on maize would grow faster than on pea (fig. 5). In the simulation period of 200 days, the total population size on log scale was higher on maize (16.53), than on pea (9.96). Beginning with ten eggs, the population fed on maize was expected to go through six generations, while five generations on pea. As the age-stage, two-sex life table can express the stage differentiation; the development of each life stage can be noticed (fig. 6). Figure 7 describes the growth and dynamics of each life stage of S. frugiperda in a logarithmic scale. The positive rate demonstrates an increase of a stage from time t to t + 1, and the negative rate indicates a decrease in stage size. The intrinsic rate of increase (r) displays the multiplication potential of a population under ideal conditions when the population approaches stable age-stage distribution. The curves of the stage-specific growth rates of S. frugiperda raised on maize leaves approached the intrinsic rate of increase in 200 days. Alternatively, the population growths of S. frugiperda on maize and pea were highly uncertain; this could be attributed to variations in developmental speed and fertility among individuals. The variability of population growth was projected by using life tables from the 2.5th and 97.5th percentiles of the intrinsic rate of increase (fig. 5).
Total population size of the Spodoptera frugiperda projected by using life tables of 0.975 and 0.025 percentiles of intrinsic rate on increase (r) on maize and pea with an initial population of ten eggs.
Population projection of Spodoptera frugiperda reared on maize and pea with an initial population of ten eggs.
Stage growth rate of Spodoptera frugiperda reared on maize and pea with an initial population of ten eggs.
Discussion
Nutrition has a major role in the development of insect herbivores, and the resources acquired during development translate to resource allocation among key life history traits throughout an individual's life (Nestel et al., Reference Nestel, Papadopoulos, Pascacio-Villafan, Righini, Altuzar-Molina and Aluja2016). Larval-derived dietary reserves are crucial in affecting insects’ adult fitness (Salgado and Saastamoinen, Reference Salgado and Saastamoinen2019). Because of the diversified range of hosts, many pests including FAW are successfully flourishing not only during the crop development period but also over the off-season (Moraes et al., Reference Moraes, Ferreira Da Silva, Leite, Karam and Mendes2020). As FAW has been reported to damage a variety of plants, only certain plant species can support its complete development, e.g. maize, sorghum, sugarcane, potato, cotton etc. (Barros et al., Reference Barros, Torres, Ruberson and Oliveira2010; Maruthadurai and Ramesh, Reference Maruthadurai and Ramesh2020; Zhou et al., Reference Zhou, Qin, Wang, Zheng and Lu2022) while other plant species may not support complete development of S. frugiperda but may still be utilised by larvae or adults for feeding and oviposition, e.g. cabbage, eggplant and Coix (Liu et al., Reference Liu, Wang and Zhong2019; Zou and Yang, Reference Zou and Yang2019; Zhou et al., Reference Zhou, Li, Su, Wang, Zheng and Lu2020). The results of the present study revealed that S. frugiperda can complete its life cycle on pea, suggesting that pea is an alternative host plant for this insect.
The longer developmental duration, higher survival rate, higher fecundity and other population growth parameters of FAW on maize observed in the present study suggest that maize is a highly susceptible host plant compared to pea. However, the biotic potential of S. frugiperda noted on pea in the present study corroborates with previous studies carried out on its favoured hosts. For instance, the larval duration of FAW reared on pea leaves (20.36 days) is similar to that reported when reared on sorghum (19.4 days), soybean (16.65 days), tomato (21.23 days) and cotton (22.81 days) (Wang et al., Reference Wang, He, Zhang, Liu, Jing and Zhang2020; He et al., Reference He, Wang, Chen, Ge, Wyckhuys and Wu2021; Li-hong et al., Reference Li-Hong, Cao, Gui-Yun, Xi-Bin, Zhi-Yan, Hong and Chao-Xing2021). This varying offspring performance of FAW can be due to the differences in larval food utilisation efficiency. El-Shennawy et al. (Reference El-Shennawy, Sabra and Kandil2022) also recorded a low larval mortality, high growth rate and fast development time of FAW when reared on pea indicating that nutritional contents of pea are suitable for its growth and development. The female adult longevity of S. frugiperda in the present study is 9.79 days on pea which is comparable with that reported when raised on soybean (9.33 days) (Wang et al., Reference Wang, He, Zhang, Liu, Jing and Zhang2020). Certainly, differences in the type of food ingested have a major impact on the development of herbivorous insect larvae and on the reproduction of adults even under the similar conditions, which in turn governs the change trend of the entire insect population. When reared on pea leaves, FAW females started oviposition after 4 days of emergence and continued to oviposit for 3.95 days. However, Wang et al. (Reference Wang, He, Zhang, Liu, Jing and Zhang2020) reported an APOP of 2.89 days and 7.22 oviposition days when reared on maize. The fecundity of S. frugiperda reared on pea in the present study was 710.84 eggs per female which is in accordance with that reported when fed with maize leaves (955.62 eggs per female), rice leaves (590.77 eggs per female) (Acharya et al., Reference Acharya, Malekera, Dhungana, Sharma and Lee2022) and cotton leaves (803.51 eggs per female) (Wang et al., Reference Wang, He, Zhang, Liu, Jing and Zhang2020). Similarly, El-Shennawy et al. (Reference El-Shennawy, Sabra and Kandil2022) reported a fecundity of 880.67 eggs per female when reared on pea. The population growth parameters of S. frugiperda recorded in pea are similar to the previous studies, on its preferred hosts. The net reproductive rate of FAW on maize was recorded to be 134.43 offspring per individual (He et al., Reference He, Wang, Chen, Ge, Wyckhuys and Wu2021), 114.59 offspring per individual, 172.23 offspring per individual at 20 and 25°C, respectively (Chen et al., Reference Chen, Chen, Yang and Liu2022), which are in line with the present study (135.06 offspring per individual). The r and λ of the FAW in the current study were greater than 0 and 1, respectively, which indicates that pea could also be a potential host crop for this pest.
Population projections drawn on the basis of life table rates display the stage structure and damage potential of a pest population. As intercropping maize with legumes including pea is a common practice, when egg masses are laid by S. frugiperda on maize, their offspring can transfer to adjacent legume fields. Although the early larval development of FAW occurs on maize, later instars are capable of moving to legume fields after attacking maize. Furthermore, the damage to peas in a maize/pea intercropping system may be more severe than that in single cropping systems of peas, as per the observations of damage in a sugarcane–maize intercropping system (Tai et al., Reference Tai, Guo, Yang, Zhang, Liu, Yang, Song, Xia, He, Lin and Wang2019). Davidson-Lowe et al. (Reference Davidson-Lowe, Ray, Murrell, Kaye and Ali2021) studied the performance and behaviour of FAW larvae on maize grown after different cover crops including pea. FAW larvae oriented more frequently towards maize plants grown in soil after radish and pea cover crops and had 90.4% higher weight when fed on maize grown after pea than triticale. Additionally, the emission of volatile organic compounds and total soil inorganic nitrogen was highest in maize plants grown after pea; resulting in attraction of FAW larvae to maize plants grown after pea. Various other studies have also shown the positive correlation between nitrogen availability and volatile terpene emissions leading to increased herbivore attractiveness to plants grown under increased nitrogen availability (Ormeño et al., Reference Ormeño, Goldstein and Niinemets2011; Ormeño and Fernandez, Reference Ormeño and Fernandez2012).
In India, Rabi maize has emerged as an important crop in the non-traditional areas widely planted in October–November, and pea is also planted in October–December as sole or inter-crop, resulting in an overlap of these crops. Moreover, many other suitable host plants, e.g. soybean, sorghum, rice, vegetable crops, etc., are commonly grown in India all year round. The presence of these alternate hosts could be the reason for S. frugiperda outbreaks occurring annually in maize fields. Assessing the impact of different host plant species on the bio-ecology of insect pests is critical for their management. The high population growth potential of S. frugiperda on pea observed in this study showed the suitability of this pest in sustaining FAW population. As shown in the present study, life table studies provide the most extensive understanding of the stage differentiation, reproduction and survival of pest populations. These findings provide a strong scientific foundation for formulating an effective and timely integrated pest management programme for managing S. frugiperda.
Data availability
The datasets created during and/or examined during the current study are available from the corresponding author on reasonable request.
Author contributions
Shubham Sharma: writing, investigation and methodology; Prem Lal Sharma: supervision and editing; Prajjval Sharma: investigation, writing – review and data analysis; Subhash Chander Verma: supervision and editing; Nidhi Sharma: supervision and formal analysis; Priyanka Sharma: formal analysis. All authors have read and approved the final manuscript.
Financial support
Not applicable.
Competing interests
The authors declare that they have no conflict of interest.
Ethics approval and consent to participate
This research did not involve any human participants and/or animals, other than the Spodoptera frugiperda.
