The fall armyworm, Spodoptera frugiperda, is a lepidopteran pest that feeds on many economically important cereal crops such as corn, rice, sorghum, and sugarcane. Native to the Americas, it has become a serious invasive pest in Africa and Asia. Recently, this pest was found in China and has spread quickly across the country. As S. frugiperda will most likely become a major pest in China, Integrated Pest Management strategies, including biological control methods, should be developed to manage its populations. Here, we report the detection of Telenomus remus parasitizing S. frugiperda eggs in cornfields in southern China based on morphological and molecular evidence. Our preliminary surveys indicated that the parasitism rates of T. remus on S. frugiperda could reach 30% and 50% for egg masses and per egg mass, respectively. Further application of T. remus against S. frugiperda in biological control programs are discussed.

Scelionidae, egg parasitoid, parasitism rates, biological control

The fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), which originates from tropical and subtropical areas of North, Central, and South America, has become an invasive pest of cereals in Africa, India, Myanmar, Thailand, etc, where it has caused serious damage (Kenis et al. 2019). In China, this species was first detected in the southeast province of Yunnan in January, 2019, and it has quickly spread northward to 17 other provinces (Cui et al. 2019, Jiang et al. 2019). Geographic distribution models have indicated that large parts of China are potentially suitable for the survival of this devastating pest (Lin et al. 2019).

In its native and introduced ranges, S. frugiperda feeds on a wide range of crops. Over 350 different host plants in numerous families have been recorded, and almost 40% of them are economically important (Montezano et al. 2018). It is estimated that, just for corn, rice, sorghum and sugarcane, this pest could cause up to 13 billion USD per annum in crop losses in Africa (Day et al. 2017). Given that corn, sugarcane, and rice are widely grew in southern China, S. frugiperda will most likely establish as a major pest in this region (Wang et al. 2019). Currently, chemical control is still the main strategy against this pest in China, although some biological control experiments using predators (Picromerus lewisi Scott (Hemiptera: Pentatomidae)) have been conducted in the laboratory (Tang et al. 2019). However, in the long run, more biological control strategies should be adopted to against S. frugiperda under the perspectives of Integrated Pest Management (IPM).

Among the ~150 parasitoid species that attack S. frugiperda, the egg parasitoid species Telenomus remus Nixon (Hymenoptera: Scelionidae) appears to be a promising biological control candidate (Kenis et al. 2019) and is reported to attack eggs of various Spodoptera species that are known from China (Chou 1987, Tang et al. 2010). In this study, we report the detection of T. remus parasitizing S. frugiperda eggs and its parasitism rates in cornfields in southern China.

Only one parasitoid species, Telenomus remus (Figure 1D), emerged from the 36 egg masses collected from the three sites. The specimens (Figure 1B, 1C) collected from the three sites show no morphological variation and match well with the holotype (Figure 1A) of T. remus (deposited in British Museum of Natural History, USNM) as well as the description of this species developed by Nixon (1937) and Chou (1987). The COI sequences were identical among females and males sampled from the three collecting sites, and over 99% of the pairs of bases were identical to a series of sequences labeled as T. remus available from the Barcoding of Life Data system and the GenBank database. Phylogenetic analysis based on COI sequences generated from this study and those used by Kenis et al. (2019) showed that the six specimens collected from the three sites of southern China were grouped well within the clade of T. remus specimens collected from Asia, Africa, and the Americas (Figure 2).

Figure 1. 

Telenomus remus Nixon. A Holotype (NHMUK010576395), female, lateral habitus B female (SCAU 3040967), lateral habitus C male (SCAU 3040968), lateral habitus D a female on egg mass of Spodoptera frugiperda.

Figure 2. 

Phylogenetic analysis of Telenomus remus and related species by maximum likelihood method based on COI sequences. The six sequences generated from this study are indicated with codes and GenBank accession numbers (see Table 1). Boostrap values above 50 indicated on branches.

Twenty-eight, five, and three egg masses of S. frugiperda were collected from Huadu, Panyu, and Gaoming, respectively (Table 1). Of the 36 egg masses collected, 11 egg masses (30.6%) were parasitized by T. remus. For the 28 egg masses collected from Huadu, we counted the number of layers of each egg mass, parasitism per egg mass and parasitoid sex ratio in detail (Figure 3 and Table 2). Of the 28 egg masses, one-layer and two-layer egg masses seem to be dominant (13 of each), followed by three-layer egg masses (3). Of the seven parasitized egg masses, six were two-layer and one was one-layer. The number of eggs of each parasitized egg masses ranges from 64 to 163. The number of emerged T. remus adults from these parasitized egg masses ranges from 29 to 87, with 79.2%±2.14 females, resulting in an approximate 50.86%±2.24 parasitism rate per egg mass.

Figure 3. 

Number of layers in Spodoptera frugiperda egg masses.

Both morphological and molecular analyses in this study showed that the Telenomus species we found attacking S. frugiperda eggs in southern China is the promising biological control agent, T. remus. In China, this parasitoid species was reported to attack eggs of other Spodoptera species, including S. litura and S. exigua (Hübner) (Chou 1987, Tang et al. 2010), but its identity was not well established. Both our morphological and molecular data confirmed the presence of T. remus and its parasitism on S. frugiperda eggs in China. Telenomus species are generally small and morphologically simplified, rendering them difficult to distinguish and identify. However, in the case of using T. remus against Spodoptera pests, biological control practitioners should note that the color of the legs is sexually dimorphic (confirmed by COI sequences from both sexes) and not indicative of different species. We recommend that a strategy of integrated taxonomy should be applied to identify Telenomus species, especially in the case of introducing a parasitoid species into a new region for biological control of pests.

Eggs of S. frugiperda are usually laid in masses of approximately 100–200 eggs which are laid in one to three layers on the surface of a leaf (Guo et al. 2019) and the egg mass is usually covered with a layer of scales (setae) from the female abdomen. Our observations showed that S. frugiperda females usually lay one-layer and two-layer egg masses and rarely three-layers in cornfields (Figure 3). Although our current data do not allow us to analyze the preference of different egg masses attacked by T. remus due to small sample size (Table 2), this parasitoid species seems to be able to parasitize multiple-layer egg masses. We observed that even the bottom layer of a three-layer egg mass can be parasitized by T. remus. Determination of how architecture of S. frugiperda egg masses affects parasitism rates of T. remus requires further investigation and is crucial for mass rearing of T. remus.

Studies have shown that T. remus has great potential use in augmentative biological control against S. frugiperda in the field (Cave 2000). Our observations showed that natural parasitism rates of T. remus in corn fields in southern China can reach 30% and 50% for egg masses and per egg mass, respectively. In a study conducted in cornfields in Venezuela, parasitism rates of T. remus on S. frugiperda reached 90% through inundative release in corn cultivation areas (Ferrer 2001). Further research programs, such as long-term monitoring of natural parasitism and mass release in the filed, should be developed for T. remus to evaluate its impact on S. frugiperda populations in China.

We are grateful to David Notton (USNM) for imaging the holotype of Telenomus remus. This study was supported by grants from the Optimization and Popularization of Plant Central Hospital’s Information Platform for Remote Diagnosis and Prevention of Diseases and Pests (2016B080802004) and China Postdoctoral Science Foundation (2019M653187).