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1 September 2003 PARASITOIDS AND PARASITES OF SPODOPTERA FRUGIPERDA (LEPIDOPTERA: NOCTUIDAE) IN THE AMERICAS AND CARIBBEAN BASIN: AN INVENTORY
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Abstract

An inventory of parasitoids and parasites of fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith), was conducted using references describing parasitized FAW eggs, larvae, pupae and adults collected from different crops or habitats throughout the Americas and the Caribbean Basin. The crops and countries where these parasites were reported occurring in the Americas is also inventoried. Maize was the crop where the FAW was more frequently collected followed by rice. Overall, Chelonus insularis (Cresson) had the broadest natural distribution in the Americas. For the North American region C. insulares, Chelonus sp., and Euplectrus platyhypenae (Howard) were the most relevant parasitoids. In Central America, C. insularis was the most prevalent parasitoid, and in the South American region the most prevalent parasites were Archytas incertus (Macq.), A. marmoratus (Tns.), C. insularis, and Meteorus laphygmae (Viereck). Diapetimorpha introita (Cresson) is the most important pupal parasitoid of FAW occurring mainly in North America. An acugutturid, Noctuidonema guyanense (Remillet & Silvain), is the most important ectoparasitic nematode attacking adults of FAW and other noctuid moths in South and Southeastern US, and Mexico in North America, Caribbean Basin, Central America, and Northern South America.

Biodiversity in agro-ecosystems can be as varied as the crops, weeds, arthropods, and microorganisms themselves, and may differ according to geographical location, climate, soil, and human factors. Experimental evidence suggests that biodiversity can be used for improved pest management (Altieri 1991). A major problem in all areas of agriculture is the lack of basic research on taxonomy of insect pests and their natural enemies. This problem is greatest in tropical countries where the needs are also greater (Claridge 1991). Waage (1991) stated that agricultural systems are generally simpler than the natural habitats from which they are developed. These systems have fewer plant species, fewer primary consumers, and generally fewer natural enemy species. In tropical systems, despite their great biodiversity, natural enemies could be particularly susceptible to local extinction as a result of habitat destruction and unfavorable cropping practices such as indiscriminate use of pesticides (Claridge 1991; Waage 1991).

More than 200 years ago, the fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith), was recognized as a destructive pest of many agricultural crops (Luginbill 1928). In the continental United States the costs for chemical control and losses due to this pest exceeded $300,000,000 during 1977 (Gross & Pair 1986). The biological control of FAW in areas of overwintering and throughout its annual geographical distribution is a highly desirable alternative to conventional control methods (Gross & Pair 1986). Luginbill (1928) and Vickery (1929) recognized the value of parasitoids in reducing larval populations of FAW. Parasitoids and parasites can be highly effective at little or no cost, serve as biotic insecticides in place of chemicals, provide long-term control without the target pest developing significant resistance to them, and impose minimal or no harm to humans or the environment (Wilson & Huffaker 1976; Stary & Pike 1999).

Sivasubramaniam et al. (1997), and Dent (2000) advocated that the first step in any investigation of the role of natural enemies in pest control should involve a field survey to determine which species are present and how their numbers vary in relation to those of the pest insects. Surveys on the FAW parasitoids and other natural enemies in different parts of its range have been conducted because of increasing economic and environmental concerns (Carrillo 1980; Ashley 1986; Castro et al. 1989; Gross & Pair 1991; Cave 1993; Lezama-Gutiérrez et al. 2001; Molina-Ochoa et al. 2001). However, information about distributions and host plants of the FAW and the accompanying parasites and parasitoids are scattered throughout the published literature, and most reviews of FAW parasitoids have emphasized those attacking the egg and larval stages (Ashley 1986). The aim of this paper is to summarize the information and provide an inventory of the known FAW parasites and parasitoids occurring in the Americas and the Caribbean, indicating the host stage attacked, the crops from which parasitized fall armyworm were collected, and the country of collection. In addition, because parasites and parasitoids of the pupal and adult stages of FAW have received little attention in most previous reviews on this subject, we provide an expanded discussion of these natural enemies.

Materials and Methods

Sources of Information

Research was conducted to obtain information, papers, and bibliographic references reporting the collection of parasitized FAW from the field. In the US, we used the Agricola and CAB Abstracts database at the University of Nebraska-Lincoln in Lincoln, Nebraska, and the University of Georgia, Coastal Plain Experiment Station in Tifton, Georgia. We collected references cited in reviews and catalogs of FAW parasites (Guimarães 1971; Marsh 1978; Ashley 1979; Ashley 1986; Andrews 1988) to verify information concerning host plant of parasitized FAW, location of the collected FAW, and stage of FAW attacked. We also used various internet search engines to identify published reports of parasitized FAW collected from the field. In México, we collected papers from Latin American journals and proceedings from meetings of International and Mexican Entomological and Biological Control Societies. Information was also obtained from the libraries in the Facultad de Ciencias Biológicas y Agropecuarias (School of Biological, Agricultural & Animal Sciences) of the Universidad de Colima, and in the Centro Nacional de Referencia de Control Biológico (CNRCB)-Comisión Nacional de Sanidad Agropecuaria-SAGARPA (National Center for Reference on Biological Control) in Tecomán, Colima, México, during 2001 and 2002.

Organization of the Information

The classification (order, family, genus and species) of each parasite and parasitoid collected from FAW is presented in Table 1. The crop from which parasitized FAW were collected, the FAW stage attacked, the country from which parasitized FAW were collected, and the bibliographic references for each record were included in Table 1 whenever the information was available. We preferred to list only original references that report the collection of FAW from the field. Therefore, review articles that contain lists of insects collected by other authors (Guimarães 1971; Marsh 1978; Ashley 1979; Ashley 1986; Andrews 1988) usually are omitted for the entries in Table 1. Because of the quantity involved, all references listed in Table 1 were not cited in the text. Data on FAW parasitoids and parasites from Table 1 have been summarized as the number of species in each taxon reported from different geographical regions (Table 2). Number of species and FAW stage attacked reported from different countries (Table 3), and number of species in each taxon reported from FAW collected from different host plants (Table 4). Omission of pertinent literature from this paper is the authors’ responsibility and was unintentional.

Results and Discussion

A great diversity of parasitoids and parasites of FAW has been reported occurring in the Americas and the Caribbean basin. In this inventory, approximately 150 species of parasitoids and parasites have been recorded from 14 families, nine in Hymenoptera, four in Diptera and one in Nematoda (Table 1). Ichneumonids and braconids were the most diverse families in Hymenoptera, represented by 36 and 28 species, respectively. The most diverse family in Diptera, as well as overall, was Tachinidae with 55 species.

Distribution among the taxa was highly variable. Three of the 14 families were only reported from one country, and five of the 14 families were reported from two or fewer countries. Bethylid and bombyliid parasitoids were only reported in the United States (US) during the 1920s and 1940s (Table 1). Of the ≈150 species, 74 were reported from only one country, and 102 were reported from only one geographical region. In contrast, nine of the 14 families and 18 of the 150 species were reported from all geographical regions (North America, Central America and the Caribbean, and South America), and eight species were reported from 10 or more countries (Table 1 and Table 2).

The number of parasitoid and parasite species reported from each FAW stage attacked in each country is summarized in Table 3. The highest number of parasitoid species attacking FAW larvae was reported from the US (75), followed by Brazil (45), Honduras (43) and Nicaragua (42). Parasitoid species that attack FAW eggs were more prevalent in Nicaragua (11) Brazil (8), Barbados (7) and Mexico (6). Parasitoid species that attack FAW pupae were reported from only 4 countries, with the greatest number of these species collected from the US (6).

Parasitized FAW were collected from 19 different host plants (Table 4). FAW collected from corn were parasitized by species from all families except Bombyliidae. The number of parasite and parasitoid species attacking FAW was greatest for FAW collected from corn (134), sorghum (40), cotton (28), peanut (24), alfalfa (17), rice (13), and Bermuda grass (11). Six of the 14 parasitoids and parasite families were recovered from FAW that had been collected from a single host plant species. Ten of the 14 parasitoids and parasite families were recovered from FAW that had been collected from three or fewer host plant species. The most diverse parasitoid families also were recovered from more FAW host plant species. Tachinids, braconids, eulophids, and ichneumonids were recovered from FAW collected from 15, 11, 8 and 8 FAW host plant species, respectively.

A considerable number of parasitoid species (≈33%) were reported only from one geographical region (Table 1). These findings emphasize the need for more surveys and taxonomical studies of the natural enemies in the different habitats of the natural distribution of the pest (Molina-Ochoa et al. 2001). It is important to consider the different developmental stages of the pest and the growing season of the crop to determine if differences in natural distribution of the parasitoids exist (Ashley 1979; Molina-Ochoa et al. 2001) or if the records related to unique occurrence are due to inadequate surveys. It also is important to determine if the occurrence of FAW parasitoids is associated with the developmental stage of the pest and the host plant. Studies related to tritrophic interactions are needed to elucidate the role of the plant metabolites on the susceptibility of the pest to parasitoids and pathogens, as well as their suitability (Molina-Ochoa et al. 1999). A high diversity of FAW parasitoids has been reported in its natural distribution exerting significant mortality on egg and larval populations. An understanding of induced parasitization of the complex of parasitoids is needed to determine the species with higher capability to attack each stage of the FAW. It is necessary to unite institutional efforts to establish programs of release of FAW parasitoids in overwintering areas and to reduce the migration of the pest northward (Gross & Pair 1986). Because much of the published work does not include environmental data with the collections, we encourage authors to include this information in the future. These data would help select candidate parasitoids for a specific or broad region.

Parasites and Parasitoids of Spodoptera frugiperda Pupae and Adults

Spodoptera frugiperda pupae and adults are attacked by several parasite and parasitoid species. Five species of Ichneumonidae: Diapetimorpha introita (Cresson), Cryptus albitarsis (Cresson), Ichneumon promissorius (Erichson), Ichneumon ambulatorius and Vulgichneumon brevicinctor (Say) have been reported attacking pupae of S. frugiperda and other noctuids (Bechinski & Pedigo 1983; Pair & Gross 1984; Wilson 1983; Pair & Gross 1989; Fitt & Daly 1990; Pavuk & Stinner 1991). Two generalist pupal parasitoids of Chalcididae, Brachymeria ovata (Say) and B. robusta (Cresson), have been collected from S. frugiperda (Wilson 1923; Luginbill 1928; Parker et al. 1953; Ashley 1979; Virla et al. 1999). Only one eulophid species, Trichospilus pupivora (Ferriere), has been reported as a generalist parasitoid of Lepidopteran pupae, including S. frugiperda (Alam 1979, Anantanarayanan 1934). Also, only one species (the ectoparasitic nematode, Noctuidonema guyanense Remillet & Silvain (Remillet & Silvain 1988)), has been observed parasitizing S. frugiperda adults.

Studies on Diapetimorpha introita

Diapetimorpha introita, a parasitoid which attacks FAW in the pupal stage, was reported for first time by Pair & Gross (1984) in Tifton, Georgia. The levels of parasitization in six trials ranged from 0.0 to 23.7%, and the percent of intact pupae that were parasitized during that study averaged 13.5%. Later, Gross & Pair (1986) emphasized the need for more efforts to explore the role of species of parasitoids that employ similar strategies. Pair & Gross (1989) reported the seasonal incidence of D. introita with rates of parasitism that averaged 5.2% (range 0-23.7%) and 8.4% (range 0-50.0%), respectively, during 1983 and 1984, with the highest rate occurring during September to November of each year. Because male D. introita are attracted to chemicals emitted by the female wasps (Jewett & Carpenter 1998) sticky traps baited with live female wasps were used to study the seasonal abundance of D. introita (Jewett & Carpenter 2001). The highest number of adult males was caught during early autumn which corresponded to the rates of parasitism reported by Pair and Gross (1989). As the investigation of their importance to biological control of Spodoptera spp. proceeds, more convenient methods of monitoring D. introita in the field are needed.

Pair (1995) studied the biology and rearing of D. introita on host and non-host noctuid pupae, Spodoptera spp., Helicoverpa zea (Boddie), and Heliothis virescens (F.) to identify factors that influence the reproduction and developmental rate of D. introita. This parasitoid was successfully reared in the laboratory on S. frugiperda pupae. Carpenter & Greany (1998) compared the developmental time, weight, fecundity, longevity, and ability to parasitize hosts for D. introita wasps developing on artificial diet and wasps reared on S. frugiperda pupae. They conclude that the ability to rear D. introita on an inexpensive, artificial diet significantly enhances the potential of mass rearing this parasitoid for inundative releases against species in the genus Spodoptera.

Studies on Ichneumon promissorius and Collection of Ichneumon ambulatorius

I. promissorius was collected in Australia from Helicoverpa armigera (Hübner), and H. punctigera (Wallengren) pupae (Chadwick & Nikitin 1976; Wilson 1983; Fitt & Daly 1990). The parasitoid was imported into the US and released in Arkansas, Georgia, Oklahoma, and Texas from 1992 to 1997 (J. E. C. et al., unpublished data). Following releases of I. promissorius in ear-stage corn in the lower Rio Grande valley in Texas during 1993 and 1994, feral noctuid pupae, including FAW, were removed from the soil. During 1993, 575 FAW pupae were collected, 8 of which were parasitized by I. promissorius. Of the 13 FAW pupae collected in 1994, none were parasitized by I. promissorius. A similar study was conducted in a cornfield in Rabun County, Georgia. During 1993, 141 of the 300 FAW pupae collected were parasitized by I. promissorius and 24 were parasitized by I. ambulatorius, a new host record. Only 5 FAW pupae collected in 1994. Two of these FAW pupae were parasitized by I. promissorius and one was parasitized by I. ambulatorius.

Carpenter et al. (1994) compared several indigenous lepidopteran species in Tifton, GA, for I. promissorius acceptance and development. Pupae of H. zea, H. virescens (F.), H. subflexa (Guenée), S. frugiperda, S. exigua (Hübner), Trichoplusia ni (Hübner), Agrotis ipsilon (Hufnagel), and Anticarsia gemmatalis (Hübner) were used as hosts. Ninety pupae/species were tested, resulting in 74, 72, 68, 66, and 62 wasps emerging from T. ni, A. ipsilon, H. suflexa, S. exigua, and S. frugiperda, respectively. Lowest emergence of wasps was obtained on A. gemmatalis (6). The most acceptable hosts of I. promissorius were H. zea and H. virescens, as expected because I. promissorius was collected in Australia from heliothid species (Fitt & Daly 1990). Carpenter et al. (1994) considered that H. zea should be the primary host species of this pupal parasitoid in the US.

Carpenter (1995) examined the influence of host species, host availability, and mating status on I. promissorius fecundity and oviposition. The results from this study suggest that the females budget their energy expenditures and regulate oogenesis to maximize their reproductive potential. Host size, as well as the host species, may have contributed to differences in weight of the wasps, and contributed to differences in fecundity, longevity, and oviposition between wasps reared on S. exigua and H. zea pupae. Virgin females reared on S. exigua pupae laid fewer eggs than virgin females reared on H. zea pupae.

Studies on Vulgicheumon brevicinctor and Cryptus albitarsis

Two V. brevicinctor were recovered from FAW pupae collected in 1982 from a cornfield near Tifton, GA (Pair & Gross 1989). Five V. brevicinctor were recovered from a sample of 300 FAW pupae collected from a corn field in Rabun County, GA, in 1993, and one V. brevicinctor was recovered from a sample of 3 FAW pupae collected from the same field in 1994 (J. E. C., unpublished data). V. brevicinctor also has been reported from other noctuids and species of other lepidopteran families (Carlson 1979). For example, Bechinski & Pedigo (1983) studied the population dynamics of the green cloverworm (Plathypena scabra F.) in soybeans in Iowa during 1979 and 1980. They and found that V. brevicinctor acted in a delayed density-dependent manner on green cloverworm pupal mortality. Pavuk & Stinner (1991) reported that V. brevicinctor was reared from pupae of an arctiid, Cisseps fulvicollis (Hübner), and pupae from a pyralid, Ostrinia nubilalis (Hübner).

Pair & Gross (1989) collected C. albitarsis in Tifton, GA, from a single sample taken November 2, 1984. Four C. albitarsis also were recovered from a sample of 300 FAW pupae collected from a corn field in Rabun County, GA, in 1993 (J. E. C., unpublished data). Pair & Gross (1989) reported that C. albitarsis had been established in a laboratory colony in Tifton, GA. C. albitarsis cohorts from this laboratory colony were successfully reared on an artificial diet devoid of any host components (Greany and Carpenter 1998).

Studies on Ectopasitic Nematodes Attacking Adults of Spodoptera frugiperda

Remillet & Silvain in 1982 discovered and reported an ectoparasitic nematode, Noctuidonema guyanense Remillet & Silvain infecting Spodoptera androgea (Cramer) in French Guiana. It was subsequently described as a new genus and species (Remillet & Silvain 1988) most commonly found on moths of FAW, Spodoptera latifascia (Walker), S. marima (Schaus), Anicla infecta (Ochsenheimer), and Leucania spp. (Remillet & Silvain 1988).

Rogers et al. (1990a) determined the life cycle and host range for N. guyanense in French Guiana. They collected moths using a white sheet illuminated by UV light, by pheromone traps, and sweeping vegetation from a variety of habitats in Northeastern French Guiana. Moths in five families, Lasiocampidae, Noctuidae, Notodontidae, Pyralidae, and Sphingidae were naturally infested with this nematode species. Twenty-five species of Noctuidae were infected by N. guyanense, the hosts most commonly infected were Lesmone formularis (Hübner), S. dolichos (F.), S. frugiperda, and Xanthopastis timais (Cramer) (Rogers et al. 1990a). Using the same methodologies, Rogers et al. (1990b) determined that multiple species of Mocis and Spodoptera were parasitized by the nematode in Florida and Georgia, and it was the first record of this parasite in North America. Simmons & Rogers (1990a) determined the distribution and prevalence of the nematode in tropical Americas, occurring in northern South America, Mexico, Texas, Florida, Bermuda, most of the Caribbean basin countries, and Central America.

Since 1990, numerous studies have been conducted on this nematode including biology (Simmons & Rogers 1994; Marti & Rogers 2000), pathological effects on the host (Marti et al. 1990; Rogers et al. 1993), infestation dynamics (Rogers & Marti 1992a; Silvain & Remillet 1993; Rogers & Marti 1993b), geographical distribution (Rogers et al. 1993; Rogers et al. 1991; Simmons et al. 1991; Rogers et al. 1997; Marti et al. 2000), ecology (Silvain & Remillet 1993), population profiles (Rogers & Marti 1992a, Rogers & Marti 1994), mating behavior (Simmons & Marti 1992), prevalence (Simmons & Rogers 1990b), maintenance of colonies (Rogers & Marti 1993a, Rogers & Marti 1993b), host range (Simmons & Rogers 1996; Rogers & Marti 1996; Marti et al. 2000), and the bionomics of host insects of N. guyanense (Rogers et al. 1996; Marti et al. 2000). Subsequently however, a study on the speciation in Acugutturidae shows that N. guyanense is limited to the lepidopteran genera Spodoptera and Pseudaletia (Marti et al. 2002).

Simmons et al. (1991) studied the seasonal chronology of the nematode in the tropical and subtropical America, and determined that host parasitism and nematode population density varied among locations and over time. Examples include higher parasitism on male moths in Grenada (77%) than in Texas (1%), and higher nematode populations at lower latitudes than higher latitudes. Simmons & Rogers (1991) also studied the dispersal and seasonal occurrence of N. guyanense on FAW adults in the US. They found that nematode populations and parasitism of FAW males were higher in Eastern States than in the Plains, Midwestern, and Central states, and that the percent parasitism and the number of nematodes per infested FAW changed over time at each location.

Acknowledgments

The authors thank J. J. Hamm and O. G. Marti (USDA-ARS-Crop Protection & Management Research Laboratory, Tifton, GA), for their critical review of earlier versions of this manuscript, and thank O. G. Marti for providing information on ectoparasitic nematodes. The authors appreciate the assistance of Duncan McClusky (University of Georgia Libraries, Tifton, GA), and Marco Antonio Mellín-Rosas (CNRCB, Tecomán, Colima, México) in obtaining scientific literature. The authors gratefully acknowledge and thank Susan Drawdy (USDA-ARS-Crop Protection & Management Research Laboratory, Tifton, GA) for her exceptional technical assistance and dedication to this project. Insect identifications and verification of insect classifications were provided by several scientists associated with the USDA/ARS Systematic Entomology Laboratory, including B. Carlson, E. E. Grissell, P. Marsh, N. E. Woodley, and N. W. Gates. This paper is a contribution of the University of Nebraska Agricultural Research Division, Lincoln, NE 68583. Journal Series No. 13681, Department of Entomology, University of Nebraska-Lincoln. The authors thank Universidad de Colima, and CONACYT-Mexico for supporting the senior author.

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Appendices

Table 1.

Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t101.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t102.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t103.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t104.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t105.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t106.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t107.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t108.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t109.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t110.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t111.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t112.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t113.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t114.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t115.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t116.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t117.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t118.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t119.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t120.gif

Table 1.

(Continued) Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), parasites and parasitoids in the Americas and Caribbean basin with accompanying references indicating family, host stage attacked, crops from which fall armyworm were collected and countries of collection.

i0015-4040-86-3-254-t121.gif

Table 2.

Number of species in each taxon reported from different regions.

i0015-4040-86-3-254-t02.gif

Table 3.

Number of species of parasitoids and stage host attacked reported from different countries.

i0015-4040-86-3-254-t03.gif

Table 4.

Number of parasitoid species in each taxon reported from FAW collected from different host plants.

i0015-4040-86-3-254-t04.gif
Jaime Molina-Ochoa, James E. Carpenter, E. A. Heinrichs, and John E. Foster "PARASITOIDS AND PARASITES OF SPODOPTERA FRUGIPERDA (LEPIDOPTERA: NOCTUIDAE) IN THE AMERICAS AND CARIBBEAN BASIN: AN INVENTORY," Florida Entomologist 86(3), 254-289, (1 September 2003). https://doi.org/10.1653/0015-4040(2003)086[0254:PAPOSF]2.0.CO;2
Published: 1 September 2003
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