The therapeutic approach of killing pest organisms with toxic chemicals has prevailed as a pest control strategy for over 50 years (Lewis et al. 1997). In the 1950s environmental effects of persistent organochlorine insecticides such as DDT began to be observed. Currently, in agricultural pest control, the adverse effects of the use of insecticides are leading scientists to search for alternatives to chemical control of insect pests based on health, environmental, wild life, and economic concerns (Johnson et al. 1998; Mattsson et al. 2000; Solomon & Schettler 2000).

Native insects and pathogens are normal parts of functioning agro-ecosystems and can profoundly influence the agricultural structure, species composition, and diversity. Agro-ecosystems exhibit high biodiversity, mainly influenced by crops, weeds, microorganisms, and arthropods, but these factors are also influenced by geographical location, soil, and climatic characteristics, as well as human factors. Scientific evidence suggests that biodiversity can be used for improved pest management (Altieri 1991). The increased use of beneficial insects and interference with the colonization of fall armyworm in multiple cropping systems have prevented outbreaks in Latin America (Altieri 1994).

The fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith), is a voracious pest inflicting damage to a multiplicity of annual crops in the Americas, and it is commonly controlled with synthetic insecticides, although insecticide resistance has been observed and is a concern (Yu 1991, Yu 1992). Moreover, two strains of FAW have been identified according to their host preference, a corn-associated strain that feeds principally on corn, and a rice-associated strain that feeds primarily on forage grasses and rice (Pashley et al. 1987). Both FAW strains exhibited differences in resistance to chemical and biological insecticides (Adamczyk et al. 1997; López-Edwards et al. 1999), and have differences in their genetic population structure and population ecology (Pashley 1988; Lu & Adang 1996; Bossart & Prowell 1998; Levy et al. 2002; Meagher & Gallo-Meagher 2003; Nagoshi & Meagher 2003). These differences between FAW strains complicate the management of this pest.

Biological control is a highly desirable alternative to insecticides for controlling FAW infestations (Gross & Pair 1986). The value of parasitoids in reducing larval populations of this noctuid has long been recognized (Luginbill 1928; Vickery 1929). In order to develop a better understanding of the natural distribution of the FAW parasitoid complex and natural enemies, surveys have been carried out in different regions of Mexico (Carrillo 1980; Lezama-Gutiérrez et al. 2001; Molina-Ochoa et al. 2001, Molina-Ochoa et al. 2003a).

Here, we report the natural distribution of parasitoids of FAW larvae collected from whorl-stage corn, grain sorghum, forage sorghum, and Sudan grass fields from five Mexican states in the Pacific coast and one state in the Gulf of Mexico, during the summer of 2000.

Materials and Methods

During August and September of 2000, S. frugiperda larvae were collected from whorl-stage corn, grain and forage sorghum, and Sudan grass fields in 64 locations in the Mexican Pacific coast states of Sinaloa, Nayarit, Jalisco, Colima, and Michoacán, and in the Gulf of Mexico state of Veracruz. Egg masses and pupae were not collected.

FAW larvae were individually placed into 30-cc plastic cups with pinto bean diet (Burton & Perkins 1989), and held in the laboratory (Laboratory of Biological Control, Universidad de Colima, Facultad de Ciencias Biológicas y Agropecuarias, Tecomán, Colima, México) for emergence of parasitoids (Molina-Ochoa et al. 2001). Adult parasitoids were placed in 70% ethanol and then submitted to the USDA/ARS Systematic Entomology Laboratory, Beltsville, MD for identification. Collection size ranged from 33 to 119 FAW larvae. The number collected was corrected by subtracting the number that died from injury or unknown causes during the first few days after collection before calculating percent parasitism. Mortality due to pathogens and parasitic nematodes has been previously reported (Molina-Ochoa et al. 2003a).

Collection dates, geographic location, altitude, crop, sample size and total parasitism of FAW larvae in six Mexican states are presented in the Table 1. A Garmin GPS III Plus was used for obtaining the coordinates and altitude data.

Results and Discussion

Out of 5591 FAW larvae collected, 772 produced parasitoids, for a parasitism rate of 13.8%. These parasitoids represented 13 genera from three families of Hymenoptera: six Braconidae, four Ichneumonidae, and three Eulophidae. Nine of the 64 collections produced no parasitoids, six of 12 collections from whorl-stage corn in Michoacán, two of 13 in Jalisco, and only one of 11 in Colima. The highest rates of parasitism in each state were found in C4 (33.3%) in Colima, J12 (21.1%)in Jalisco, M12 (14.4%) in Michoacán, N9 (18.9%) in Nayarit, S5 (27.4%) in Sinaloa, and V4 (11.5%) in Veracruz (Table 1). The most diverse collections of parasitoids were found in the locations C5, J12, and N9 with 5, 4, and 4 species, respectively, (Table 2 and Table 3). The collection from S5 produced the highest rate of parasitism for a single species with 22.1%; the braconid Meteorus laphygmae Viereck was the most common parasitoid collected from Sudangrass. Other parasitoids in that collection were the eulophid Euplectrus plathypenae Howard (2 individuals), and the ichneumonid Ophion flavidus Brulle (1 individual). The braconid C. insularis occurred in 29 of the 64 collections from the six states, and it was the most widely distributed parasitoid. Another important braconid was M. laphygmae, occurring in 21 of the 64 collections. The ichneumonid parasitoids, O. flavidus, and Pristomerus spinator F., occurred in 18, and 17 of the 64 collections, respectively. E. plathypenae was the most important and widely distributed eulophid, occurring in 16 of the 64 collections (Table 2 and Table 3).

Chelonus insularis was the most widely distributed parasitoid of FAW larvae in this survey, occurring in all the six Mexican States, and it was the braconid species with the second highest parasitism rate per location with 16.7%. Thus, C. insularis is one of the most abundant natural enemies of fall armyworm larvae in the Western Coast and Gulf of Mexico. Chelonus insularis has been reported as an important parasitoid controlling FAW populations in the US (Lugingill 1928; Vickery 1929). Ashley (1986) and Andrews (1988) listed C. insularis occurring in Central America and the US, highlighting its role as parasitoid of FAW in southern Florida where 63% of the FAW larvae were attacked. Recently, Molina-Ochoa et al., (2003b) reported C. insularis syn. C. texanus as the braconid with the broadest distribution in Latin America, including South America (Uruguay and Venezuela), the Caribbean Basin (Trinidad and Puerto Rico), and the US. In that inventory Chelonus sp. is also reported in Brazil, Mexico, and Peru. Lewis and Nordlund (1980) emphasized its role considering it as an excellent candidate for the following augmentative approaches: a) release throughout its overwintering zone; b) early-season colonization, and c) direct therapeutic release on target crops.

In a previous survey, Molina-Ochoa et al. (2001) commented on the importance and need of more study in Mexico on the taxonomy of the genus Chelonus (P. M. Marsh, pers. comm.).

Meteorus laphygmae occurred in 21 of the 64 collections. The highest rate of parasitism for a single location was obtained in S5 with 22.1%. This parasitoid occurred in all of the collections from Sinaloa, and the rate of parasitism ranged from 2.1 to 22.1%. Meteorus laphygmae was also collected in Colima, Nayarit, Michoacán, Jalisco, and Veracruz occurring in 45.5%, 30%, 25%, 10%, and 8.3% of the collections, respectively. This braconid was reported by Ashley (1986) occurring in the Continental US, exhibiting its greatest impact on FAW collected from grass. Other reports were made by Alvarado-Rodríguez (1987) in Sinaloa, Mexico attacking Spodoptera exigua (Hübner) infesting tomatoes with a parasitism rate of 9.0%. A similar rate of parasitism was reported by Molina-Ochoa et al. (2001) in a single collection of FAW larvae made in El Mante, Tamaulipas with 10.3%. Molina-Ochoa et al. (2003b) listed several reports from countries of Central and South America, such as Honduras, Nicaragua, Mexico, Chile, Colombia, and Suriname, where M. laphygmae was collected from other crops such as maize, rice, cotton, sorghum, peanuts, and Bermudagrass, and was one of the most prevalent parasitoids in South America.

Low rates of occurrence and parasitization of Cotesia sp. probably marginiventris (Cresson), Glyptapanteles sp. probably militaris (Walsh), Aleiodes sp., and Homolobus sp. probably mellea (Cresson) were recorded. They were found in 5, 2, 1, and 1 of the 64 collections, respectively.

Cotesia sp. occurred in Colima, Jalisco, Nayarit with lower parasitization rates than 2.3%. Similar rates were reported by Molina-Ochoa et al. (2001) in a previous survey conducted in four Mexican States. This parasitoid is reported attacking FAW larvae in Argentina, Brazil, Chile, Honduras, Lesser Antilles, Mexico, Nicaragua, Puerto Rico, Suriname (Molina-Ochoa et al. 2003b), but it has been often reported as a parasitoid of FAW in the US (Ashley 1986) with parasitization rates of 6.3% on FAW larvae collected from maize (Riggin et al. 1993) and from less than 1% to 40% collected from maize and Bermudagrass, respectively (Ashley et al. 1983).

Glyptapanteles sp. was found in Nayarit in two collections, N2 and N4, with parasitization rates of 8.3% and 1.9%, respectively, and in one location in Veracruz (V7) with 1.7% of parasitism rate. Rohlfs & Mack (1985), and Cave (1993) reported the occurrence of this parasitoid attacking FAW larvae in the US and Honduras, collected from sorghum and maize, respectively. Steffey (2001) reported G. militaris attacking armyworms and other caterpillars in Illinois. He speculated that this braconid and other natural enemies could suppress armyworm populations and keep them well below economic levels. Recently, Reis et al. (2003) suggested that the parasitoid may be well adapted to the Azorean agricultural systems in Portugal, characterized by prevalence of the grass, Lolium perenne L., throughout the year. The armyworm, Pseudaletia unipuncta (Haworth) when fed on fresh leaves of L. perenne is the most suitable host for the mass rearing of this braconid.

Aleiodes sp. occurred only in one collection in Nayarit (N2), and Homolobus sp. was found in Michoacán (M3), and their parasitism was lower than 1.2%. Ruíz-Cancino (1991) reported species of Rogas (Syn: Aleiodes) occurring in “La Reserva de la Biosfera El Cielo” in Tamaulipas, Mexico, and the family Braconidae is the second more abundant with 10% of the individuals, these braconids were attacking insect pest of annual, perennial and ornamental crops. Aleiodes laphygmae was reported by Molina-Ochoa et al. (2001) with a low parasitism rate (0.3%) on FAW larvae in Tamaulipas, Mexico. This braconid, A. laphygmae was the most abundant parasitoid attacking FAW larvae (12.8% parasitism) in South Georgia (Riggin et al. 1993).

Homolobus sp. probably mellea (Cresson), syn: Zele mellea (Cresson) was previously found in small numbers attacking FAW larvae in Honduras (Cave 1993), Nicaragua (Huis 1981) and the US (Vickery 1929; Wilson 1933; Riggin et al. 1992), but was not previously reported in Mexico. Parasitism by this species was low (1.1%), but finding it contributes to our knowledge on the occurrence and diversity of beneficial insects affecting FAW populations in Michoacán.

The ichneumonid parasitoids, O. flavidus, P. spinator, and C. flavicincta were the most frequently reared species in 18, 17, and 14 of the 64 collections, respectively. Ophion flavidus was recovered in more locations in Michoacán, and Colima (5 and 4 locations, respectively), but the highest parasitism rate for a single location was obtained in Colima (C7) with 6.7%. Similar results were reported by Molina et al. (2001), and Riggin et al. (1993). Recently, Molina-Ochoa et al., (2003b) listed the occurrence of O. flavidus in Argentina, Brazil, Honduras, Mexico, Nicaragua, and the US. Ashley et al. (1983) reported that Ophion sp. attacked FAW larvae developing on volunteer corn and Paragrass at Homestead, Florida. Gross & Pair (1991) emphasized that the tachinid Archytas marmoratus (Townsend) and O. flavidus provide opportunities for advancing biological strategies for managing FAW, with the development of economical methods for mass-propagation.

P. spinator was the second most widely distributed ichneumonid parasitoid. It was recovered in 17 of the 64 collections, 7 in Colima, 2 in Jalisco, 4 in Michoacán, and Nayarit, but this species was not recovered from Sinaloa, and Veracruz. The highest rate of parasitism for a single location was obtained in Michoacán (M12) with 22.2%. Pristomerus spinator has been reported in Mexico occurring in Quintana Roo, Tamaulipas (Carrillo 1980), and Michoacán, Colima, and Jalisco (Molina-Ochoa et al. 2001). Two collections from Michoacán during 1998 and 2000 exhibited the highest parasitism rates for a single location (El Hueso, and El Cirián, Nueva Italia) with 12.7%, and 22.2%, respectively. The ichneumonid was previously reported from Brazil, Honduras, Mexico, Nicaragua, and the US (Molina-Ochoa et al. 2003b).

Campoletis flavicincta was found in 14 of 64 collections, one in Colima, 5 in Jalisco, 3 in Michoacán, and 5 in Nayarit, but it was not recovered in Sinaloa, and Veracruz. Campoletis flavicincta had an overall parasitism range from 0 to 3.3%. The highest parasitism rate for a single location was obtained in N9. In a previous survey conducted by Molina-Ochoa et al. (2001), C. flavicincta accounted for 23% of parasitism in El Batillero, Michoacán, a location surrounded by avocado orchards and pine forest near to Apo, Michoacán; however, the FAW larvae from nearby locations in this survey (M1 and M2) showed low parasitism rates (3.3%, and 2.2%, respectively) by this parasitoid. It appears that, C. flavicincta, prefers or was associated with locations with high altitude; in this survey, it was found in locations with altitudes with an average of 1417 meters, as well as in locations near forests mainly constituted with pine and oak trees. Molina-Ochoa et al. (2003b) reported C. flavicincta occurring in Brazil, Honduras, Mexico, Nicaragua, and the US. This species was also reported attacking beet armyworm larvae fed on cotton in Georgia, USA (Ruberson et al. 1993, Ruberson 1994).

Eiphosoma vitticole was the ichneumonid with the most limited distribution in this survey, found in 6 of the 64 collections. E. vitticole occurred in 2 locations in Colima, 3 locations in Michoacán, and 1 location in Nayarit. The highest rate of parasitism for a single location was recorded in M12 with 5.6%. This species showed low parasitism rates, and it was not found in Jalisco, Sinaloa, and Veracruz. It was collected from locations with an average altitude of 472m, with a range between 255 and 744m. Pair et al. (1986) reported the occurrence of E. vitticole in Texas, and Tamaulipas, Mexico. It also has been reported from Bolivia, Brazil, Colombia, Honduras, and Nicaragua (Molina-Ochoa et al. 2003b)

Three species of eulophid parasitoids were found in this survey, Aprostocetus sp., Euplectrus plathypenae Howard, and Horismenus sp. Euplectrus plathypenae was the most widely distributed eulophid, occurring in 16 of the 64 collections. It was found in Veracruz in all collections (10), Sinaloa in 3 collections, 2 in Michoacán, and one in Jalisco. Molina-Ochoa et al. (2001) reported a parasitism rate of 8.3% by E. plathypenae in a single collection in El Mante, Tamaulipas, similar rates in several locations in Veracruz, and low rate of about 1% in Michoacán. We also did not find levels higher than 1.6% in Michoacán; however, we found a range of parasitism in Sinaloa between 1% and 4.2%. The highest level of parasitism for a single location was obtained in the location V4 with 11.5%. Montoya-Burgos (1980) reported natural parasitism of about 15% by Euplectrus sp. against L2 FAW developing on corn in Veracruz. Euplectrus plathypenae is an important and well distributed parasitoid in the tropical Americas, and the US (Molina-Ochoa et al. (2003b).

The other eulophids, Aprostocetus sp. and Horismenus sp., occurred only in the location V2, with a parasitism rate of 3.0% for both species. This is the first report of Aprostocetus sp. and Horismenus sp. as parasitoids of FAW larvae. Aprostocetus sp. has been reported as a hyperparasitoid of Gelechia senticetella (Stgr.) (Lepidoptera: Gelechiidae) fed on Juniperus excelsa in Bulgaria (Mirchev et al. 2001). Aprostocetus sp. also was reported as an egg parasitoid of mango leafhoppers (Fasih & Srivatava 1990). Aprostocetus diplosis Crawford is a parasitoid of Stenodiplosis sorghicola, a dipterous pest of sorghum in Brazil (Campos et al. 1998). Horismenus sp. has been reported to be a parasitoid of prepupae and pupae of the Citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Mexico (Perales et al. 1996, Bautista-Martínez et al. 1998). Coffelt & Schultz (1993) mentioned that it is very common to find species of this genus acting as hyperparasitoids.

Our results demonstrate that hymenopteran parasitoids of FAW differentially occurred throughout the six Mexican states surveyed. However, this may have been influenced by the size of the FAW larvae collected. The hymenopteran parasitoids caused significant mortality of FAW larvae in most of the localities of this survey. It is important to highlight the occurrence and role on the FAW larval mortality caused by the braconids, C. insularis, and M. laphygmae, the ichneumonids, O. flavidus, P. spinator, and C. flavicincta, as well as the eulophid E. plathypenae. Our findings agree with Ashley (1986) in that no single parasitoid species exerted significant mortality throughout a major portion of the range of FAW. Another important aspect to note is the need for more taxonomic studies on two genera, Chelonus and Meteorus, which are important sources of mortality for FAW larvae.