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1 June 2013 Occurrence of Entomopathogenic Fungi and Parasitic Nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) Larvae Collected in Central Chiapas, México
Ramiro E. Ruiz-Nájera, Ramiro A. Ruiz-Estudillo, Juan M. Sánchez-Yáñez, Jaime Molina-Ochoa, Steven R. Skoda, Roberto Coutiño-Ruiz, René Pinto-Ruiz, Francisco Guevara-Hernández, John E. Foster
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Fall armyworm larvae (FAW), Spodoptera frugiperda (J. E. Smith) were collected from whorl-stage corn, Zea mays (L.), between the V2 and V4 stages, in 22 localities of Central, Chiapas, México, called “La Frailesca” during late Jun 2009 to determine the occurrence of native entomopathogens and parasitic nematodes, and to determine the most parasitized instars. A total of 1,247 larvae were examined in search of native biological control agents. Overall total larval mortality was 16.36%. The percent larval mortality due to entomopathogens and parasitic nematodes was 12.99%. Hexamermis sp., probably albicans Siebold (Mermitha: Mermithidae) were isolated from 105 FAW larvae (8.42%) with highest incidence from the 4th, 5th, 6th and 3rd instars, respectively. Ahyphomycete, Nomuraea rileyi Farlow (Samson), was recovered from 38 larvae (about 3.05% parasitism) with highest incidence in the 5th, 3rd, 4th, and 6th instars, respectively. Lowest percentage of FAW larval parasitism was caused by unidentified microsporidian or microsporidium (1.52%), infecting 19 larvae in the 6th, 5th and 3rd instars, respectively. First and 2nd instars did not show parasitism. This information is useful in designing future biological control programs.

The fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is well known in the Western Hemisphere as a voracious insect pest of multiple agricultural crops (Clark, 2007; Murúa et al. 2009). It is an important economic pest of corn, Zea mays (L.) (Poales: Poaceae), other grain crops and forage sorghums, peanuts, cotton, soybeans, alfalfa, and occasionally other crops (Sparks 1986; Lu & Adang 1996).

Corn is one of the most valuable field crops in the United States of America (USA). The FAW is one of the most destructive insects attacking corn; FAW feeds on tender leaves and stalks causing severe damage in every stage of plant development, resulting in limited production or complete destruction of whorl-stage plants (Wiseman et al. 1967, 1996). In Latin America maize losses in grain production are about 90% (Andrews 1988; Hruska & Gould 1997). Chemical control of FAW is a common practice; however, the adverse effects of the use of insecticides lead to a search for alternatives (Aktar et al. 2009). Microbial control is an environmentally sound and valuable alternative for controlling the FAW. FAW larvae are susceptible to entomopathogenic microorganisms such as bacteria, fungi, nematodes, viruses, and protozoa (Gardner & Fuxa 1980; Hamm et al. 1986; Patel & Habib 1988; Lezama-Gutiérrez et al. 1996; Molina-Ochoa et al. 1999; Molina-Ochoa et al. 2003; Ríos-Velasco et al. 2010).

The natural enemy complex, particularly pathogens, is poorly known in México, and there is an increased interest in developing biological control methods for FAW. Most concentrated efforts for biological control appear to be directed towards the “rear and release” augmentation, followed by importation and thirdly by conservation; Lewis et al. (1997) suggested a reversed order of priorities. There is a need to understand, promote and maximize the effectiveness of indigenous populations of natural enemies, and based on the knowledge and results of these, we should supplement any gaps by importation. The information on the naturally occurring natural enemy complex of the FAW larvae in “La Frailesca” located in central-western Chiapas, México is scarce, so we surveyed whorl-stage corn to determine the occurrence, and parasitism rates of entomopathogenic microorganisms and parasitic nematodes of FAW larvae, as well as to determine which of the larval instars were the most parasitized.


This survey was conducted during late Jun 2009 in the region known as “La Frailesca” located in the central-western of the state of Chiapas (municipalities of Villaflores, Villacorzo, La Concordia and Angel Albino Corzo) located between the coordinates 15°45′ and 16°30′ N latitude, and between 92°30′ and 93°45′ W longitude; elevation ranging between 700 and 800 m asl (Anuario Estadístico de la Producción Agrícola 2008). The region has an annual mean temperature of 22 °C, and annual rainfall between 700 to 1200 mm (Table 1).

During late Jun 2009 collections of FAW larvae were made from whorl-stage corn in the phenological stages V2 to V4 (Ritchie et al. 1992). For each locality, at least 274 larvae were sampled. Each sample consisted of different FAW instars. FAW larvae were individually placed into 250 mL plastic cups, covered on top with a paper lid, held in the laboratory (25 ± 3 °C, 80% RH, and 12:12 h L:D) to record infected larvae. Larvae were fed with fresh corn leaves, each about 20 cm2/cup, replenished every 36 h until pupation. Corn leaves were disinfected by immersion for 2 min in a 0.5% sodium hypoclorite solution, then washed with sterile, distilled water (Sánchez & Bellotti 1997).

Mermithid nematodes that emerged from larvae were placed in 2 mL crystal vials with 70% ethanol, and were identified according Nickle (1972). Dead larvae showing signs of fungus infection were placed in plastic Petri dishes (60 × 10 mm) lined with filter paper moistened with sterile distilled water until the fungus sporulated on the insect (Fargues & Rodríguez-Rueda 1980). Nomuraea rileyi Farlow (Samson) (Moniliales: Moniliaceae) was isolated from dead larvae on medium composed of 200 mL of “V8” vegetable juice, 3 g CaCO3 5 g glucose, 2 g yeast extract, 15 g agar, and 800 mL distilled water (Fargues & Rodríguez-Rueda 1980). Fungal identification was according to Brady (1979) and Barnett & Hunter (1998). Larvae showing signs of infection by microsporidia were examined microscopically.





Out of 1,247 larvae collected from corn in 22 locations of “La Frailesca” Chiapas, 204 larvae were found to be infected by mermithid nematodes, entomopathogenic fungi and microsporidia. Total mortality by these agents was 12.99%. Larval mortality by unknown causes was about 3.37% (42).

Mermithid nematode species Hexamermis probably albicans Siebold (Nematoda: Mermithidae) caused the highest mortality rate of 8.42% (105 larvae), followed by N. rileyi causing 3.05% mortality (38 larvae), and an unidentified microsporidia causing 1.52% (19 dead larvae).

Thus mermithid nematodes were the most important natural enemies of FAW larvae. In the four locations, the 4th, 5th, and 3rd FAW instars were most parasitized by the mermithid Hexamermis sp. with 34, 25, and 22 larvae or 2.73%, 2.00%, and 1.76% parasitized, respectively (Table 2).

Hexamermis sp. has a wide distribution range, having been reported infesting FAW larvae in Honduras, Brazil, Nicaragua, and Argentina (Van Huis 1981; Valicente 1989; Wheeler et al. 1989; Vera et al. 1995). In México, Hexamermis sp. was reported in the states of Colima (Lezama-Gutiérrez et al. 2001), Nayarit and Veracruz (Molina-Ochoa et al., 2003) causing percentage mortality ranging from 0.0–14.9%, 0.0–3.33% and 0.0-15.05%, respectively. Hexamermis sp., has been also reported attacking other insect pests such as Diatraea saccharalis (F.) (Lepidoptera: Crambidae), and Hypsipyla grandella (Zeller) (Lepidoptera: Pyralidae) in Colombia (Vergara 2004).

Nomuraea rileyi was the only entomopathogenic fungus species isolated from dead FAW larvae, mostly 3rd to 6th instars. Twelve 3rd instars (0.96%), ten 4th and ten 5th instars (0.80%, respectively), and six 6th instars (0.48%) were infected by this fungus in the 4 locations (Table 2); larvae were fully covered with whitish hyphae, dusty green mass of N. rileyi spores, conidia as well as phialides (Bosa et al. 2004). The highest infection percentage caused by N. rileyi was exhibited by 3rd instars at 0.96%. We did not observe 1st and 2nd instars parasitized by N. rileyi; however, Bosa et al. (2004) emphasized that 2nd instar FAW was the most susceptible, but we found that the 5th instars suffered the highest mortality with 0.40% at Villaflores (Table 2). However, Molina-Ochoa et al. (2003), and Lezama-Gutiérrez et al. (2001) reported 44.4% and 16.7% for a single location in the state of Jalisco. Nomuraea rileyi caused an epizootic in Coahuila, México, and the number of rainy days and the rainfall amount were possibly the most important environmental factors favoring the growth of the fungus (Ríos-Velasco et al. 2010).




An unidentified microsporidia that infected FAW larvae was the third most frequent cause of FAW total larval mortality (1.52%) (Table 2). Mortality ranged from 0.00 to 0.48%. Similar mortality percentages were reported by Lezama-Gutiérrez et al. (2001) in the Mexican states of Colima, Jalisco and Michoacán. In these studies FAW larvae showed no obvious symptoms prior to their death, but after death the cadavers were often dry and fragile, resembling the ash of a cigarette. The identification was not verified by electron microscopy. Of the total larval mortality 4.24% was attributed to unknown causes (Table 2).

Regardless of location, the highest mortality rates caused by entomopathogens and parasitic nematodes were observed on the 3rd, 4th, 5th and 6th FAW instars (Table 2). Similar results were reported by Alcocer & Méndez (1965), who asserted that FAW last instar larvae allow the development of entomopathogens and parasitic nematodes. Gross & Pair (1991), stated that a parasitoid Ophion flavidus Brulle (Hymenoptera: Ichneumonidae), parasitized 4th, 5th, and 6th FAW instars with equal success, but was minimally successful in completing development on late 6th instar larvae.

Ruiz-Nájera et al. (2007) stated that the parasitoid complex, as part of the native natural enemy complex in corn fields of Chiapas can cause a reduction in the FAW larval populations. We also found that the distribution of the entomopathogens indicates a potential for biological control.

Results of this survey suggest a need for more taxonomic studies of microsporidia and parasitic nematodes in Mexico, particularly for the mermithid species of Hexamermis in central Chiapas. We speculate that the augmentation and release of N. rileyi in La Frailesca, Chiapas corn fields during the rainy season would reduce FAW infestations and their damage to the crop.



W. Aktar , D. Sengupta , and A. Chowdhury 2009. Impact of pesticide use in agriculture: their benefits and hazards. Interdisciplinary Toxicol. 2: 1–12. Google Scholar


G. L. Alcocer , and M. Méndez 1965. Estudios preliminares sobre parasitismo en larvas de Laphygma frugiperda Smith &Abbot, por un nematodo de la familia Mermithidae. Fitófilo 18: 5–20. Google Scholar


K. L. Andrews 1988. Latin American research on Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomol. 71: 630–653. Google Scholar


ANUARIO ESTADÍSTICO DE LA PRODUCCIÓN AGRÍCOLA. 2008. Estado de Chiapas. Cíclicos y Perennes. Modalidad riego + temporal. (7 Jul 2011). Google Scholar


G. J. Barnett , and B. B. Hunter 1998. Illustrated genera of imperfect fungi. Fourth Edn., St. Paul, MN, APS Press, 218 pp. Google Scholar


O. C. F. Bosa , O. Chávez , L. Torres , A. París L. Villamizar , and Y. A. M. Cotes 2004. Evaluación de aislamientos nativos de Nomuraea rileyi para el control de Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev. Colombiana Entomol. 30(1): 93–97. Google Scholar


B. L. K. Brady 1979. CMI description of pathogenic fungi and bacteria, sets 61 and 62 (No. 601-620), Commonwealth Mycological Institute, Agricultural Bureaux, UK. Google Scholar


P. L Clark , J. Molina-Ochoa S. Martinelli , S. R. Skoda D. J. Isenhour D. J. Lee , J. T. Krumm , and J. E. Foster 2007. Population variation of the fall armyworm, Spodoptera frugiperda, in the Western Hemisphere. J. Insect Sci. 7: 1–10. Google Scholar


J. Fargues , and D. Rodríguez-Rueda 1980. Sensibilité des larves de Spodoptera littoralis (Lepidoptera: Noctuidae) aux hyphomycetes entompathogenes Nomuraea rileyi et Paecilomyces fumosoroseus. Entomophaga 25: 42–54. Google Scholar


W. A. Gardner , and J. R. Fuxa 1980. Pathogens for the suppression of the fall armyworm. Florida Entomol. 63: 439–447. Google Scholar


H. R. Gross , and S. D. Pair 1991. The fall armyworm: status and expectations of biological control with parasitoids and predators. Florida Entomol. 69: 502–515. Google Scholar


J. J. Hamm , S. D. Pair , and O. G. Marti 1986. Incidence of host range of a new ascovirus isolated from fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomol. 69: 524–531. Google Scholar


A. J. Hruska , and F. Gould 1997. Fall armyworm (Lepidoptera: Noctuidae) and Diatraea lineolata (Lepidoptera: Pyralidae): Impact of larval population level and temporal occurrence on maize yield in Nicaragua. J. Econ. Entomol. 90: 611–622. Google Scholar


R. Lezama-Gutiérrez , R. Alatorre-Rosas , L. F. Bojalil-Jaber , J. Molina-Ochoa , M. Arenas-Vargas , M. González-Ramírez , and O. Rebolledo-Domínguez 1996. Virulence of five entomopathogenic fungi (Hyphomycetes) against Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs and neonate lavae. Vedalia 3: 35–39. Google Scholar


Y. Lu , and M. J. Adang 1996. Distinguishing fall armyworm (Lepidoptera: Noctuidae) strains using a diagnostic mitochondrial DNA marker. Florida Entomol. 79: 48–55. Google Scholar


J. Molina-Ochoa , R. Lezama-Gutiérrez , J. J. Hamm , B. R. Wiseman , and M. López-Edwards 1999. Integrated control of fall armyworm (Lepidoptera: Noctuidae) using resistant plants and entomopathogenic nematodes (Rhabditida: Steinernematidae). Florida Entomol. 82: 263–271. Google Scholar


J. Molina-Ochoa , R. Lezama-Gutiérrez , M. González-Ramírez M. López-Edwards , M. A. Rodríguez-Vega , and F. Arceo-Palacios 2003. Pathogens and parasitic nematodes associated with populations of fall armyworm (Lepidoptera: Noctuidae) larvae in Mexico. Florida Entomol. 86: 244–253. Google Scholar


G. M. Murúa , J. Molina-Ochoa , and P. Fidalgo 2009. Natural distribution of parasitoids of larvae of the fall armyworm, Spodoptera frugiperda, in Argentina. J. Insect Sci. 9(20): 1–17. Google Scholar


W. R. Nickle 1972. A contribution to our knowledge of the Mermithidae. J. Nematol. 4: 113–146. Google Scholar


P. N. Patel , and M. E. M. Habib 1988. Protozoosis caused by Vairimorpha necatrix microsporidia Nosematidae in larvae of Spodoptera frugiperda Lepidopera Noctuidae. Rev. Brasileira Zool. 5: 593–598. Google Scholar


C. Ríos-Velasco , E. Cerna-Chávez , S. Sánchez-Peñla , and G. Gallegos-Morales 2010. Natural epizootic of the entomopathogenic fungus Nomuraea rileyi (Farlow) Samson infecting Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila México. J. Res. Lepid. 43: 7–8. Google Scholar


S. W. Ritchie , J. J. Hanway , G. O. Benson , and J. C. Herman 1992. How a corn plant develops, Special Report No. 48, Iowa State University Science and Technology, Cooperative Extension Service. Ames, IA, Scholar


R. E. Ruiz-Nájera , J. Molina-Ochoa , J. E. Carpenter , J. A. Espinosa-Moreno , J. A. Ruiz-Nájera , R. Lezama-Gutiérrez , and J. E. Foster 2007. Survey for hymenopteran and dipteran parasitoids of the fall armyworm (Lepidoptera: Noctuidae) in Chiapas, México. J. Agric. Urban. Entomol. 24: 35–42. Google Scholar


S. D. Sánchez , and C. A. Bellotti 1997. Patogenicidad de hongos Hyphomycetes sobre Cyrtomenus bergi Froeschner (Hemiptera: Cydnidae) chinche subterránea de la yuca. Rev. Colombiana Entomol. 25: 17–21. Google Scholar


A. N. Sparks 1986. Fall armyworm (Lepidoptera: Noctuidae) potential for area-wide management. Florida Entomol. 69: 603–614. Google Scholar


R. R. Vergara 2004. Enfoque agroecológico del empleo de entomopatógenos para el control de piagas. Octavo Seminario de Agroecología, Agromedicina y Medio Ambiente. Tunja, Universidad Pedagógica y Tecnológica de Colombia, 34 pp. Google Scholar


B. R. Wiseman , C. F. Wassom , and R. H. Painter 1967. An unusual feeding habit by the fall armyworm, Spodoptera frugiperda (J. E. Smith). Agron. J. 59: 279–281. Google Scholar


B. R. Wiseman , F. M. Davis , W. P. Williams , and N. W. Widstrom 1996. Resistance of a maize population, FAWCC(C5), to fall armyworm larvae (Lepidoptera: Noctuidae). Florida Entomol. 79: 329–336. Google Scholar
Ramiro E. Ruiz-Nájera, Ramiro A. Ruiz-Estudillo, Juan M. Sánchez-Yáñez, Jaime Molina-Ochoa, Steven R. Skoda, Roberto Coutiño-Ruiz, René Pinto-Ruiz, Francisco Guevara-Hernández, and John E. Foster "Occurrence of Entomopathogenic Fungi and Parasitic Nematodes on Spodoptera frugiperda (Lepidoptera: Noctuidae) Larvae Collected in Central Chiapas, México," Florida Entomologist 96(2), 498-503, (1 June 2013).
Published: 1 June 2013
enemigos naturales
entomopathogenic microorganisms
fall armyworm
Gusano cogollero del maíz
mermithid nematodes
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