New records of Hymenoptera parasitoids of the sesame webworm, Antigastra catalaunalis Duponchel (Lepidoptera: Crambidae), are presented for Northwest Mexico. Taxonomic assignation was based on morphological features. Partial sequences of the COI region from the most common parasitoids were deposited in GenBank. Six species of wasps were obtained: Bracon (Habrobracon) platynotae Cushman (Braconidae), Eiphosoma dentator Fabricius (Ichneumonidae), Perilampus platigaster species group (Perilampidae), Brachymeria annulata Walker, Conura side Walker, Conura maculata Fabricius (Chalcididae) and Goniozus punctaticeps Kieffer (Bethylidae). Partial sequences of the COI region obtained from the most common parasitoids helped to confirm at genus level but not species. This is the first record of the association of all these parasitoid species with A. catalaunalis.

Braconidae, Chalcididae, molecular biology, Sesame webworm

The sesame webworm, Antigastra catalaunalis Duponchel (Lepidoptera: Crambidae), is native in the tropical and subtropical areas of Africa, although it was first reported in South America on sesame crops (Hallman and Sanchez 1982), and it has recently established in North America (Sarazú-Pillado et al. 2020). The second instar larva produces silk with which it binds leaves, branches, and flowers to form a shelter to protect itself from adverse abiotic conditions such as temperature and natural enemies, including parasitoids and predators (Simoglou et al. 2017). It is considered as a pest as it feeds on most parts of the plant except the root, and generally, it attacks the crop since the seedling stage (Gebregergis et al. 2016; Sarazú-Pillado et al. 2020).

Antigastra catalaunalis is a significant pest of sesame in the main producing countries in Asia and Africa. Gupta et al. (2002), reported losses from 6.2 to 43.1% in Madhya Pradesh, India; while Simoglou et al. (2017), in Drama, Northern Greece, reported losses exceeding 50% of production, with 80% of plants infested and 50% of capsules damaged. In South America, this pest was first detected in Colombia in 1971 (Hallman and Sanchez 1982). Recently, according to Sarazú-Pillado et al. (2020), it was found in Sinaloa, the main sesame-producing state in Mexico.

Currently, chemical control is the most widely used tactic against A. catalaunalis. However, its use also results in an imbalance in agroecosystems, environmental contamination, and a negative impact on beneficial fauna. There are 39 species of parasitoids associated with A. catalaunalis (Table 1), some of them are present in India (Jakhmola 1983; Naveen et al. 2019), Tanzania (Robertson 1973), Nigeria (Chadha 1974), and Colombia (Hallman and Sanchez 1982). Although, few of these parasitoids have been proposed for augmentative biological control programs, a strategy that may imply laboratory rearing and periodic mass release of the parasitoid species; for example, Elasmus sp. (Eulophidae) in Vietnam (Tung et al. 2011); Trathala flavoorbitalis Cameron (Ichneumonidae) in India (Baskaran and Thangavelu 1990); and Bracon (Habrobracon) hebetor Say (Braconidae) in Egypt (El-Basha 2015). However, it is necessary to identify, by morphological and molecular taxonomy, parasitoid that could be associated to A. catalaunalis in sesame field in northern Sinaloa, Mexico.

In the present study a total of 77 parasitoid specimens from seven species were obtained associated to A. catalaunalis in commercial sesame fields of Sinaloa. Among these, three species emerged from larvae and four from pupae. The highest number and diversity of parasitoids were found in the municipalities of Sinaloa and El Fuerte, with six species each, while four species were collected in Mocorito. Bracon (Habrobracon) platynotae Cushman (Braconidae) was the most abundant species (39 specimens), followed by Goniozus punctaticeps (Bethylidae) (15 specimens), Conura maculata (Chalcididae) (8 specimens), Brachymeria annulata (Chalcididae) (6 specimens), Eiphosoma dentator (Ichneumonidae) (5 specimens), Conura side (Chalcididae) (3 specimens), and Perilampus platigaster species group (Perilampidae) (one specimen).

When the obtained sequences were compared to the GenBank database, no similarity above 98% was obtained, which could have helped to confirm species. However, for the sequences of E. dentator, the closest match was with a sequence of E. tantalium (JF793018.1) with a 91.32% identity, an E-value of 0.0 and 95% query cover, which confirmed the correct genus identification. For the sequences of B. platynotae, the closest match obtained was 92.24% similarity with a sequence of Habrobracon sp. (MG439564.1), an E-value of 0.0 and 95% query cover, confirming the correct genus identification.

The species complex of parasitoids associated with A. catalaunalis in northern Sinaloa (Fig. 1) could be an important component for the integrated management of this pest in sesame. Below are some details of the collected species.

Figure 1. 

Eiphosoma dentator A female lateral view B male lateral view; Bracon (Habrobracon) platynotae C female lateral view D male lateral view; Goniozus punctaticeps E female lateral view F male lateral view; Brachymeria annulata G female lateral view H male lateral view; Conura side I female lateral view J male lateral view; Conura maculata K female lateral view L male lateral view; Perilampus platigaster species group M male lateral view N male Front view. Scale bars: 1 millimeter.

Bracon (Habrobracon) platynotae Cushman (Braconidae) (Fig. 1C, D) was the most abundant parasitoid species from the three municipalities, except for one collection date in Mocorito, where the parasitoid was absent, possibly due to insecticide application before collection. Up to four parasitoid adults were obtained from a single A. catalaunalis larva, indicating it is a gregarious ectoparasitoid (Table 2). Although it only parasitizes large larvae of the 4^th and 5^th instars, it was observed to cause permanent paralysis and death of small larvae, possibly for feeding, like what was observed with B. hebetor on A. catalaunalis larvae, in Egypt (El-Basha 2015). This species has only been reported in Mexico on Pectinophora gossypiella Saunders (Gelechiidae), under the synonym Microbracon platynotae Cushman, in Durango (Muesebeck 1925). This study reports for the first time B. platynotae as a parasitoid of A. catalaunalis in Sinaloa, Mexico. Given that several species of the subgenus Habrobracon have shown success in biological control programs, B. platynotae would be a viable option for laboratory and field evaluation studies; considering that it also has P. gossypiella as host (Muesebeck 1925).

Goniozus punctaticeps Kieffer (Bethylidae) (Fig. 1E, F) is a gregarious ectoparasitoid of lepidopteran larvae (Evans 1979). It was found in the municipalities of El Fuerte and Sinaloa, with up to four adults obtained from one A. catalaunalis larva (Table 2). The parasitized larvae exhibited permanent paralysis. This parasitoid has been reared in Texas, USA on Acrobasis nuxvorella Neunzig (Pyralidae) and Cidia caryana Fitch (Tortricidae) on pecan (Nickels et al. 1950), also in Coleotechnites (=Evagora) milleri Busck (Gelechiidae), C. (=Lespeyresia) caryana, A. nuxvorella and Etiella zinckenella Treitschke (Pyralidae) also in the USA (Evans 1979). In Mexico, G. punctaticeps (cited as P. cellularis) has only been reported on A. nuxvorella and C. caryana in walnut trees in Nuevo León (Reyes-Villanueva 1987). There are no previous records of Bethylidae species associated with A. catalaunalis, so G. punctaticeps is reported for the first time as a parasitoid on this host in northern Sinaloa, Mexico.

Eiphosoma dentator Fabricius (Ichneumonidae) (Fig. 1A, B) is a solitary ectoparasitoid of lepidopteran larvae (Dasch 1979). It was reared in all three municipalities, but in low numbers (Table 2). A. catalaunalis larvae parasitized by E. dentator exhibited permanent paralysis. It was first reported in Texas, USA, by Mann (1969), parasitizing Loxomorpha flavidissimalis Grote (Crambidae), a potential pest in prickly pear crops. In South Florida, USA, it was found parasitizing Lineodes interga Zeller (Crambidae), a pest of eggplant (Dasch 1979). In Barbados, it is also associated with a pest of the family Crambidae, such as Diaphania hyalinata L. (Alam 1989). Recently, it was also reported in Tamaulipas, Mexico, on L. flavidissimalis (Gaona-García et al. 2020). In this study, E. dentator is reported for the first time as a parasitoid of A. catalaunalis in Sinaloa, Northwest Mexico. In some studies, it is reported without major impact on pest lepidopteran populations (Mann 1969; Dasch 1979; Alam 1989; Gaona-García et al. 2020). However, based on observations in this study, this parasitoid is considered an additional regulatory factor for A. catalaunalis populations in sesame, which could be exploited in conservation biological control programs.

Brachymeria annulata Walker (Chalcididae) (Fig. 1G, H), adults were collected individually from A. catalaunalis pupae, one specimen in El Fuerte, two specimens in Mocorito and three specimens in Sinaloa municipality (Table 2). There exist records of B. annulata parasitizing Talides hispa Evans (Hesperiidae) in Panama (Santos-Murgas et al. 2021); Erinnys ello L. (Sphingidae) in Acre, Brazil, Alabama argillacea Hubner (Noctuidae) in Paraguay (Silvie et al. 2007), and as a hyperparasitoid associated with Diadegma leontiniae Brèthes (Ichneumonidae) in the Brasilia region, Brazil (Guilloux et al. 2002), parasitoid released in cruciferous crops. Brachymeria sp. (Hallman and Sanchez 1982) and Brachymeria nigricorporis (Din-Gurs and Husain 1997) (Table 1) are the only previous records of association between wasps of the genus Brachymeria as parasitoids of A. catalaunalis. In this study, B. annulata is reported for the first time as a parasitoid of A. catalaunalis pupae in Sinaloa, Northwest Mexico.

Three specimens of Conura side Walker (Chalcididae) (Fig. 1I, J) were obtained from A. catalaunalis pupae (Fig. 2I, H), one from El Fuerte and two from Sinaloa. As a primary parasitoid, it has been associated with some species of Chrysomelidae (Coleoptera), such as Gratiana boliviana Spaeth, a beetle released in Florida and other parts of the USA as a biological control agent against Solanum viarum Dunal (Solanaceae) (Diaz et al. 2012). It was also released in Maryland, USA, for biological control of Cassida rubiginosa Muller, a chrysomelid considered an invasive pest and defoliator of some Carduus species (Tipping 1993). As primary parasitoid it was reared from pupae of Anagasta kuhniella Zeller and Galleria mellonella L. (Pyralidae) in Belleville, Canada (Arthur 1958). As a hyperparasitoid it was collected on Campoletis sonorensis Cameron, parasitoid of important pests of maize (Vinson and Iwantsch 1980); also, on Diadegma insulare Cresson on cruciferous pests (Lee and Heimpel 2005).

Figure 2. 

Eiphosoma dentator A larva feeding on an Antigastra catalaunalis larvae B cocoon; Bracon (Habrobracon) platynotae C eggs D larvae on A. catalaunalis larva; E cocoon F Goniozus punctaticeps larvae and cocoon on A. catalaunalis larvae; C. maculata G healthy pupae of A. catalaunalis (below) and pupae parasitized H parasitized pupae; Conura spp. I pupae parasitized by C. side (above) C. maculata (below); C. side J pupae of A. catalaunalis parasitized.

Conura maculata Fabricius (Chalcididae) (Fig. 1K, L) was collected as a solitary parasitoid in A. catalaunalis pupae, with four specimens in El Fuerte and Sinaloa, respectively (Table 2). As a primary parasitoid, it has been reported on chrysalids of Opsiphanes invirae amplificatus Stichel, a pest of palm oil in Argentina (Gervazoni and Arbino 2018), and Rio Grande do Sul, Brazil (Salgado-Neto and Lopes-Da-Silva 2011). Conura maculata has been recorded as a hyperparasitoid on Cotesia rubecula Marshall and C. glomerata L. (McDonald and Kok 1991). This parasitoid species is widely recorded in America, mostly from tropical areas (Delvare 1992). Özdikmen (2011), noted that C. maculata is distributed from Mexico to Paraguay. Recently, Huber et al. (2021), reported the presence of C. maculata in Canada and the USA. Conura (=Spilochalcis) sp. (Hallman and Sanchez 1982) was the only record of association between this genus of parasitoid wasp on A. catalaunalis in Colombia (Table 1). Thus, in the present study, the association of C. side and C. maculata with A. catalaunalis in sesame in Sinaloa, Northwest Mexico, is reported for the first time.

Only one specimen of Perilampus platigaster species group (Smulyan 1936), (Perilampidae) (Fig. 1M, N), was obtained in Mocorito (Table 2). Members of this genus are known to be hyperparasitoids, mainly of Tachinidae (Diptera) and Ichneumonoidea (Hymenoptera) (Darling 1997). This is the first report of Perilampus platigaster species group associated with A. catalaunalis pupae.

The lack of sequences of E. dentator and H. platynotae in the GenBank database, did not allow a molecular confirmation at the species level; however, it helped to confirm the genus, and because these sequences were deposited in this database, they can be used as references in future research on this species.

Among the three species of A. catalaunalis larval parasitoids, only Bracon (Habrobracon) platynotae was more abundant in all three collection sites and throughout the crop cycle (Table 2), with a higher presence in August, consistent with the population peaks of A. catalaunalis. This parasitoid has attributes that could position it as a candidate for mass-rearing studies and for use as a biological control agent. In this study, no apparent hyperparasitism was found on its larvae, nor on the larvae of the other larval parasitoids such as Goniozus punctaticeps and Eiphosoma dentator. The most abundant pupal parasitoids were Conura maculata and Brachymeria annulata. The four wasps reared from pupae also can act as hyperparasitoids of Ichneumonoidea (Hymenoptera) and Tachinidae (Diptera). In this study, all specimens of the families Chalcididae were obtained from A. catalaunalis pupae, and it is very likely that Perilampus platigaster species group is a hyperparasitoid of the collected Ichneumons, due to the background we have on this species group.

The obtained results offer alternatives for using several parasitoid species in an integrated management program for sesame cultivation in Sinaloa, Mexico. This includes the proposal of using B. platynotae as a biological control agent through augmentation, or the use of the parasitoid complex in conservation strategies for beneficial parasitoid and predator fauna.