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The repository of biocontrol agents for Spodoptera frugiperda (Smith, 1797) with emphasis on their mode of action
The Journal of Basic and Applied Zoology volume 85, Article number: 18 (2024)
Abstract
Background
Spodoptera frugiperda (Smith, 1797) is one of the most destructive pests of Maize plants, causing an estimated 40% crop loss in 2019. It is a native pest of America and difficult to control since it has developed resistance against most insecticides efficient in controlling lepidopteran pests, including recommended Chlorantraniliprole and Flubendiamide. Due to the increasing need for a change in pest management methods, it is necessary to consider biological control on a commercial level.
Main body
In this review, we have put together a list of all the biocontrol agents (parasites, parasitoids, predators, viruses, bacteria, and fungi) reported from different parts of the world effective in managing the impact of S. frugiperda, along with an elaborate mechanism of action of each natural killer. After analyzing the procured data, Pareto charts were prepared plotting the distribution of the mortality of S. frugiperda caused by parasitoids and pathogens. The regional abundance was plotted in the form of graph.
Conclusion
Pareto’s charts (Fig. 6) shows that Telenomus remus and Steinernema riobrave accounts for a maximum of 90% mortality of S. frugiperda among other high contributors (Chelonus insularis, Trichospilus pupivora, Ophion flavidus, Heterorhabditis indica, Heterorhabditis bacteriophora, Trichogramma mwanai). NPV and Metarhizium anisopliae were proved to be the most effective micro-entomopathogens causing up to 98% mortality. Also, these entomopathogens were reported all over the world but found abundant in Mexico and India. Based on this study, we recommend the augmentation of entomopathogenic insects on a large scale only to commercialize them in the market and produce different ready-to-use pathogenic formulations to be applied in the fields combined with a significantly less quantity of harmful chemical ailments.
Background
Spodoptera frugiperda belongs to the family Noctuidae of the order Lepidoptera. It is one of the most invasive and destructive pest species found globally. It is best known to cause irreversible damage to over 353 plant species, especially rice and maize crops (Montezano et al., 2018; CABI, 2020). S. frugiperda (Smith, 1797) (Lepidoptera: Noctuidae) is commonly found in the tropical and subtropical region of the USA (CABI, 2020). In Asia, the first occurrence of S. frugiperda was reported in Karnataka, India, in 2018, during a massive pest infestation that has caused severe damage to the maize crops (Manupriya, 2019). The infestation further spread to the multiple states of India, including the Northeastern part of the country (Firake et al., 2019). In North-East states of India, including Mizoram, Tripura, Nagaland, Meghalaya, Manipur, Sikkim, and Arunachal Pradesh, the S. frugiperda outbreak was reported during the period of March–May 2019 (Firake et al., 2019). Concurrently, S. frugiperda infestation invaded the neighboring countries of India, and its occurrence has been cited in China, Bangladesh, Indonesia, Japan, Korea, Republic of Laos, Malaysia, Myanmar, Nepal, Sri Lanka, Thailand, Vietnam, and Yemen (CABI, 2020). S. frugiperda was first reported in Shimoga, Karnataka, India, in mid-July 2018 and then spread quickly to Tamil Nadu, Telangana, Andhra Pradesh, West Bengal, and Maharashtra. It attacks not only maize but also sugarcane in Maharashtra (Deshmukh et al., 2020). Soon afterward, it was migrated to Bangladesh, Nepal, Sri Lanka, and Myanmar (Deshmukh et al., 2020). In China, S. frugiperda was first reported in Yunnan, China, in January 2019. Sugarcane is one of the preferred plant species of S. frugiperda (Montezano et al., 2018). It was found that S. frugiperda migrated to sugarcane fields in Gencun, Wuxuan (23° 590 E, 109° 660 N), Guangxi, on May 10, 2019. The larvae were hidden inside the unexpanded top leaves. There was an inverted ‘Y’ shape mark on the head and four black flecks arranged in a square on the back of the last somite of the abdomen. It cowered and even pretended to be in thanatosis if disturbed.
The North-East belt of India is a significant biodiversity hotspot and a transition zone between the Indian, Indo-Burma-Malaysian, and Indo-Chinese regions. It is ecologically represented by the Eastern Himalayan biome and is exceptionally rich in endemic flora and fauna. The Indian government is promoting this region for organic farming because of its distinct climatic and geographic conditions, high flora and fauna diversity, and traditional practices of native farmers who use fewer synthetic agrochemicals. Since maize is the second most important cereal crop in northeast India, next to rice, it is grown mainly by small landholding organic farmers in rainfed hilly upland conditions (Ansari et al., 2015). Severe infestation by the S. frugiperda wreaks havoc for maize farmers. Generally, native natural enemies of related existing pest species are the first defense against invasive pest species in such conditions. Invasion of an alien pest species poses a significant challenge after the failure of the existing natural enemies to combat the foreign pest, which may force farmers to use chemical pesticides. Chemical pesticides are known for their effective results but are way more dangerous and poisonous to non-target species, including humans. The mortality caused by native natural enemies is one of the first steps in developing a comprehensive management program for an invasive insect pest. The establishment of an invasive species outside its natural range represents a threat to the ecological balance (Molnar et al., 2008).
S. frugiperda has become a nightmare for central and western Africa since its epidemic in 2016 (Goergen et al., 2016). It may have several generations per year, and the moth can fly up to 100 km per night. Its larvae feeds on various plants’ leaves, stems, and reproductive parts and attacks 353 agriculturally important plant species, mainly Poaceae, Asteraceae, and Fabaceae. Due to the peculiarities of polyphagia, strong adaptability, feeding voracity, periodic outbreaks, and migration ability, it is not easy to control (Montezano et al., 2018, Westbrook et al., 2016). It has been known that S. frugiperda has two races, a ‘rice strain’ and a ‘corn strain.’ Rice strain preferentially feeds on rice and various pasture grasses, whereas corn strain feeds on maize, cotton, and sorghum (Cock et al., 2017).
Main text
The idea of biological control has been used for the management of pests for many years. It is a powerful tool and an essential alternative control measure that provides environmentally safe and sustainable plant protection (Assefa & Ayalew, 2019). It has regained new interest due to the increasing health hazards of persistent chemical pesticides. Most augmentation strategies are directed toward the rearing and releasing of biocontrol agents to the importation and conservation of their kind. Grewal et al. (1997) suggested a reverse order to practice. Following Grewal et al. (1997), surveys have been done to assess the number of biocontrol agents (like parasites, parasitoids, and pathogens) and their pathogenicity toward S. frugiperda. The occurrence and parasitism rate of S. frugiperda pupal and larval parasites and parasitoids varies between localities, plant stages, crop practices, and time. The rate of parasitism is positively affected by cultural methods. This information is needed to assess the potential value of the existing parasitoid fauna in controlling S. frugiperda. In this review, most biocontrol agents found around the globe have been listed, along with their parasitism rate, to ease the process of selecting a better biocontrol agent for its application into the field. The study also includes a future perspective on the direct application of bio-formulations into the field. The bibliographic references for each entry are mentioned in Tables 1, 2 and 3.
Biocontrol agents
Entomopathogenic fungi
The entomopathogenic fungi can affect a broad range of insects with different stadia, causing epizootics due to the spread of external sporulation under suitable conditions, particularly high humidity (Zarkani et al., 2020). The entomopathogenic fungi were found helpful in controlling S. frugiperda are mainly Beauveria bassiana (Balsamo), Vuillemin, Metarhizium anisopliae (Metschn.), and Metarhizium rileyi (Farlow) Kepler, SA Rehner and Humber (formerly in the genus Botrytis, Spicaria, or Nomuraea) (Wraight et al., 2010).
The infection cycle of entomopathogenic fungi, B. bassiana, in invertebrate bodies, was presented by Mascarin and Jaronski (2016). The fungal infection in insects occurs in 4 phases: attachment, germination, penetration, and dissemination. It begins with the recognition and compatibility mechanism of host cuticle cells (Kouassi et al., 2003). During the first phase, conidial spores or blastophores attach themselves to the integument of insects with the help of chemical and electrostatic forces, as explained by Mascarin and Jaronski (2016). Later, they induce epicuticular modifications through mucilage production, leading to conidial germination (Dannon et al., 2020). The second phase begins with forming a germ tube with rehydration and chemical stimuli (Mascarin & Jaronski, 2016). The germ tube then forms a specialized structure called an appressorium, bearing hydrolytic cuticle degrading enzymes, to breach the integument of the host (Kouassi et al., 2003). The appressorium contains enzymes (such as proteases, chitinases, and lipases) that help in penetrating the skin, along with mechanical pressure and other factors (such as oxalate), and reach nutrient-rich medium, the hemolymph (Dannon et al., 2020). The fungus then undergoes a morphological differentiation to colonize the internal organ system and disturb the host immune system. It also secretes toxins during this phase. (Dannon et al., 2020). An antibiotic called Oosporin is used to compete against bacterial infection in insect gut (Kouassi et al., 2003). At this stage, the fungal infection appears as cottony white due to the conidiophores being ready for disease dispersal (Fig. 1).
Four phases of fungal development: a attachment of spores onto the host integument, b germination of conidial spores through formation of germ tube, c penetration penetrating into the integument by hydrolytic enzymes located in the appressorium and d dissemination of conidiospores for dispersal of disease
The entomopathogenic fungi found to infect the S. frugiperda larvae and pupae are listed in Table 1, along with their bibliographic references. The fungi Beauveria bassiana were reported from Mexico, India, and Africa. Different spore concentrations show different results on the population of insects. In laboratory assay, the isolate Bb42 obtained from larvae of S. frugiperda and evaluated against second instar larvae of the same insect resulted in the highest virulence 96.6% of mortality to rate of 1 × 109 spores mL−1, with LC50 of 5.92 × 103 spores mL−1, and lethal time of 3.6 days (Cipriano García et al., 2011). Similar results were obtained in assays, where larvae were sprayed topically and were maintained for 24 h on the treated substrate at 100% relative humidity. The 6-day experiment at 25 °C showed a median lethal concentration (LC50s) of 1213 conidia/mm2, and the application of 4234 conidia/mm2 caused mortality of 96% (Wraight et al., 2010). Metarhizium anisopliae ICIPE 78, ICIPE 40, and ICIPE 20 caused egg mortalities of 87.0%, 83.0%, and 79.5%, respectively, and M. anisopliae ICIPE 41 and ICIPE 7 outperformed all the others by causing 96.5% and 93.7% mortality to the neonate larvae, respectively. The cumulated mortality of eggs and neonates was highest with M. anisopliae ICIPE 41 (97.5%), followed by M. anisopliae ICIPE 7, 655, 40, 20, and 78 with total mortality of 96.0%, 95.0%, 93.5%, 93.0%, and 92.0%, respectively. The isolates with high cumulated mortality ≥ 92% would serve as candidates for the development of biopesticides for the management of S. frugiperda in Africa. Particularly ICIPE 78 and 7 are already commercialized for the spider, mites, and ticks control, respectively, only if further evidence of their efficacy is obtained in the field (Akutse et al., 2019). M. rileyi showed a different mortality rate in S. frugiperda, ranging from 0.75 to 8.6% due to the change in environmental conditions from country to country.
Entomopathogenic virus
A viable alternative for the control of S. frugiperda is represented by the entomopathogenic viruses, especially a family of Baculovirus (Baculoviridae). Baculovirus has the most attention for the development of pest control agents, predominantly due to their intrinsic safety to humans and other non-target organisms as well as their high pathogenicity to susceptible insects (Jones, 2000).
The baculoviruses are distributed and included in four genera: Alphabaculovirus (lepidopteran-specific Nucleopolyhedrovirus (NPV), Betabaculovirus (lepidopteran-specific Granuloviruses), Deltabaculovirus (dipteran-specific NPV), and Gammabaculovirus (hymenopteran-specific NPV) (Jehle et al., 2006; Jiang et al., 2018; Wan et al., 2019; Zamora et al., 2017). The geographical origin of the virus and the target pest also decide the effectiveness of the baculovirus. It is highly effective against the target pest from the same region (Barrera et al., 2011).
Pathogenic mechanisms of the viral disease include (1) Implantation of the virus at the portal of entry, (2) Local replication, (3) Spread to target organs (disease sites), and (4) Spread to sites of shedding of virus into the environment (Coen, 1994). The virus takes its entry into the insect body either orally or transovarially (through spiracle) or via parasitism (Paschke & Summers, 1975). Most susceptible to infections are the larvae of insects (Granados, 1980). The virus enters the body through the midgut and spreads all over the body. The foregut and hindgut are of ectodermal origin and are lined with cuticles, which provides a formidable barrier to invade for viruses (Paschke & Summers, 1975). Two groups of baculovirus, i.e., nucleopolyhedroviruses (NPVs) and granuloviruses (GVs), are infectious to the insects. The NPVs differ from GVs in having occlusion bodies (OB) bearing multiple virus particles, whereas GVs only have single virus particles (Cory, 2000). Upon attachment with the midgut epithelium, the enveloped nucleocapsids were released from the OBs by dissolving the protein matrix adjacent to the virion (Granados, 1980). This dissolution gradually spread outward. Inside the midgut, the occlusion bodies release the virions, which further degrades into the virus envelopes and capsids. The infectious nature of these subviral components was reported by Summers and Paschke (1970). Granados (1980) found that the primary mode of GVs attachment is membrane fusion during the entry of non-enveloped capsids. The establishment of attachment allows the virus to invade the host tissues, fat bodies easily by associating themselves with the nuclear pore complex and injecting their DNA complexes into the host nucleus (Granados, 1980). It is the beginning of the eclipse phase (post 6 to 20 h. of infection) (Summers & Paschke, 1970), where the cells are hypertrophic and contain a characteristic virogenic network of stroma which gives rise to nucleocapsids. The nucleus loses its structure and intermingles with the cytoplasmic constituents (Cory, 2000; Summers & Paschke, 1970; Robertson et al., 1974; David, 1978). The larvae climb higher at the canopy before death. This behavior ensures the spread of the virus to healthy insects (Dara, 2013) (Fig. 2).
Pathogenic mechanisms of the viral disease include a Implantation of the virus at the portal of entry, b Local replication, c Spread to target organs (disease sites), and d Spread to sites of shedding of virus into the environment
In an experiment, three (SfCH15, SfCH18, and SfCH32) out of the eight tested isolates of native NPVs caused ˃98% mortalities at 168-h post-inoculation (hpi) with a dose of 9.2 × 104 OBs/larvae (Ordóñez-García et al., 2020). It accounts for the highest mortality recorded in the entomopathogenic virus (refer to Table 1). Several baculovirus formulations such as Madex™ are recommended for moths, mostly Oriental fruit moth, and Cyd-X™, efficient for codling moth management (Arthurs & Lacey, 2004; Arthurs et al., 2005). Also, some NPV formulations such as Gemstar™ for Heliothis zea NPV and Spod-X™ for beet armyworm NPV were recommended (Arthurs et al., 2005). Furthermore, Certis has a registered celery looper (Syngrapha falcifera) NPV and an alfalfa looper (Autographa californica) NPV (EPA, 2006).
Entomopathogenic bacteria
Bacteria are commonly being used as microbial pesticides nowadays. The commercial release of transgenic plants opened the world toward the insecticidal properties of Bacillus thuringiensis (Bt) proteins (Céleres, 2016). The introduction of Bt transgenic plants like maize, cotton, brinjal, corn, etc., has revolutionized the concept of biological pesticides (Burtet et al., 2017). The bacteria secrete Cry proteins that are toxic to insects. The Bt plants produce the same proteins (Fig. 3).
The Bt toxins enters the insect body through oral ingestion. The solubilized crystals release protoxins which forms active proteins. The active proteins bind to their specific receptors to mediate their entry into the peritrophic membrane which leads to destruction of microvilli. Due to which the insect stops feeding leading to its death
Various bacterial subspecies like Bacillus, Pseudomonas, etc., have been considered biopesticides and are primarily used to control pests and insect-borne plant diseases. The most significant one among these is B. thuriengiensis. Crystalline proteins are produced by the bacteria, which kill specific target species like lepidopteran pests. The target is determined by the binding of Bt crystals to the insect gut (Kumar, 2012). The moment insects ingest the Bt plant, and it shows symptoms like alteration in nutrient absorption, degenerative transformation, appetite loss and abandonment of food, gut paralysis, physiological disorder, all leading to complete paralysis (Monnerat and Bravo, 2000).
The chewing mouthparts in caterpillars promote the ingestion of Bt toxins both in a product and toxin-containing GMP form. Some histopathological studies have studied the interaction between the midgut and Bt toxins (Bravo et al., 1992; Knaak & Fiuza, 2005; Knaak et al., 2010; Knaak et al., 2012). After ingesting, the crystals get solubilized in the alkaline midgut (pH 9–12) (Knowles, 1994). The Lepidoptera-specific Cry proteins are soluble at a pH of more than 9.5 (Knowles & Dow, 1993). The pH of the midgut plays a vital role in the activity of Cry toxins. Cry II1A are activated under alkaline conditions while Cry1b function in neutral to acidic pH (Bravo et al., 2007). The toxins solubilize to release protoxins through the action of proteases, which results in the formation of active proteins weighing around 60–70 kDa (Bravo et al., 2005). The digestive enzymes further act upon these protoxins. After their activation, they bind to their specific receptors located in the microvilli of the apical membrane of the columnar cells of the gut epithelium, which determines the specificity of the Cry toxins (Jurat‐Fuentes & Adang, 2004). Cadherins are the unique molecules that bind to the Cry proteins. These are the aminopeptidases anchored to a glycosyl phosphatidyl inositol (GPI) and a 270 kDa glycoconjugate (Bravo et al., 2007; Gómez et al., 2007). Some studies showed that the toxicity of Cry proteins might be related to the G-protein mediated apoptosis (Zhang et al., 2006). The binding of Cry proteins to their receptors facilitates the opening or pore formation and hence mediates their entry into the peritrophic membrane. At this time, the osmotic imbalance between the extracellular and intracellular environments causes vacuolation of cytoplasm and, subsequently, disruption of cells. Due to the destruction of microvilli, the insect stops feeding, leading to its death (Fiuza, 2004; Bravo et al., 2007; Knaak et al., 2010; Oestergaard et al., 2007; Sousa et al., 2010; Fig. 1).
Zhang et al. (2006) reported that Cry1Ab toxin produced by the Bt kills insects by activating an Mg2+-dependent cytotoxic event after binding to its specific receptor BT-R1. The toxin binding stimulates the G-protein (Gαs) and adenylyl cyclase, thereby increasing cAMP levels, which activates protein kinase A (PKA). The induction of the PKA pathway causes sequential cytological changes that include membrane blebbing, the appearance of ghost nuclei, cell swelling, and lysis.
Some scientists have reported the resistance of S. frugiperda to Bt maize. Horikoshi et al. (2016) discovered that resistance of S. frugiperda had been characterized by some Cry and Vip3A proteins. He evaluated the dominance of resistance genes through the survival rate of neonates from selected Bt-resistant maize and cotton varieties. The strains found highly resistant to proteins Cry1F (HX-R), Cry1.105/Cry2Ab (VT-R), and Cry1A.105/Cry1F (PW-R) were Herculex, YieldGard VT PRO, and PowerCore maize. The same results were found with Vip3A-resistant strain (Vip-R). The heterozygotes from HX-R × Sus and VT-R × Sus, PW-R × Sus, and Vip-R × Sus had absolute mortality. Muraro et al. (2020) observed a 24.8% increase in the mortality of S. frugiperda resistant, heterozygous, susceptible strains in the laboratory. In the field against natural infestations of S. frugiperda, Bt maize with a seed treatment had ~ 30% less S. frugiperda damage than non-Bt maize with the same seed treatment at 7 and 14 DAE (Table 1).
Entomopathogenic nematodes
These are non-segmented, soft-bodied obligatory or facultative parasites belonging to the order Nematoda. The nematodes are used nowadays to control pest insects in agricultural practices and can be supervised with cover crops, crop rotation, and internalization of organic material into the soil (McSorely, 1999). The entomopathogenic nematodes kill the insects within 48 h by impinging the insects through the expulsion of pathogenic bacteria. (Thangavel & Sridevi, 2015). Sometimes the nematodes infect the host body by laying the foundation for infective juveniles, which survive on the host nutrition medium (Anthony, 1985). As soon as the host dies, the infectious stage of nematode grows into the adult and hence develops a modern generation of infective juveniles (IJ). EPNs are commonly used to protect plants from severe pests and some pest-borne diseases (Peters, 1996). The insect infecting nematodes are commercially used as aqueous suspensions and may also be applied in infected insect cadavers, but this may entail problems in storage and ease of handling (ShapiroIlan et al., 2001).
The 3rd stage infectious juvenile initiates the parasitic cycle. They infect suitable hosts by entering through the natural body openings of the host like mouth, anus, and spiracles (Grewal et al., 1997). After entering the host body, these IJs infect the hemocoel and release the symbiotic bacteria into the host body system. The host dies of septicemia within the time span of about 24–48 h (Thangavel & Sridevi, 2015). The uptake of nutrients by IJs is processed continuously by the bacteria and hence simultaneously decomposes the host tissues. Almost 2 to 3 nematode generations are complete within the host cadaver (Pomar & Leutenegger, 1968) (Fig. 4).
Infectious juveniles initiate the cycle by entering the host body through natural openings. They infect the hemocoel and release the symbiotic bacteria into the host leading to septicemia and host death. The remaining cycle is completed on host cadaver
An entomopathogenic nematode, Steinernema sp., was found lethal to S. frugiperda species in Texas, causing damage of about 46.1% to the total larval population (Raulston, Pair, Loera, & Cabanillas, 1992). The effect of another nematode, Heterorhabditidae indica, was assessed by Zamora et al. (2017). The entomopathogenic nematodes succeed in infecting 65% of the S. frugiperda population. S. frugiperda adults infested with an ectoparasitic Noctudonema guyanense reduced the longevity of adult male and female insects by 30% and 15%, respectively. The fertility, in this case, was found to be reduced by 20% (Rogers et al., 1993). In a study, four nematode isolates were analyzed, and based on sequencing of the internal transcribed spacer (ITS) region, they were identified as belonging to the species Heterorhabditis indica. However, one isolate showed low similarity to known H. indica strains in the GenBank database, leading to its classification as a new species, named Heterorhabditis alii, and deposited in the National Center for Biotechnology Information (NCBI) under accession no. (OP555450). Additionally, it was registered in ZooBank under LSID (urn:lsid:zoobank.org:act:306F9D57-CC30-4B8E-8B19-4F0E42B08F34). Furthermore, testing its virulence against the fall armyworm (FAW), Spodoptera frugiperda, demonstrated that H. alii was more effective against this destructive insect pest compared to the foreign EPN species Heterorhabditis bacteriophora (HP88) and the local Heterorhabditis indica (Mango 2 isolate) (Shamseldean et al., 2024).
Predators
Predators, feeding on live insects, catch, consume, and kill their prey at once. The enlarged setae are an efficient substitute for teeth and spines in predatory insects. They serve in holding prey insects and are located along the inner margins of the mandible in some insects like larval Nymphidae (Lepidoptera) and Myrmeleontidae (Neuropteran), while in others, similar setae are located on the inner margins of the fore femora adult Lepidoptera and Heteroptera (Winterton, 2009). It has become crucial to promote the abundance and diversity of predator insects for the sake of nature conservation and agroecology. To enhance the practice of natural control and to reduce the misuse of pesticides, it is necessary to enhance the baseline production and augmentation of pest-specific predators into the environment (Booij & Noorlander, 1992).
During the process of feeding, an egg predator would remove its beak and insert it again on a different location in the same egg to ensure uptake of the maximum amount of nutrients. Once feeding has been initiated upon the egg, it is improbable for the predator Orius insidiosus to leave it unfinished and move to other eggs if they were allowed to feed uninterrupted (Isenhour, Layton, & Wiseman, 1990). Moreover, the visual observation of S. frugiperda predations revealed that feeding durations of 30 s or more produced mortality of 100%, whereas when the predators were allowed to feed for 10 s only, the mortality was 75%. Lewis and Nordlund (1980) stressed the importance of utilizing the exotic parasitoid and predator species, their augmentation, and release into the cultural fields as shown in Table 2. Information regarding predation on S. frugiperda pupae has been provided by Pair and Gross (1989). The families contributing to most of the predation activities belong to the order Hemiptera, Hymenoptera, Coleoptera, and Dermaptera. The species diversity index shows high diversity of predators in the various parts of Meghalaya, India.
A very interesting two-way predation has been reported by Hui et. al. (2021) in China. The reported Syrphid larvae of E. corollae preyed upon early 1st and 2nd instar stages of S. frugiperda attacking approximately half the population (2nd instar E. corollae consuming 63.3% and 46.7% of 1st and 2nd instar S. frugiperda) and 3rd instar E. corollae consuming 100% and 80% of the respective stages. It showed that predation rate of E. corolla tends to increase with the aging of the larvae. But the predation was limited to the early stages of prey only. Once the prey reaches 3rd instar, they equally preyed upon the early instar predator species. According to Pair and Gross (1989), the primary mortality factor was predation, averaging 44.7, 37.8, and 95.8%, respectively, during 1983, 1984, and 1985. During his research, earwigs, Labidura riparia (Pallas); non-identified carabid beetles; wireworms, Conoderus sp.; and the imported fire ant, Solenopsis invicta Buren were the predators found either in S. frugiperda pupation tunnels or feeding directly upon pupae. These studies specify that the pupal predators of S. frugiperda are the primary protagonist in regulating the population of S. frugiperda throughout their development process and is the leading cause in reducing the pests by scavenging within their habitats.
Parasites and parasitoids
According to Firake and Behere (2020), the braconid wasp, Chelonus formosanus was the primary parasitoid of S. frugiperda. They also reported parasitizing S. frugiperda in Barbados and Trinidad (Alam, 1978; Yaseen, 1978). It is an egg-larval parasitoid of S. frugiperda, usually parasitizing more than 70% of eggs in each encountered host egg mass (Rao, 1972; Choudhari et al., 1983). Larval koinobiont parasitoids often emerge onto plant surfaces where generalist predators can attack them before or after forming cocoons. The parasitoid wasps are known to parasitize larvae and pupae of many Spodopteran species worldwide (Gupta, 2013). The Hymenoptera, Braconidae, Ichneumonidae, and Trichogrammatidae were the families mainly infesting S. frugiperda (Molina-Ochoa et al., 2003). The role of some egg parasitoids like Telenomus remus was found limited and only evident at the end of spring (Firake & Behere, 2020). The braconid, Chelonus insularis Cresson had a significant level of parasitization on the population of S. frugiperda, causing mortality of about 82.1%, whereas the parasitization by Telenomus remus was found to be 9.7%. T. difficilis increased steadily throughout the first test period (weeks 17–19) and the first half of test period 2 (weeks 22–23). For the remaining season, the proportion of S. frugiperda larvae parasitized by T. difficilis remained relatively constant. Two probable explanations for this pattern are that C. insularis is a better internal competitor, or T. difficilis would not oviposit in host larvae containing developing C. insularis (Ashley, Waddill, Mitchell, & Rye, 1982).
The parasite Trichogramma mwanzai Schulten and Feijen (1991) is a native to Malawi and Kenya (Guang & Oloo, 1990). It was introduced from Kenya to India in 2004 to control Helicoverpa armigera (Hubner) (Jalali et al., 2016). During the study by Elibariki (2020) in Tanzania, the culture of T. mwanzai was found parasitizing 70% of S. frugiperda eggs, indicating that it is an excellent candidate for augmentative biological control.
In a study by Molina-Ochoa et al. (2003), a survey of fields searching for the parasitoid larvae was conducted in six Mexican states during August and September 2000. Out of 5591 larvae of S. frugiperda, a total of 772 larvae were found successfully exhibiting parasitism, accounting for a total of 13.8%. The highest rate of 42.2% parasitism was observed from a single batch of eggs representing three major contributing species: Chelonus insularis Cresson, Pristomerus spinator (F.), and Meteorus laphygmae (Viereck). Pristomerus spinator (F.) displayed the highest rate of 22.2% parasitism, followed by 22.1% parasitism by Meteorus laphygmae (Viereck).
Among Dipterans, Winthemia rufopicta and Eucelatoria rubentis were the two species with the highest parasitism rate. The parasitism of S. frugiperda larvae increases rapidly, reaching 100% toward the first week of September (Tingle et al., 1994) (Table 3).
Conclusions
There are two strains of S. frugiperda known to exist, i.e., rice strain and corn strain. It has been observed throughout this study that the maize strain of S. frugiperda is prevailing all over India. Rice strain prefers rice and various pasture grasses in feed, and the corn strain devours maize, cotton, and sorghum (Cock et al., 2017). S. frugiperda prefers to feed on the sugarcane plant frequently (Montezano et al., 2018). The experiment conducted by Song et al. (2024) inferred that over 62% of sugarcane plants were damaged by S. frugiperda larvae, where around 28 larvae were used against 100 plants and a maximum of two larvae per plant.
A study on the Intrusion of S. frugiperda was carried out by Song (2024) in China. This study emphasizes the course of migration throughout America, Africa, and China, predicting its movement to Southern China and the northeast region. The insect is capable of such large movements due to its strong adaptability and flight ability (Westbrook et al., 2016). Since last year, S. frugiperda has been seen to spread disaster all over India, mainly the northern parts of India. In India, the maize production was about 28.7 million tons, which fell down by 3.2% during March 2019 after the attack of S. frugiperda, and it was expected to decline even further by the end of the year. The condition worsened in the Northern states when the shortage of maize had a cascading effect on the poultry industry, increasing the production cost of chicken and eggs (Manupriya, 2019). Hence, it requires the urgency to monitor the pest extensively.
Spraying chemicals is the most accessible approach practiced by farmers throughout the country, but it is also hazardous. Centre for Agriculture and Bioscience International suggested using Flubendiamide, Emamectin benzoate, Chlorantraniliprole, Spinetoram, Indoxacarb, Lambda-cyhalothrin, and Novaluron for effective control of S. frugiperda in India. On the other hand, research showed that using some of the listed insecticides is futile as S. frugiperda has developed resistance against them. Continuous laboratory studies of S. frugiperda showed 225-fold and 5400-fold resistance against Flubendiamide and Chlorantraniliprole (Boaventura et al., 2020). With increasing insecticidal resistance and its toxic effect on non-target species, it is high time to take safety measures to check the pest population. The protective management of pests includes the implementation of biological control, in addition to cultural and mechanical.
The field management should begin with reduced monoculture and alternate row-plantation of undesired crops with the desired crop. It checks the population of pests to some extent. Also, the use of transgenic seeds should be encouraged among farmers. Studies have reported that the use of transgenic Bt maize reduced the need for insecticide by 47.8% (Brookes and Barfoot, 2017). Our studies presented a list of almost all the biological killers of S. frugiperda found around the globe and their mechanism of action, which could help their execution and future studies. Among predators, 12 species of Hemiptera, five species of Hymenoptera, five species of Dermaptera, and seven species of Coleoptera were found preying on S. frugiperda eggs and larvae along with some Spiders (Table 2). However, most bio-enemies constitute a total of 110 different species belonging to the eggs or larval parasitoids category. A bibliographic representation with references is provided in Table 3. Chelonus sp and Telenomus sp were found to have the highest cumulative toxicity to S. frugiperda than other Genera, while Chelonus insularis alone can infest 82.1% of eggs or larval S. frugiperda population and is ubiquitous (Fig. 6). The performance of fungi Metarhizium anisopliae was found astonishing, controlling 79.5–87% population of pests by itself (Table 1). Of all the pathogens listed in Table 3, NPV was found as a prominent contributor infecting over 92% pest population.
This review serves as a repository of the potential biocontrol agents against S. frugiperda available around the world. As per the findings of this study, the toxicity of each pathogen provided in the table could deliver insight on the production of the ready-to-use biocidal formulation containing the desired concentration of natural pathogens (bacteria, fungus, virus) (Table 1). It will reduce the overuse of chemical pesticides, which causes much severe harm than expected, both to non-target species and humans. The production of the biocidal formulation will open a new field of interest to the manufacturing agencies and factories, which will indeed support the economy of the country and some serious issues like unemployment. The geographical abundance of virus, bacteria, and fungi was analyzed. It is clear from the collected data that these pathogens occur abundantly in Mexico and India (Fig. 5). Furthermore, India was found to inhabit most of the predator species followed by Indonesia. The insect traps are advised to be used around the fields and should be manufactured more or made available to the farmers at a cheaper cost for effective utilization and marketing. The abundance of parasites and parasitoids is shown in Fig. 5. A proper field practice guideline should be established and shared between countries for the proper management of S. frugiperda using these biocontrol agents. These guidelines should be focused on the specific host plant, crop stage, prey stage, and application methods. The application of all these measures the crop yield as a function of prey density, in this case S. frugiperda. Besides this, a biocontrol formulation can be prepared using entomopathogenic fungi, bacteria, and viruses in the form of ready-to-use doses (Fig. 6), which could be applied directly in the fields. The authors believe that the cumulative effect of parasitoids/predators and biocidal formulations will successfully help control S. frugiperda.
Graphical representation of the data from Tables 1, 2 and 3 showing abundance of pathogens in various parts of the world. a Mexico inhabits the highest number of pathogens specific to FAW. b India inhabits the highest number of predators specific to FAW. c Mexico and the USA bearing the highest number of parasites and parasitoids specific to FAW
A Pareto chart plotting the distribution of the mortality of S. frugiperda caused by a parasitoids belonging to orders hymenoptera, diptera, lepidoptera, mermithida, and rhabditida; and b various pathogens (nucleopolyhedrovirus and entomopathogenic fungi) in descending order of frequency, with a cumulative line on a secondary axis as a percentage of the total
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
References
Akutse, K. S., Kimemia, J. W., Ekesi, S., Khamis, F. M., Ombura, O. L., & Subramanian, S. (2019). Ovicidal effects of entomopathogenic fungal isolates on the invasive fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Applied Entomology, 143(6), 626-634.
Alam, M. M. (1978). Attempts at the biological control of major insect pests of maize in Barbados, WI (No. 2019-2017-4349).
Andaló, V., Santos, V., Moreira, G. F., Moreira, C., Freire, M., & Moino, A., Jr. (2012). Movement of Heterorhabditis amazonensis and Steinernema arenarium in search of corn fall armyworm larvae in artificial conditions. Scientia Agricola, 69, 226–230.
Ansari, M. H., Ardakani, M. R., Asadi, R. H., Paknejad, F., & Habibi, D. (2015). Effect of pseudomonas fluorescent strains on soluble sugar, proline and hormonal status of maize (zea mays l.) Under drought stress.
Anshary, A., Edy, N., & Pasaru, F. (2024). Natural Enemy of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Palu Valley, Central Sulawesi. In 2nd international interdisciplinary conference on environmental sciences and sustainable developments 2022 environment and sustainable development (IICESSD-ESD-22) (pp. 75–80). Atlantis Press.
Anthony, S. (1985). Survival of infective juveniles of Heterorhabditis spp., and Steinernema spp. (Nematoda: Rhabditida) at various temperatures and their subsequent infectivity for insects. Revue Nematol, 8(1.2), 16–5.
Arthurs, S. P., & Lacey, L. A. (2004). Field evaluation of commercial formulations of the codling moth granulovirus: Persistence of activity and success of seasonal applications against natural infestations of codling moth in Pacific Northwest apple orchards. Biological Control, 31, 388–397.
Arthurs, S. P., Lacey, L. A., & Fritts, R., Jr. (2005). Optimizing the use of codling moth granulovirus: Effects of application rate and spraying frequency on control of codling moth larvae in Pacific Northwest apple orchards. Journal of Economic Entomology, 98, 1459–1468.
Ashley, T. R., Waddill, V. H., Mitchell, E. R., & Rye, J. (1982). Impact of Native Parasites on the Fall Armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), in South Florida and Release of the Exotic Parasite, Eiphosoma vitticole (Hymenoptera: Ichneumonidae). Environmental Entomology, 11(4), 833–837. https://doi.org/10.1093/ee/11.4.833
Assefa, F., & Ayalew, D. (2019). Status and control measures of fall armyworm (Spodoptera frugiperda) infestations in maize fields in Ethiopia: A review. Cogent Food & Agriculture, 5(1), 1–16. https://doi.org/10.1080/23311932.2019.1641902
Barrera, G., Simón, O., Villamizar, L., Williams, T., & Caballero, P. (2011). Spodoptera frugiperda multiple nucleopolyhedroviruses as a potential biological insecticide: Genetic and phenotypic comparison of field isolates from Colombia. Biological Control, 58(2), 113–120.
Bissiwu, P., & Pérez, M. J. (2016). Control efficacy of Spodoptera frujiperda using the entomopathogens Heterorhabditis bacteriophora and Metarhizium anisopliae with insecticide mixtures in corn.
Boaventura, D., et al. (2020). Detection of a ryanodine receptor target-site mutation in diamide insecticide-resistant fall armyworm, Spodoptera frugiperda. Pest Management Science, 76(1), 47–54.
Booij, C. J. H., & Noorlander, J. (1992). Farming systems and insect predators. Agriculture, Ecosystems & Environment, 40(1–4), 125–135.
Bravo, A., Gill, S. S., & Soberón, M. (2005). Comprehensive molecular insect science. Bacillus thuringiensis, 175e206.
Bravo, A., Gill, S. S., & Soberón, M. (2007). Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon, 49(4), 423–435.
Bravo, A., Hendrickx, K., Jansens, S., & Peferoen, M. (1992). Immunocytochemical analysis of specific binding of Bacillus thuringiensis insecticidal crystal proteins to lepidopteran and coleopteran mudgut membranes. Journal of Invertebrate Pathology, 60(3), 247–253.
Brookes, G., & Barfoot, P. (2017). Environmental impacts of genetically modified (GM) crop use 1996–2015: Impacts on pesticide use and carbon emissions. GM Crops & Food, 8(2), 117–147.
Bruner, S. C., de Cuba, A. D. C., Scaramuzza, L. C., & Otero, A. R. (1975). Catálogo de los insectos que atacan a las plantas económicas de Cuba-2.
Burtet, L. M., Bernardi, O., Melo, A. A., Pes, M. P., Strahl, T. T., & Guedes, J. V. (2017). Managing fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), with Bt maize and insecticides in southern Brazil. Pest Management Science, 73(12), 2569–2577.
CABI. 2020. Spodoptera frugiperda (fall armyworm). Invasive Species Compendium. CABI. Retrieved from https://www.cabi.org/isc/datasheet/29810. Retrieved July 07, 2020.
Cañas, L. A., & O’Neil, R. J. (1998). Applications of sugar solutions to maize, and the impact of natural enemies on Fall Armyworm. International Journal of Pest Management, 44(2), 59–64. https://doi.org/10.1080/096708798228329
Caniço, A., Mexia, A., & Santos, L. (2020). First report of native parasitoids of fall armyworm Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) in Mozambique. Insects, 11(9), 615.
Castro, M. (1992). Density and aspects of the biology of some pest and beneficial insects on sorghum and maize: Influence of intercropped systems with and without pigeonpea or cowpea in central and southern Honduras.
Cave, R. (1993). Parasitoides larvales y pupales de Spodoptera frugiperda (Smith) en centro américa con una clave para las especies encontradas en Honduras. Ceiba, 34(1), 24.
Cave, R. D. (2000). Biology, ecology and use in pest management of Telenomus remus. Biocontrol News Information, 21, 21–26.
Céleres. (2016). 2nd Follow‐up on agricultural biotechnology adoption for the 2016/17 crop. [Online]. Available: http://www.celeres.com.br/ [July 8 2015].
Choudhary, R., Prasad, T., & Raj, B. T. (1983). Field evaluation of some exotic parasitoids of potato tubermoth, Phthorimaea operculella (Zell.).
Cipriano García, G., María Berenice González, M., & Néstor Bautista, M. (2011). Patogenicidad de aislamientos de hongos entomopatógenos contra spodoptera frugiperda (Lepidoptera: Noctuidae) y Epilachna varivestis (Coleoptera: Coccinellidae). Revista Colombiana De Entomologia, 37(2), 217–222.
Cock, M. J., Beseh, P. K., Buddie, A. G., Cafa´, G., & Crozier, J. (2017). Molecular methods to detect Spodoptera frugiperda in Ghana, and implications for monitoring the spread of invasive species in developing countries. Scientific Reports, 7(1), 4103.
Coen, D. M. (1994). Acyclovir-resistant, pathogenic herpes viruses. Trends in Microbiology, 2, 481.
Cory, J. S. (2000). Assessing the risks of releasing genetically modified virus insecticides: Progress to date. Crop Protection, 19(8–10), 779–785.
Dara, S. K. 2013. Entomopathogenic fungus Beauveria bassiana promotes strawberry plant growth and health. UCANR eJournal Strawberries and Vegetables, September 30, 2013.
David, W. A. L. (1978). The granulosis virus of Pieris brassicae (L.) and its relationship with its host. In Advances in virus research (Vol. 22, pp. 111–161). Academic Press.
Deshmukh, S., Pavithra, H. B., Kalleshwaraswamy, C. M., Shivanna, B. K., Maruthi, M. S., & Mota-Sanchez, D. (2020). Field efficacy of insecticides for management of invasive fall armyworm, Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae) on maize in India. Florida Entomologist, 103(2), 221–227.
Elibariki, N. (2020). Candidates for augmentative biological control of Spodoptera Frugiperda in Kenya, Tanzania and Nepal. Indian Journal of Entomology. https://doi.org/10.1371/journal
Enkerlin, D. (1975). Review of Spodoptera in Lation America. Summary of research at Monterrey Tech. Inst., N.L. Mexico. 13 pp.
EPA (Environmental Protection Agency). (2006). New biopesticide active ingredients. www.epa.gov/pesticides/biopesticides/productlists/. Retrieved July 23, 2013
Espky, N. D., & Capinera, J. L. (1994). Invasion efficiency as a measure of efficacy of the entomogenous nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). Journal of Economic Entomology, 87, 366–370.
Dannon, H. F., Dannon, A. E., Douro-Kpindou, O. K., Zinsou, A. V., Houndete, A. T., Toffa-Mehinto, J., et al. (2020). Toward the efficient use of Beauveria bassiana in integrated cotton insect pest management. Journal of Cotton Research, 3, 1-21.
Ferrer, F. (2001). Biological control of agricultural insect pests in Venezuela; advances, achievements, and future perspectives. Biocontrol News Information, 22, 67–74.
Firake, D. M., & Behere, G. T. (2020). Natural mortality of invasive fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India. Biological Control, 148, 104303. https://doi.org/10.1016/j.biocontrol.2020.104303
Firake, D., Behere, G., Babu, S., & Prakash, N. (2019). Fall Armyworm: Diagnosis and Management. An Extension Pocket Book. Umiam-, 793, 103.
Fiuza, L. M. (2004). Receptores de Bacillus thuringiensis em insetos. Biotecnologia Ciência e Desenvolvimento, 32, 84–89.
Garcia-Gonzlez, F., Rios-Velasco, C., & Iglesias-Pérez, D. (2020). Chelonus and campoletis species as main parasitoids of spodoptera frugiperda (JE Smith) 1 in Forage Maize of Lagunera Region, Mexico. Southwestern Entomologist, 45(3), 639-642.
Goergen, G., Kumar, P. L., Sankung, S. B., Togola, A., & Tamò, M. (2016). First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith)(Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS One, 11(10), e0165632.
Gómez, I., Pardo-López, L., Munoz-Garay, C., Fernandez, L. E., Pérez, C., Sánchez, J., Soberón, M., Bravo, A. (2007). Role of receptor interaction in the mode of action of insecticidal Cry and Cyt toxins produced by Bacillus thuringiensis. Peptides, 28(1), 169–173.
Goncalves, C. R., & Goncalves, A. J. L. (1973). Novas observacoes sobre insetos hospedeiros de moscas da familia Tachinidae (Diptera). Agronomia, 31, 9–15.
Granados, R. R. (1980). Infectivity and mode of action of baculoviruses. Biotechnology and Bioengineering, 22(7), 1377–1405. https://doi.org/10.1002/bit.260220707
Grewal, P. S., Lewis, E. E., & Gaugler, R. (1997). Response of infective stage parasites (Nematoda: Steinernematidae) to volatile cues from infected hosts. Journal of Chemical Ecology, 23, 503–515.
Gross Jr, H. R., & Pair, S. D. (1986). The fall armyworm: Status and expectations of biological control with parasitoids and predators. Florida Entomologist, 69, 502–515.
Guang, L. Q., & Oloo, G. W. (1990). Host preference studies on Trichogramma sp. Nr. mwanzai Schulten and Feijen (Hymenoptera: Trichogrammatidae) in Kenya. International Journal of Tropical Insect Science, 11(4–5), 757–763.
Guilger-Casagrande, M., Migliorini, B. B., Germano-Costa, T., Bilesky-José, N., Harada, L. K., Campos, E. V. R., Gonçalves, K. C., Polanczyk, R. A., Fraceto, L. F., & Lima, R. (2024). Beauveria bassiana biogenic nanoparticles for the control of Noctuidae pests. Pest Management Science, 80(3), 1325–1337.
Guimarães, J. H. (1977). Host-parasite and parasite-host catalogue of South American Tachinidae (Diptera). Arq. Zool. Mus. Zool. Sao Paulo, 28, 1–131.
Gupta, A. (2013). Revision of the Indian Microplitis Foerster (Hymenoptera: Braconidae: Microgastrinae), with description of one new species. Zootaxa, 3620, 429–452.
Horikoshi, R. J., Bernardi, D., Bernardi, O., Malaquias, J. B., Okuma, D. M., Miraldo, L. L., & Omoto, C. (2016). Effective dominance of resistance of Spodoptera frugiperda to Bt maize and cotton varieties: Implications for resistance management. Scientific Reports, 6, 34864.
Hui, L. I., et al. (2021). Two-way predation between immature stages of the hoverfly Eupeodes corollae and the invasive fall armyworm (Spodoptera frugiperda JE Smith). Journal of Integrative Agriculture, 20(3), 829–839.
Huis, A. Van. (1981). Integrated pest management in the small farmer's maize crop in Nicaragua. In: H. Veenman and Zonen B.V.-Wageningen, The Netherlands. pp. 221
Idemudia, I., Fening, K. O., Agboyi, L. K., Wilson, D., Clottey, V. A., Beseh, P., & Aigbedion-Atalor, P. O. (2024). First report of the predatory potential and functional response of the red flower assassin bug Rhynocoris segmentarius (Germar), a natural enemy of Spodoptera frugiperda (JE Smith). Biological Control. https://doi.org/10.1016/j.biocontrol.2024.105465
Idrees, A., & Afzal, A. (2023). Virulence of entomopathogenic fungi against fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) under laboratory conditions. Frontiers in Physiology, 14, 1107434.
Isenhour, D. J., Layton, R. C., & Wiseman, B. R. (1990). Potential of adult Orius insidiosus [Hemiptera: Anthocoridae] as a predator of the fall armyworm, Spodoptera frugiperda [Lepidoptera: Noctuidae]. Entomophaga, 35(2), 269–275. https://doi.org/10.1007/BF02374802
Jalali, S. K., Venkatesan, T., Murthy, K. S., & Ojha, R. (2016). Management of Helicoverpa armigera (Hübner) on tomato using insecticide resistance egg parasitoid, Trichogramma chilonis Ishii in farmers’ field. Indian Journal of Horticulture, 73(4), 611–614.
Jehle, J. A., Blissard, G. W., Bonning, B. C., Cory, J. S., Herniou, E. A., Rohrmann, G. F., & Vlak, J. M. (2006). On the classification and nomenclature of baculoviruses: A proposal for revision. Archives of Virology, 151(7), 1257–1266.
Jeon, I., & Kim, J. S. (2024). Soil treatment with Beauveria and Metarhizium to control fall armyworm, Spodoptera frugiperda, during the soil-dwelling stage. Journal of Asia-Pacific Entomology, 27(1), 102193.
Jiang, J. X., Yang, J. H., Ji, X. Y., Zhang, H., & Wan, N. F. (2018). Experimental temperature elevation promotes the cooperative ability of two natural enemies in the control of insect herbivores. Biological Control, 117, 52–62.
Jones, K. A. (2000). Bioassays of entomopathogenic viruses. Bioassays of Entomopathogenic Microbes and Nematodes. CAB International, Oxon, 95–140.
Jurat-Fuentes, J. L., & Adang, M. J. (2004). Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. European Journal of Biochemistry, 271(15), 3127–3135.
Karundeng, A., Mamahit, J. M. E., & Kandowangko, D. S. (2024). Predators and parasitoids species of Spodoptera frugiperda JE Smith on Corn Plant In North Minahasa Regency. Jurnal Agroekoteknologi Terapan, 5(1), 6–12.
Kenis, M. (2023). Prospects for classical biological control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in invaded areas using parasitoids from the Americas. Journal of Economic Entomology, 116(2), 331–341.
Knaak, N., Berlitz, D. L., & Fiuza, L. M. (2012). Toxicology of the bioinsecticides used in agricultural food production. Histopathology: Reviews and Recent Advances, 177–194.
Knaak, N., & Fiuza, L. M. (2005). Histopathology of Anticarsia gemmatalis Hübner (Lepidoptera; Noctuidae) treated with Nucleopolyhedrovirus and Bacillus thuringiensis serovar kurstaki. Brazilian Journal of Microbiology, 36(2), 196–200.
Knaak, N., Franz, A. R., Santos, G. F., & Fiuza, L. M. (2010). Histopathology and the lethal effect of Cry proteins and strains of Bacillus thuringiensis Berliner in Spodoptera frugiperda JE Smith Caterpillars (Lepidoptera, Noctuidae). Brazilian Journal of Biology, 70(3), 677–684.
Knowles, B. H. (1994). Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins. In Advances in insect physiology (Vol. 24, pp. 275–308). Academic Press.
Knowles, B. H., & Dow, J. A. (1993). The crystal δ-endotoxins of Bacillus thuringiensis: Models for their mechanism of action on the insect gut. BioEssays, 15(7), 469–476.
Kouassi, M., Coderre, D., & Todorova, S. I. (2003). Effects of the timing of applications on the incompatibility of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). Journal of Applied Entomology, 127(7), 421–426.
Kumar, A., Babu, S. R., Singh, B., & Sruthi, K. K. (2024). First report on Brachymeria spp (Hymenoptera: Chalcididae) as a Hyperparasitoid of Charops bicolor Szepligeti (Hymenoptera: Ichneumonidae) an larval parasitoid of Spodoptera frugiperda (JE Smith) in Maize from Southern Rajasthan India.
Kumar, S. (2012). Biopesticides: A need for food and environmental safety. J Biofertil Biopestic, 3(4), 1–3.
Laminou, S. A., Ba, M. N., Karimoune, L., Doumma, A., & Muniappan, R. (2023). Parasitism of Telenomus remus Nixon on Spodoptera frugiperda JE Smith and acceptability of Spodoptera littoralis Boisduval as factitious host. Biological Control, 183, 105242.
Lewis, W. J., & Nordlund, D. A. (1980). Employment of parasitoids and predators for fall armyworm control. The Florida Entomologist, 63(4), 433-438
Leyva-Hernández, H. A., García-Gutiérrez, C., Ruíz-Vega, J., Calderón-Vázquez, C. L., Luna-González, A., & García-Salas, S. (2018). Evaluación de la Virulencia de Steinernema riobrave y Rhabditis blumi contra Larvas del Tercer Instar de Spodoptera frugiperda1. Southwestern Entomologist, 43(1), 189–197.
Luginbill, P. (1928). The fall armyworm. U.S. Dept. Agric.Tech. Bull. 34, pp. 91
Mallapur, C. P., Naik, A. K., Hagari, S., Praveen, T., Patil, R. K., & Lingappa, S. (2018). Potentiality of Nomurae arileyi (Farlow) Samson against the fall armyworm, Spodoptera frugiperda (Smith J. E.) infesting maize. Journal of Entomology and Zoology Studies, 6(6), 1062–1067.
Manupriya. (2019). Fall armyworm, destroyer of maize farms, causes concern in India. Mongobay, 2nd September.
Margaría, C., Roberto, J., & Parra, P. (2015). V41N2a06, 41(2), 184–186
Mascarin, G. M., & Jaronski, S. T. (2016). The production and uses of Beauveria bassiana as a microbial insecticide. World Journal of Microbiology and Biotechnology, 32, 1–26.
McCutcheon, G. S., & Harrison, W. (1987). Host range and development of Microplitis rufiventris (Hymenoptera: Braconidae) an imported parasitoid of several lepidopterous pests. Environmental Entomology, 16(4), 855–858. https://doi.org/10.1093/ee/16.4.855
McCutcheon, G. S., Salley, W. Z., & Turnipseed, S. G. (1983). Biology of Apanteles ruficrus1, an Imported Parasitoid of Pseudoplusia includens, Trichoplusia ni, and Spodoptera frugiperda (Lepidoptera: Noctuidae). Environmental Entomology, 12(4), 1055–1058. https://doi.org/10.1093/ee/12.4.1055
McSorley, R. (1999). Host suitability of potential cover crops for root-knot nematodes. Journal of Nematology, 31(4S), 619.
Mekonnen, M. A., Emirie, G. A., Mitiku, S. Y., Hailemariam, B. N., Mekonnen, M. B., & Mengistu, A. A. (2024). Occurrence and pathogenicity of indigenous entomopathogenic fungi isolates to fall armyworm (Spodoptera frugiperda JE Smith) in Western Amhara, Ethiopia. Psyche: A Journal of Entomology. https://doi.org/10.1155/2024/7444094
Minarni, E. W., & Nurtiati, N. (2024). The preference of parasitoid Telenomus remus ON Spodoptera litura eggs as an alternative host in its propagation. Proceeding ICMA-SURE, 3(1), 33–37.
Molina-Ochoa, J., Carpenter, J. E., Heinrichs, E. A., & Foster, J. E. (2003). Parasitoids and parasites of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas and Caribbean Basin: An inventory. Florida Entomologist, 86(3), 254–289.
Molina-Ochoa, J., Carpenter, J. E., Lezama-Gutiérrez, R., Foster, J. E., González-Ramírez, M., Angel-Sahagún, C. A., & Farías-Larios, J. (2004). Natural distribution of hymenopteran parasitoids of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae in Mexico. Florida Entomologist, 87(4), 461–472. https://doi.org/10.1653/0015-4040(2004)087[0461:NDOHPO]2.0.CO;2
Molnar, J. L., Gamboa, R. L., Revenga, C., & Spalding, M. D. (2008). Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment, 6(9), 485–492. https://doi.org/10.1890/070064
Monnerat, R. G., & Bravo, A. (2000). Proteínas bioinseticidas produzidas pela bactéria Bacillus thuringiensis: Modo de ação e resistência. Controle Biológico, 3, 163–200.
Montezano, D. G., Specht, A., Sosa-Go´mez, D. R., Roque-Specht, V. F., Sousa-Silva, J. C., Paula-Moraes, S. V., Peterson, J. A., & Hunt, T. E. (2018). Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, 26(2), 286–301.
Mugo, S., Anani, B., Ahonsi, M., Beyene, Y., & Prasanna, B. M. (2018). Fall Armyworm: State of invasion and Management in Africa and Beyond. ICRC Agro/Livestock Workshop: Water in Agriculture and Livestock Production Systems.
Muraro, D. S., Stacke, R. F., Cossa, G. E., Godoy, D. N., Garlet, C. G., Valmorbida, I., Oneal, M. E., & Bernardi, O. (2020). Performance of seed treatments applied on bt and non-bt maize against fall armyworm (Lepidoptera: Noctuidae). Environmental Entomology. https://doi.org/10.1093/ee/nvaa088
Murúa, G., Molina-Ochoa, J., & Coviella, C. (2006). Population dynamics of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) and its parasitoids in northwestern Argentina. Florida Entomologist, 89(2), 175–182. https://doi.org/10.1653/0015-4040(2006)89[175:PDOTFA]2.0.CO;2
Nurkomar, I., Putra, I. L. I., Buchori, D., & Setiawan, F. (2024). Association of a global invasive pest Spodoptera frugiperda (Lepidoptera: Noctuidae) with the local parasitoids: prospects for a new approach in biological control.
Oestergaard, J., Ehlers, R. U., Martínez-Ramírez, A. C., & Real, M. D. (2007). Binding of Cyt1Aa and Cry11Aa toxins of Bacillus thuringiensis serovar israelensis to brush border membrane vesicles of Tipula paludosa (Diptera: Nematocera) and subsequent pore formation. Applied and Environmental Microbiology, 73(11), 3623–3629.
Ordóñez-García, M., Rios-Velasco, C., Berlanga-Reyes, D. I., Acosta-Muñiz, C. H., Salas-Marina, M. Á., & Cambero-Campos, O. J. (2015). Occurrence of natural enemies of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Chihuahua, Mexico. Florida Entomologist, 98(3), 843–847. https://doi.org/10.1653/024.098.0305
Ordóñez-García, M., Rios-Velasco, C., de Ornelas-Paz, J., Bustillos-Rodríguez, J. C., Acosta-Muñiz, C. H., Berlanga-Reyes, D. I., & Gallegos-Morales, G. (2020). Molecular and Morphological characterization of multiple nucleopolyhedrovirus from Mexico and their insecticidal activity against Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Applied Entomology, 144(1–2), 123–132. https://doi.org/10.1111/jen.12715
Painter, R. H. (1955). Insects on corn and teosinte in Guatemala. Journal of Economic Entomology, 48, 36–42.
Pair, S. D., & Gross, H. R. (1989). Seasonal incidence of fall armyworm (Lepidoptera: Noctuidae) pupal parasitism in corn by Diapetimorpha introita and Cryptus albitarsis (Hymenoptera: Ichneumonidae). Journal of Entomological Science, 24(3), 339–343.
Pal, S., Bhattacharya, S., Dhar, T., Gupta, A., Ghosh, A., Debnath, S., Gangavarapu, N., Pati, P., Chaudhuri, N., Chatterjee, H., Senapati, S. K., & Laing, A. M. (2024). Hymenopteran parasitoid complex and fall armyworm: a case study in eastern India. Scientific Reports, 14(1), 4029.
Parker, H., Berry, P., & Guido, A. S. (1953). Host-par- asite and parasite-host lists of insects reared in the South American parasite laboratory (p. 100). Republica Oriental del Uruguay.
Paschke, J. D., & Summers, M. D. (1975). Early events in the infection of the arthropod gut by pathogenic insect viruses (Vol. 75). New York: Academic Press.
Perier, J. D. (2019). Integration of Two Predaceous Stinkbugs and a Larval Parasitoid to Manage the Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Diss. Florida Agricultural and Mechanical University
Perumal, V., Kannan, S., Alford, L., Pittarate, S., & Krutmuang, P. (2024). Study on the virulence of Metarhizium anisopliae against Spodoptera frugiperda (JE Smith, 1797). Journal of Basic Microbiology. https://doi.org/10.1002/jobm.202300599
Peters, A. (1996). The natural host range of Steinernema and Heterorhabditis spp. and their impact on insect populations. Biocontrol Science and Technology, 6, 389–402.
Pomar, G. O., Jr., & Leutenegger, R. (1968). Anatomy of the effective and normal third stage juveniles of Steinernema carpocapsae Weiser (Steinernematidae: Nematoda). Journal of Parasitology, 54, 340–350.
Rao, B. N. (1972). Studies on the biology of chelonus formosanus sonanan egg-larval parasite of Spodoptera litura F (Doctoral dissertation, AAU, Anand).
Raulston, J. R., Pair, S. D., Loera, J., & Cabanillas, H. E. (1992). Prepupal and Pupal Parasitism of Helicoverpa zea and Spodoptera frugiperda (Lepidoptera: Noctuidae) by Steinernema sp. in Cornfields in the Lower Rio Grande Valley. Journal of Economic Entomology, 85(5), 1666–1670. https://doi.org/10.1093/jee/85.5.1666
Ravlin, F. W., Stehr, F. W. (1984). Revision of the genus Archytas (Diptera: Tachinidae) for America North of Mexico. Misc. Pub. Entomol. Soc. Am. 58, pp. 59
Richter, A. R., & Fuxa, J. R. (1990). Effect of Steinernema feltiae on Spodoptera frugiperda and Heliothis zea (Lepidoptera: Noctuidae) in corn. Journal of Economic Entomology, 83(4), 1286–1291.
Riggin, T. M., Espelie, K. E., Wiseman, B. R., & Isenhour, D. J. (1993). Distribution of fall armyworm (Lepidoptera: Noctuidae) parasitoids on five corn genotypes in South Georgia. Florida Entomologist, 292–302.
Rios-Velasco, C., Gallegos-Morales, G., Cambero-Campos, J., Cerna-Chávez, E., Del Rincón-kre, M. C., & Valenzuela-García, R. (2011). Natural enemies of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila, Mexico. Florida Entomologist, 94(3), 723–726. https://doi.org/10.1653/024.094.0349
Robertson, J. S., Harrap, K. A., & Longworth, J. F. (1974). Baculovirus morphogenesis: The acquisition of the virus envelope. Journal of Invertebrate Pathology, 23(2), 248–251.
Rodriguez-Chalarca, J., Valencia, S. J., Rivas-Cano, A., Santos-González, F., & Romero, D. P. (2024). Impact of Bt corn expressing Bacillus thuringiensis Berliner insecticidal proteins on the growth and survival of Spodoptera frugiperda larvae in Colombia. Frontiers in Insect Science, 4, 1268092.
Rogers, C. E., O. G. Marti, Jr., and A. M. Simmons. 1993. Noctuidonema guyanense (Nematoda: Aph- elenchoididae): Host range and pathogenicity to the fall armyworm, Spodoptera frugiperda (Lepi- doptera: Noctuidae), pp. 27–32. In Nematodes and the biological control of insect pests. Bedding, R., R. Akhurst & H. Kaya [eds.] CSIRO, Australia.
Rohlfs, W. M., & Mack, T. P. (1984). Functional response of Ophion flavidus Brulle (Hymenoptera: Ichneumonidae) females to various densities of Fall Armyworm (Spodoptera frugiperda J. E. Smith) (Lepidoptera: Noctuidae). Environmental Entomology, 13(3), 708–710. https://doi.org/10.1093/ee/13.3.708
Roque-Romero, L., Cisneros, J., Rojas, J. C., Ortiz-Carreon, F. R., & Malo, E. A. (2020). Attraction of Chelonus insularis to host and host habitat volatiles during the search of Spodoptera frugiperda eggs. Biological Control, 140, 104100. https://doi.org/10.1016/j.biocontrol.2019.104100
Ruíz-Nájera, R. E., Molina-Ochoa, J., Carpenter, J. E., Espinosa-Moreno, J. A., Foster, J. E., Ruíz-Nájera, J. A., & Lezama-Gutiérrez, R. (2007). Survey for hymenopteran and dipteranparasitoids of the fall armyworm (lepidoptera: Noctuidae) in Chiapas, Mexico. Journal of Agricultural and Urban Entomology, 24(1), 35–42. https://doi.org/10.3954/1523-5475-24.1.35
Ruiz-Nájera, R. E., Ruiz-Estudillo, R. A., Sánchez-Yáñez, J. M., Molina-Ochoa, J., Skoda, S. R., Coutiño-Ruiz, R., Pinto-Ruiz, R., Guevara-Hernández, F., & Foster, J. E. (2013). Occurrence of entomopathogenic fungi and parasitic nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae collected in Central Chiapas, México. Florida Entomologist, 96(2), 498–503. https://doi.org/10.1653/024.096.0215
Ryder, W. D., Pulgar, N. (1969). A note on parasitism of the fall armyworm, Spodoptera frugiperda, on maize. Rev. Cuban Cien. Agric. [English ed.] 3: 267–271.
Saakre, M., Kesiraju, K., Raman, K. V., Jaiswal, S., Tyagi, S., Tilgam, J., Paul, K., Bhattacharjee, S., Sreevathsa, R., & Pattanayak, D. (2024). Transgenic tobacco expressing a novel Bt gene, cry1AcF, show resistance against fall armyworm (Spodoptera frugiperda). Journal of Plant Biochemistry and Biotechnology, 33(1), 85–91.
Sabrosky, C. W. (1981). A partial revision of the genus Eucelatoria (Diptera, Tachinidae), including important parasites of Heliothis (No. 1635). The Administration.
Semidey, N., & Aviles, L. N. (1998). Proceedings of the Caribbean Food Crops Society, Vol 33, XV, 2013. Retrieved from http://cfcs.eea.uprm.edu/Proceedings/CFCS 1997 Vol. 33.pdf
Shamseldean, M. S. M., Abo-Shady, N. M., El-Awady, M. A., & Heikal, M. N. (2024). Heterorhabditis alii n. sp. (Nematoda: Heterorhabditidae), a novel entomopathogenic nematode from Egypt used against the fall armyworm, Spodoptera frugiperda (Smith 1797) (Lepidoptera: Noctuidae). Egyptian Journal of Biological Pest Control, 34(1), 13.
Shapiro-Ilan, D. I., Lewis, E. E., Behle, R. W., & McGuire, M. R. (2001). Formulation of entomopathogenic nematode-infected cadavers. Journal of Invertebrate Pathology, 78(1), 17–23.
Shi, Z., Li, Y., Wu, S., Xiao, Y., Zeng, W., Jia, S., Xie, Y., Yang, Y., Tan, L., & Wang, Y. (2024). The complete genome and biological activity of a novel Spodoptera litura multiple nucleopolyhedrovirus for controlling Spodoptera frugiperda. Biological Control, 188, 105412.
Simmons, A. M., & Rogers, C. E. (1996). Ectoparasitic Acugutturid Nematodes of adult Lepidoptera. Journal of Nematology, 28(1), 1–7.
Sisay, B., Simiyu, J., Malusi, P., Likhayo, P., Mendesil, E., Elibariki, N., Wakgari, M., Ayalew, G., & Tefera, T. (2018). First report of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), natural enemies from Africa. Journal of Applied Entomology, 142(8), 800–804. https://doi.org/10.1111/jen.12534
Sisay, B., Simiyu, J., Mendesil, E., Likhayo, P., Ayalew, G., Mohamed, S., Subramanian, S., & Tefera, T. (2019). Fall armyworm, spodoptera frugiperda infestations in East Africa: Assessment of damage and parasitism. Insects, 10(7), 1–10. https://doi.org/10.3390/insects10070195
Song, Y., Chen, Y., Zhang, K., Yang, M., & Liu, J. (2024). A mite parasitoid, Pyemotes zhonghuajia, negatively impacts the fitness traits and immune response of the fall armyworm, Spodoptera Frugiperda. Journal of Integrative Agriculture, 23(1), 205–216.
Sousa, M. E. C., Santos, F. A., Wanderley-Teixeira, V., Teixeira, Á. A., de Siqueira, H. Á. A., Alves, L. C., & Torres, J. B. (2010). Histopathology and ultrastructure of midgut of Alabama argillacea (Hübner)(Lepidoptera: Noctuidae) fed Bt-cotton. Journal of Insect Physiology, 56(12), 1913–1919.
Sparks, A. N. (1986). Fall Armyworm (Lepidoptera: Noctuidae): Potential for Area-Wide Management Author (s): A. N. Sparks Published by : Florida Entomological Society Florida Entomological Society is collaborating with JSTOR to digitize, preserve and extend access to T. Florida Entomological Society, 69(3), 603–614.
Styer, E. L., Hamm, J. J., & Nordlund, D. A. (1987). A new virus associated with the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae): Replication in noctuid host larvae. Journal of Invertebrate Pathology, 50(3), 302–309. https://doi.org/10.1016/0022-2011(87)90096-6
Summers, M. D., & Paschke, J. D. (1970). Alkali-liberated granulosis virus of Trichoplusia ni: I. Density gradient purification of virus components and some of their in vitro chemical and physical properties. Journal of Invertebrate Pathology, 16(2), 227–240.
Sun, B., et al. (2020). First report of Ovomermis sinensis (Nematoda: Mermithidae) parasitizing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in China. Journal of Nematology, 52, 1.
Sun, J.-W., et al. (2021). Performance of two trichogrammatid species from Zambia on Fall Armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). Insects, 12(10), 859.
Tefara, T., Goftishu, M., Ba, M., & Muniappan, R. (2019). A guide to biological control of fall armyworm in Africa using egg parasitoids, (September). Retrieved from http://34.250.91.188:8080/xmlui/handle/123456789/1001
Tendeng, E., Labou, B., Diatte, M., Djiba, S., & Diarra, K. (2019). The fall armyworm Spodoptera frugiperda (J.E. Smith), a new pest of maize in Africa: biology and first native natural enemies detected. International Journal of Biological and Chemical Sciences, 13(2), 1011. https://doi.org/10.4314/ijbcs.v13i2.35
Thangavel, P., & Sridevi, G. (2015). Environmental sustainability: Role of green technologies. Environmental Sustainability: Role of Green Technologies. https://doi.org/10.1007/978-81-322-2056-5
Tian, S., Di, X. Y., Yan, B., Ren, P., Wu, H. Z., & Yang, M. F. (2024). Parasitism success of Microplitis manilae (Hymenoptera: Braconidae) on different diet-fed Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. Journal of Applied Entomology, 148(2), 199–204.
Tingle, F. C., Mitchell, E. R., & McLaughlin, J. R. (1994). Lepidopterous pests of cotton and their parasitoids in a double-cropping environment. Florida entomologist, 334–341.
Varella, A. C., Menezes-Netto, A. C., De Souza Alonso, J. D., Caixeta, D. F., Peterson, R. K. D., & Fernandes, O. A. (2015). Mortality dynamics of Spodoptera frugiperda (Lepidoptera: Noctuidae) immatures in maize. PLoS One, 10(6), 1–12. https://doi.org/10.1371/journal.pone.0130437
Varshney, R., Poornesha, B., Raghavendra, A., et al. (2021). Biocontrol-based management of fall armyworm, Spodoptera frugiperda (J E Smith) (Lepidoptera: Noctuidae) on Indian Maize. Journal of Plant Diseases and Protection, 128, 87–95. https://doi.org/10.1007/s41348-020-00357-3
Virla, E. G., Colomo, M. V., Berta, C., & Valverde, L. (1999). The complex of parasitoids of fall armyworm of maize, Spodoptera frugiperda, in Argentina. Lepidoptera.
Viteri, D. M., Linares, A. M., & Flores, L. (2018). Use of the entomopathogenic nematode Steinernema carpocapsae in combination with low-toxicity insecticides to control fall armyworm (Lepidoptera: Noctuidae) larvae. Florida Entomologist, 101(2), 327–329.
Wall, R., & Berberet, R. C. (1975). Parasitoids associated with lepidopterous pests on peanuts; Oklahoma fauna. Environmental Entomology, 4, 877–882.
Wan, N. F., Yang, J. H., Zhang, H., Wang, J. Y., Chen, Y. J., Ji, X. Y., & Jiang, J. X. (2019). Prior experiences of endoparasitoids affect their ability to discriminate NPV-infected from non-infested caterpillars. Biological Control, 128, 64–75.
Westbrook, J. K., Nagoshi, R. N., Meagher, R. L., Fleischer, S. J., & Jairam, S. (2016). Modeling seasonal migration of fall armyworm moths. International Journal of Biometeorology, 60, 255–267.
Wheeler, G. S., Ashley, T. R., & Andrews, K. L. (1989). Larval parasitoids and pathogens of the fall armyworm in honduran maize. Entomophaga, 34(3), 331–340. https://doi.org/10.1007/BF02372472
Winterton, S. L. (2009). Scales and setae. In Encyclopedia of insects (pp. 901–904). Academic Press.
Wraight, S. P., Ramos, M. E., Avery, P. B., Jaronski, S. T., & Vandenberg, J. D. (2010). Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops. Journal of Invertebrate Pathology, 103(3), 186–199. https://doi.org/10.1016/j.jip.2010.01.001
Yaseen, M. (1978). Introduction of exotic parasites for control of Spodoptera and Heliothis in Trinidad (No. 2019-2017-4351).
Zamora, N., Murillo, R., Lasa, R., Pineda, S., Figueroa, J. I., Bravo-Patiño, A., Díaz, O., Corrales, J. L., & Martínez, A. M. (2017). Genetic and biological characterization of four nucleopolyhedrovirus isolates collected in Mexico for the control of Spodoptera exigua (Lepidoptera: Noctuidae). Journal of Economic Entomology, 110(4), 1465–1475.
Zapata, M. R. (1984). Enemigos naturales de Spodoptera frugiperda, Mocis latipes y Diatrea spp. en el cultivo de maiz. Sociedad Mexicana de Entomologia, p. 56 En Resumenes XIX Congreso Nacional de Entomologia. Guanajuato, Guanajuato, Mexico.
Zarkani, A., Risky, H. W., Sipriyadi, S. (2020). New invasive pest, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) attacking corns in Bengkulu, Indonesia. Serangga 25(1).
Zhang, X., Candas, M., Griko, N. B., Taussig, R., & Bulla, L. A. (2006). A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proceedings of the National Academy of Sciences, 103(26), 9897–9902.
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Mahmood, S., Parwez, H. The repository of biocontrol agents for Spodoptera frugiperda (Smith, 1797) with emphasis on their mode of action. JoBAZ 85, 18 (2024). https://doi.org/10.1186/s41936-024-00358-w
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DOI: https://doi.org/10.1186/s41936-024-00358-w