The fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), native to the Americas, is considered one of the important invasive polyphagous pests. It is prevalent in several countries such as Brazil, Argentina, and the USA (Prowell et al. 2004; Clark et al. 2007), instigating economic losses in a variety of crops such as maize, soybean, cotton, beans (Pogue 2002; Nagoshi et al. 2007; Bueno et al. 2010), rice, other grasses, and a number of weeds (Nabity et al. 2011). Because of its wide host range, S. frugiperda is one of the most harmful pests threatening annual crops in tropical regions (Andrews 1980; Cruz et al. 1999). Severe incidences of fall armyworm were reported from African countries such as Sao Tome, Nigeria, Benin, and Togo in 2016 (Goergen et al. 2016). The incursion of fall armyworm as an invasive pest into Asia was reported for the first time in India by Sharanabasappa et al. (2018), Ganiger et al. (2018), and Shylesha et al. (2018). Recently this pest has been widely reported in many parts of southern and northern India (Mahadeva Swamy et al. 2018). Other species of Spodoptera, such as S. litura (F.), S. exigua (Hübner), and S. mauritia (Boisduval), are major pests of several crops in India with a rich array of indigenous natural enemies. The native bioagents of Spodoptera spp. have an opportunity to expand their niche by parasitizing S. frugiperda, a closely related pest of foreign origin. It is highly probable that the local bioagents may widen their niche by adapting to S. frugiperda, and check its population buildup and further spread. Hence, there is a need to identify the existing natural enemies of fall armyworm in India, which could be used for its management in the future. This study was undertaken to document the natural enemies of fall armyworm, and to record their abundance from different locations in Karnataka and Tamil Nadu in southern India.

Surveys for the occurrence of S. frugiperda were conducted in different maize growing areas of Karnataka and Karur District of Tamil Nadu. An attempt was made at each site, e.g., Shivamogga, Davanagere, Chitradurga, Chikmagaluru, Chamarajanagar, Bellary and Belagavi districts of Karnataka, to collect at least 100 larvae of different stages; however, greater numbers of larvae were collected in only a few locations. In the infested field, feeding injury in the leaf whorl and the presence of fresh frass were used to identify the infestation of S. frugiperda larvae. Larvae were pulled from the whorl and placed in a circular insect breeding dish (Himedia TCP030, HiMedia Laboratories Pvt. Ltd., Mumbai, Maharashtra, India; 90 mm diam, 40 mm height) containing cut maize leaf bits, brought to the laboratory and maintained at 26 ± 2 °C, 75 to 80% relative humidity, and 12:12 h (L:D) photoperiod. These were observed for the emergence of parasitoids; parasitoids emerging from fall armyworm at different stages (larval and pupal) were preserved in 70% ethanol and later identified taxonomically. Larvae from 2 unsprayed maize fields were brought to the laboratory in 25 mL plexiglass vials, and reared individually in the laboratory until the emergence of the parasitoids. Observations were recorded on the number of adult parasitoids that emerged from larvae, and the percentage parasitization and sex ratio were calculated. For the entomofungal pathogens, numbers of field-infected larvae and total larvae were recorded and converted to percentage infection.

In total, we recorded 5 larval parasitoids, 3 predators, and 1 entomopathogenic fungus in our surveys (Table 1), of which 3 parasitoids, namely Coccygidium melleum (Roman) (Hymenoptera: Braconidae) (Fig. 1), Odontepyris sp. (Hymenoptera: Bethylidae) (Fig. 2), and Eriborus sp. (Hymenoptera: Ichneumonidae), are reported for the first time on S. frugiperda in the world. The single female specimen reared from S. frugiperda matched the description of C. melleum by Achterberg (2011). Coccygidium melleum is “common in the Afrotropical region (from South Africa up to Senegal and Somalia) and reaching Yemen and the United Arab Emirates” (Achterberg 2011), but it has not been recorded so far in the Indian subcontinent. Coccygidium spp. (Hymenoptera: Braconidae) are known to parasitize Noctuidae, including Spodoptera spp. (Achterberg 2011). Sisay et al. (2018) reported Coccygidium luteum (Brullé) (Hymenoptera: Braconidae) as a parasitoid of S. frugiperda in Ethiopia. Three species of Coccygidium (C. luteum, C. melleum, and Coccygidium sissoo [Wilkinson]) have been known to parasitize S. exigua (Hübner). This is the first report of C. melleum as a parasitoid of S. frugiperda in the world. We recorded 2 more larval endoparasitoids, Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae) and Eriborus sp. on S. frugiperda in Karnataka. The extent of parasitism by C. chlorideae was 2 to 3% in 2 untreated maize fields monitored at Shivamogga and Davanagere districts of Karnataka. Shylesha et al. (2018) also recorded it on S. frugiperda. Campoletis chlorideae and Eriborus argenteopilosus (Cameron) (Hymenoptera: Ichneumonidae) are responsible for the regulation of 2 major noctuid pests in India, S. litura and Helicoverpa armigera Hübner (Lepidoptera: Noctudae). Both parasitoids attack the host larvae in the first or second instar stage (Bajpai et al. 2006). About 6 species of Campoletis have been known to parasitize S. frugiperda in the Americas and the Caribbean (Molina-Ochoa et al. 2003). Species of Odontepyris are known to be ectoparasitoids of lepidopteran larvae belonging to Noctuidae, Pyralidae, Oecophoridae, and Tortricidae (Lim & Lee 2013), and this is the first report of it as a parasitoid of S. frugiperda. We recorded negligible levels of parasitism of fall armyworm by a tachinid, Exorista sorbillans (Wiedemann) (Diptera: Tachinidae). Predators such as earwigs and coccinellids (Harmonia octomaculata [F.] and Coccinella transversalis [F.]) (both Coleoptera: Coccinellidae) also were found to be active in fall armyworm infested maize fields in the surveyed locations. Harmonia octomaculata and C. transversalis, which were found to be abundant in fall armyworm infested maize fields, may play a significant role in controlling the early stage larvae. Various larger species of Coccinellidae attack caterpillars and other beetle larvae (Hodek et al. 2012), and several genera feed on various insects or their eggs. For instance, in India, Micraspis vincta (reported as Veraniavincta) (Coleoptera: Coccinellidae) was found feeding on the egg masses of S. litura on a groundnut crop (Rajasekhara Rao 1997), and S. exigua on an onion crop (Subba Rao 1998; Sailaja Rani 2004). Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is known to feed on eggs and larvae of S. exigua in China (Liu et al. 2016), and Coccinella sp. is a predator of S. exigua in Vietnam (Chau 1995). Shylesha et al. (2018) recorded earwigs (Forficula sp.) (Dermaptera: Forficulidae) as predators of fall armyworm on maize. The entomofungal pathogen Nomuraea rileyi (Clavicipitaceae), was found to be associated commonly with fall armyworm and caused 10 to 15% larval infection in August.

Table 1.

List of natural enemies of Spodoptera frugiperda in maize ecosystem.

The present study reports new associations of natural enemies with fall armyworm in India. A wide range of parasitoids has been recorded on fall armyworm worldwide as shown by the inventory of parasitoids and parasites of fall armyworm in the Americas and the Caribbean basin that included approximately 150 species of parasitoids and parasites from 14 families (Molina-Ochoa et al. 2003). Our results clearly indicate that native parasitoids of other Spodoptera spp. in India, such as C. chlorideae and E. argenteopilosus, may also adapt to S. frugiperda in due time. It would be worthwhile to evaluate indigenous parasitoids of Spodoptera spp. that known to be effective in India against S. frugiperda. For instance, Telenomus remus Nixon (Hymenoptera: Platygastridae), an effective egg parasitoid of S. litura, is known to parasitize S. frugiperda as well (Molina-Ochoa et al. 2003). Nomuraea rileyi was found to be very effective against S. litura (Padanad & Krishnaraj 2009) in Karnataka.

Further information on the occurrence and rates of parasitism of indigenous natural enemies is of paramount importance in designing a biological control program for fall armyworm, either through conservation of native natural enemies or the introduction of new species for augmentative release. The current blanket recommendation and indiscriminate use of pesticides against the fall armyworm may have a negative impact on natural enemies. Application of insecticides that are less toxic to natural enemies should be encouraged, rather than the continued use of conventional broad-spectrum insecticides, so as to protect natural enemies from the adverse effects of insecticides. The design of more comprehensive IPM programs for fall armyworm management in the region would be a useful strategy.

Fig. 1.

Odontepyris sp.: Larval parasitoid on Spodoptera frugiperda.

Fig. 2.

Coccygidium melleum: Larval parasitoid on Spodoptera frugiperda.