Prerpints.org logo
Preprint
Article

Revisiting Classical Biological Control Through the New Associations Between the Invasive Pest Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) and Local Parasitoids

Altmetrics

Downloads

405

Views

264

Comments

0

supplementary.xlsx (16.01KB )

Submitted:

30 October 2023

Posted:

31 October 2023

Read the latest preprint version here

Alerts
Abstract
Spodopotera frugiperda is a worldwide invasive pest that has caused major economic damage. According to classical biological control theory, natural enemies that can control invasive pests come from the area of origin as the pests that have gone through coadaptation processes. Our study, however, suggests that new associations between S. frugiperda and local natural enemies offer insights into the possibilities of biological control using local parasitoids. The research was conducted through a rapid survey in Yogyakarta, Indonesia, covering four districts in Sleman, Bantul, Gunung Kidul, and Kulon Progo from September 2019 to June 2022. The results showed a stable increase of parasitoid species richness found yearly, with 15 parasitoid species associated with S. frugiperda. Four egg parasitoids, eight larval parasitoids, and three pupal parasitoids were found to be associated with S. frugiperda for three years after it was first discovered in Indonesia. Telenomus remus is the most dominant parasitoid, with a higher abundance and parasitism rate than other parasitoids. A new association was found between S. frugiperda and twelve parasitoid species, consisting of three egg parasitoids (Telenomus remus, Hymenoptera sp.1 and Hymenoptera sp.2), six larval parasitoids (Apanteles sp., Microplitis sp., Campoletis sp., Coccygidium sp., Eupelmus sp., and Stenobracon sp.), and three pupal parasitoids (Brachymeria lasus, B. femorata, and Charops sp.). This study also reported the first findings of the association of S. frugiperda with the larval parasitoid Megaselia scalaris in Indonesia. The result suggests the revisit of classical biological control and that local natural enemies can foster quick adaptation to invasive pests.
Keywords: 
Subject: Biology and Life Sciences  -   Insect Science

1. Introduction

The appearance of invasive pests is a problem that requires attention because it may threaten agriculture and the variety of local species [1] and cause biotic homogenization [2]. Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae) is an invasive pest from America. It has become a new pest in Indonesia since early 2019 [3]. This pest has a wide range of distribution. It has now spread to 32 provinces in Indonesia, including Sumatra [4], Java [5], Kalimantan [6], and Sulawesi [7]. Spodoptera frugiperda infestations should be severely considered since a population of 0.2 to 0.8 S. frugiperda larvae/plant can decrease maize productivity by 20 to 50% [3]. Reports of damage due to S. frugiperda have been reported in several countries, such as Ethiopia and Kenya (32 - 47%) [8], Zimbabwe (32 - 48%) [9], Ghana (22 - 67%) [10], and Indonesia (60%) [11]. Spodoptera frugiperda has reportedly replaced the position of Asian corn borer Ostrinia furnacalis Guenée (Lepidoptera: Crambidae) as the primary pest of maize in China [12]. Rizali et al. [2] mentioned that the presence of S. frugiperda significantly decreases the intensity of attack of other lepidopteran pests and indirectly causes negative effects on the diversity of their natural enemies (particularly predators) in different maize fields in Indonesia.
Several studies have been reported since S. frugiperda was first reported in Indonesia. The studies were mostly focused on the presence/absence, diversity, infestation level, and ecology of S. frugiperda [5,13,14,15,16]. Research on the performance of local parasitoid species in Indonesia in parasitizing S. frugiperda on a lab scale has even been reported [17,18]. Surveys on the infestation level of S. frugiperda, the association between S. frugiperda with local parasitoids, and its associated parasitism rate have also been carried out but limited within a specific period [2,5,19,20,21,22,23,24,25,26,27,28]. Preliminary research in Yogyakarta, Indonesia, showed a low attack rate from local parasitoids toward S. frugiperda [29]. Thus, there is scattered information regarding the possibility of a new association between S. frugiperda and local parasitoids.
According to classical biological control theory, invasive pest control can be carried out by importing parasitoids from the original habitat of the pest, which have been proven as potential biological agents [30]. For example, the introduction of Rodolia cardinalis Mulsant (Coleoptera: Coccinellidae) to control the cotton aphid, Icerya purchasi Maskell (Hemiptera: Margarodidae) in California [31], and the introduction of Urophora affinis Frauenfeld and U. quadrifasciata Meigen (Diptera: Tephritidae) to control spotted knapweed Centaurea maculosa Lam. and C. diffusa Lamarck in western North America [32]. In Indonesia, the introduction of biological control agents was also carried out several times, such as the introduction of Curinus coeruleus Mulsant (Coleoptera: Coccinellidae) from Hawaii to control Heteropsylla cubana Crawford (Hemiptera: Psyllidae) on mimosoid tree Leucaena leucocephala [33], the introduction of Anagyrus lopezi De Santis (Hymenoptera: Encyrtidae) from Thailand to control cassava mealybugs Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) [34], and the introduction of Cecidochares connexa Macquart (Diptera: Tephritidae) from Columbia to control the invasive species - siam weed Chromolaena odorata L. [35].
The latest example provides important information that 28 years after introduction, C. connexa has been reported to be associated with several local parasitoid species [36,37,38,39]. Another example is the association between leaf miner Liriomyza spp. and local parasitoids in Indonesia. Liriomyza spp. is an invasive pest found in Indonesia from America in the 1990s [40]. Liriomyza spp. was reported to be associated with 11 parasitoid species in 2000 [41], and in 2022, Liriomyza spp. was associated with 18 local parasitoid species [42]. These findings support Hokkanen and Pimentel’s old hypothesis [43] on the possibility of new associations that can be formed between herbivores and their local natural enemies. Therefore, this research aimed to study the diversity of parasitoids associated with S. frugiperda for three years after it was first discovered in Indonesia. This is important to study as an effort to prepare local biological agents potentially to be used in controlling S. frugiperda in the future.

2. Materials and Methods

2.1. Sampling Location Determination

Sampling locations were determined using a stratified random sampling method in four central districts in Yogyakarta, including Sleman, Bantul, Kulon Progo, and Gunung Kidul. Parasitoid sampling activities were carried out in all sub-districts in each district. A total of 2-3 villages were selected from each sub-district as sampling points. From each village, a maize field was chosen as a sampling point using GPS Essentials (mictale.com), resulting in 143 sampling points (Figure 1, Supplementary file). Sampling of parasitoids was carried out on maize fields during the vegetative phase (2-3 weeks old) because the highest S. frugiperda infestation occurs at this stage [13].

2.2. Sampling

The survey was carried out from September 2019 to June 2022. Sampling was carried out once on each field. Parasitoids were collected by collecting hosts (eggs, larvae, and pupae) of S. frugiperda, found on maize plants in every field. Sampling was carried out purposively by taking eggs, larvae, and pupae found. The samples obtained were brought from the field to the laboratory using an insect-rearing plastic container (21 x 21 cm) and then kept individually in plastic cups (400 ml) until moths or parasitoids appeared under laboratory conditions (26±1 °C, 60-80% r.h.). Parasitoids that appeared were counted, recorded, and grouped based on similar morphological characteristics, then preserved in a 1.5 ml microtube filled with 70% ethanol for further identification.

2.3. Parasitoid Identification

The parasitoids that appeared were identified at the Plant Protection Laboratory, Department of Agrotechnology, Universitas Muhammadiyah Yogyakarta. Identification of parasitoids was carried out by observing and matching the morphological characteristics of the parasitoids with some relevant literature [23,44,45,46]. The identified parasitoids were then documented and measured using TrueChromeII, TCapture 5.1 software (Fuzhou Tucsen Photonics Co., Ltd., China), and a Leica S6E Stereo Microscope (Leica Microsystems, Germany) at the Biological Control Laboratory, Department of Plant Protection, Faculty of Agriculture, IPB University. All identified parasitoids were confirmed at the Ecology and Systematics Laboratory, Faculty of Applied Science and Technology, Ahmad Dahlan University.

2.4. Data Analysis

The diversity (species richness and abundance) and parasitism rate of S. frugiperda parasitoids were tabulated using a pivot table on Microsoft Office Excel 365. Parasitoid distribution was mapped based on sampling points (regional administrative data) using ArcGis 10 (ESRI, Environmental Systems Research Institute, California, USA).

3. Results

The results showed that 15 species of parasitoids were associated with S. frugiperda. 80% (12/15) of the parasitoids discovered were new associations (Table 1). Four species were egg parasitoids, eight were larval parasitoids, and three were pupal parasitoids. The egg parasitoids found were Hymenoptera sp.1 (Figure 2a), Hymenoptera sp.2 (Figure 2b), Trichogramma sp. (Figure 2c), and Telenomus remus (Figure 2d). The larval parasitoids found were Hymenoptera, such as Apanteles sp. (Figure 3a), Campoletis sp. (Figure 3b), Coccygidium sp. (Figure 3c), Eupelmus sp. (Figure 3d), Microplitis sp. (Figure 3e), Stenobracon sp. (Figure 3f), and Diptera such as Archytas marmoratus (Figure 4a) and Megaselia sp. (Figures 4b). Based on its morphological characteristics, we confirmed that the last Dipteran species is M. scalaris (Figure 5). Meanwhile, the pupal parasitoids found were Brachymeria femorata (Figure 6a), Brachymeria lasus (Figure 6b), and Charops sp.
However, not all parasitoid species were found in every location. Eight species of parasitoids were found in Bantul, seven in Sleman, six in Gunung Kidul, and only three in Kulonprogo. The richest and most abundant species of parasitoids were found in Bantul (8748 parasitoids). This amount is far higher than in other places. Two thousand seven hundred forty-eight parasitoids were obtained in Sleman, 924 in Gunung Kidul, and 494 in Kulon Progo (Table 1).
Based on a mapping analysis of the parasitoid species distribution found in the field, S. frugiperda has spread almost throughout the Yogyakarta region (Figure 7A). Telenomus remus was the most dominant parasitoid because of its abundance. However, T. remus was only distributed in a few areas (Figure 8), with the highest abundance found in Bantul.
In addition to its high abundance, T. remus had the highest parasitism rate (26-87%). Other parasitoids such as Hymenoptera sp.1, Campoletis sp., Coccygidium sp., and Microplitis sp. had maximum parasitism rates of 12.81%, 12.69%, 17.54%, and 19.84% respectively. Apanteles sp. had a parasitism rate of 2-30%. The parasitism rate of other parasitoids occurred at lower rates, such as Stenobracon sp., Brachymeria femorata, and B. lasus, with 1 – 2% parasitism rate. Meanwhile, the other parasitoids, including Hymenoptera sp.2, Megaselia scalaris, Archytas marmoratus, and Charops sp., had a less than 1% parasitism rate (Figure 9).
Periodically, only one parasitoid was found associated with S. frugiperda in 2019. The number of parasitoid species associated with S. frugiperda increased to eight, thirteen, and fifteen species in 2020, 2021, and 2022, respectively (Table 2).
Preprints 89072 g009
Figure 9. Parasitism rate of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Figure 9. Parasitism rate of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Preprints 89072 g009

4. Discussion

A survey was conducted to study the diversity and the new associations between S. frugiperda and local parasitoids in the Special Region of Yogyakarta for three years after S. frugiperda was discovered in Indonesia to revise from the old to the new association biological control theoretical approach.
Classical Biological Control emphasizes old associations that invasive pests are controlled by the natural enemy from the country of origin because local natural enemies cannot control the invasive pest [30]. Meanwhile, a new association between invasive pests and local natural enemies will not result in suppression/regulation of the pest because adaptation will take too long. In fact, a physiological equilibrium that results from coevolution between a parasitoid and its hosts might prohibit such long-associated parasitoids from acting as efficient biological control agents [47]. Adaptation can happen relatively quickly, as we found during this study. Elton [48] said that when a parasite species is introduced into an ecosystem with a host or hosts it has never been associated with, the parasite population often rises quickly, often to outbreak levels, and its host population is suppressed.
Our research shows an increase in the number of parasitoids associated with S. frugiperda. These findings indicate a similar pattern in other areas of Indonesia. For example, one parasitoid (T. remus) was found to be associated with S. frugiperda at the beginning of survey activities in 2019. According to Jindal et al. [49], no parasitoids were seen in India in 2019 because S. frugiperda had just recently infected the crop in the late season. Maharani et al. [5] also reported no parasitoids directly associated with S. frugiperda in Bandung and Garut, West Java, Indonesia in 2019.
However, A. marmoratus and Hymenoptera larvae were found from Mythymna separata obtained from the same field where S. frugiperda was collected. Furthermore, Pu’u and Mutiara [50] reported no parasitoids associated with S. frugiperda in Ende, East Nusa Tenggara, in 2020. Suroto et al. [24] reported one parasitoid (Apanteles sp.) associated with S. frugiperda in Banyumas, Central Java, in 2021. Then, Minarni et al. [21] reported the association of S. frugiperda with one egg parasitoid (T. remus) and three larval parasitoids from the Braconidae, Ichneumonida, and Chalcididae families in the same location in 2022.
Based on the abundance of parasitoids, this study also showed differences in the abundance found in the four districts in Yogyakarta. The area with the highest abundance of parasitoids was Bantul. This is due to the characteristics of the sampling site, where Bantul Regency serves as Yogyakarta’s primary maize-producing hub [51], making hosts (S. frugiperda) more accessible than in other districts. Kishinevsky et al. [52] said that an individual parasitoid would be more prevalent in a site if its host population is more numerous, as are its hosts.
Some parasitoids are similar to those found in the Western Hemisphere, while others differ. Chelonus insularis (Hymenoptera: Ichneumonidae) is identified as the primary parasitoid of S. frugiperda in most investigations conducted in North, Central, and South America. However, Eiphosoma laphygmae (Hymenoptera: Icheumonidae) is more recommended as a prospective candidate for introduction because of its specificity and significance as a parasitoid of the pest across most of its natural habitat [53]. These two parasitoids were not discovered during our research. They were not associated with S. frugiperda in other investigations, including those conducted in Cameroon [54] and India [55].
The most prevalent parasitoid identified in this investigation is T. remus. This study reported similar results from other investigations [56,57], where T. remus was the dominant parasitoid for S. frugiperda because this parasitoid has a high abundance and parasitism rate (26-87%). Kumela et al. [8] also reported that T. remus was a parasitoid of S. frugiperda eggs, with the highest parasitism rate (69.3%) in Kenya and Southern China (30-50%) [57]. Sari et al. [17] reported the potential of T. remus as a biological agent of S. frugiperda in Indonesia, with a parasitism rate of 69.40%. This value is quite comparative compared to other egg parasitoids such as T. chilotraeae [58]. The parasitism rate of T. remus may be higher in a situation with many potential hosts. Junaedi et al. [59] said that the availability of hosts for parasitoid survival could increase the parasitism rate. During sampling in the field, the population of S. frugiperda eggs was abundant. The high parasitism rate is also due to T. remus’ ability to find and recognize its host [60]. Goulart et al. [61] said that the ability of T. remus to search and recognize its hosts is better than other S. frugiperda egg parasitoids such as Trichogramma pretiosum.
Telenomus remus is a native egg parasitoid from Malaysia and Papua New Guinea [62]. Telenomus remus is a common egg parasitoid used to control pests in the Noctuidae group, especially the Spodoptera genus [63]. Telenomus remus has been introduced to many countries, including America [63], despite having little success in controlling S. frugiperda [64]. In contrast to studies in Indonesia and other countries like Africa (Benin, Cameroon, Côte d’Ivoire, Ghana, Kenya, Niger, Nigeria, Uganda, South Africa, Tanzania, and Zambia) and Asia (China, India, and Nepal) [65] which claimed that T. remus is a potential biological control agent for controlling S. frugiperda. This could occur because S. frugiperda is not native to these regions. When a parasitoid can attack a new host species, the host typically suffers greatly [66]. In contrast to America, the existence of other parasitoids cannot successfully control S. frugiperda because they have evolved to its original natural enemies, making it resistant to effective control by other parasitoids [47].
Other egg parasitoids found were Hymenoptera sp.1 and Hymenoptera sp.2. Morphologically, these two parasitoid species are different from T. remus, even though they both come from the Platygasteridae family, and these parasitoids are characterized by eight flagellum segments and a wider second metasoma segment, different from T. remus, which has dilation in the third metasoma [67]. Unfortunately, due to minimal sample conditions, identification could not be carried out to the genus level. Platygasteridae was found, with a lower abundance than T. remus. This might happen because the two are not the primary parasitoids of S. frugiperda eggs. Hymenoptera sp.1 has a similar morphological character to Platygaster oryzae, the main parasitoid of Asian rice gall midge Orseolia oryzae [68]. However, Hymenoptera sp.1 species could not be confirmed, even though this parasitoid emerged from the rearing of S. frugiperda egg clusters collected from maize fields adjacent to rice fields. Meanwhile, Hymenoptera sp.2 has a different body color from P. oryzae. Platygaster oryzae has a metallic black body color [69,70], while the parasitoids found were a bright yellow. The discovery of two different egg parasitoid species from T. remus and Trichogramma indicates the existence of two new associations between S. frugiperda and local egg parasitoids.
Another new association has been found between S. frugiperda and larval parasitoids from Hymenoptera order, including Apanteles sp., Microplitis sp., Campoletis sp., Coccygidium sp., Eupelmus sp., and Stenobracon sp. All of these parasitoids are present in the Western hemisphere. However, Apanteles like A. ruficrus imported from the Australia [71], M. manilae from the Thailand [72], and C. chloridae from the India [73] to the US. Apanteles sp. is a larval parasitoid with the highest parasitism rate (2-30%) compared to other S. frugiperda larval parasitoids. Supeno et al. [23] and Suroto et al. [24] also reported the incidence of parasitism of Apanteles on S. frugiperda larvae with a 17 - 22% parasitism rate, higher than other S. frugiperda larval parasitoids. Moreover, Microplitis also has a significant parasitism rate (0.5 – 19.84%). The genus Microplitis, reported as a larval parasitoid of S. frugiperda, includes M. manilae [72]. Microplitis is a genera widely distributed throughout all biogeographic zones, with macrolepidopterans as their primary hosts [74]. The results of this study also indicate that Apanteles and Microplitis are parasitoids of S. frugiperda larvae potentially developed as biological agents. Association of S. frugiperda larvae with Apanteles and Microplitis was also reported from Bogor, West Java, with 0.39 and 12.3% parasitism rates, respectively [75]. Surprisingly, Stenobracon sp. and Eupelmus sp. have never been found in the western hemisphere or elsewhere. Meanwhile, Coccygidium sp. is reported from other regions. Campoletis and Coccygidium had 0.2-12.69% and 0.2-17.54% parasitism rate, respectively. Campoletis has also been reported in India, with a 2-4% parasitism rate [55]. Meanwhile, Coccygidium was also reported in India, with a 0.001% parasitism rate [55], and in Ghana, with a 3.9-19.3% parasitism rate [44].
Apart from the Hymenoptera order, there were also S. frugiperda larvae parasitoids from the Diptera order, such as Archytas marmoratus and Megaselia scalaris. Archytas marmoratus is a potential parasitoid for S. frugiperda in the American field [76]. However, the parasitism rate found in this study was very low. The parasitism level of M. scalaris was also very low. Megalia scalaris was first reported in Asian regions, including India [77] and China [78]. Megalia scalaris was also found in the Mexican region [79]. This finding is also the first report of an association between S. frugiperda and M. scalaris in Indonesia. Megaselia scalaris is an insect found in various regions, usually in decaying organic matter [80]. Besides being reported as a larval parasitoid of S. frugiperda, M scalaris was also reported to be associated with peach fruit fly, Bactrocera zonata (Saunders), Mediterranean fruit fly, Ceratitis capitata (Wiedemann) in Egypt [81], and fruit-piercing moths Thyas coronota (Fabricius) (Lepidoptera: Erebidea) in India [82]. However, according to a recent study, M. scalaris is not recommended as a potential biological control agent for S. frugiperda. Megaselia scalaris prefers to consume deceased larvae instead of acting as an endoparasitoid with parasitism rates of 2.2 and 0.7% in third- and fifth-instar larvae of S. frugiperda, respectively [83].
Besides the new association between S. frugiperda and several egg and larval parasitoids, there was another new association with three pupal parasitoids, such as Brachymeria lasus and B. femorata from the Chalcididae family, and Charops sp. from Ichneumonid family. Because these parasitoids also have never been documented in the western hemisphere. Several chalcidid families reported to be associated with S. frugiperda include B. flavipes (= robusta) (Fabricius), B. ovata (Say), Conura femorata (Fabricius), C. hirtifemora (Ashmead), C. igneoides (Kirby), C. immaculata (Cresson), and C. meteori (Burks) [84]. These two S. frugiperda pupal parasitoids were only found in Bantul. Brachymeria lasus and B. femorata usually attack hidden insects, such as the banana leafroller caterpillar Erinota thrax (Lepidoptera: Hesperiidae) [85], fire caterpillars, and other Noctuidae families. The proximity of banana plants to the sampling site in Bantul Regency suggests that there may be other hosts for these parasitoids. However, these two parasitoids have also been found parasitizing the pupae of S. frugiperda in Egypt [86]. Lastly, Charops sp. was identified through its pupal characteristics. Charops sp. was also reported as a pupal parasitoid of S. frugiperda in Cameroon [87], Ghana, and Benin [54] but has never been reported from the western hemisphere as well.
Our findings support Hokkanen and Pimentel’s theory on using the New Association biological control approach for controlling S. frugiperda with local parasitoids such as T. remus and Microplitis sp. Telenomus remus has been used as a biological agent for S. exigua [88], and Microplitis manilae has also been around for a long time and is associated with other Spodoptera species, such as S. litura in Indonesia [89]. This evidence led us to conclude that these parasitoids existed earlier than S. frugiperda in Indonesia. Hokkanen and Pimental [43] also said that the original host of the most effective new association biocontrol agents is closely connected to the new host of the agent was introduced against. The original and subsequent hosts have typically belonged to the same genus. Longer taxonomic ''jumps'' to a new host from distinct families of hosts are also feasible, as exemplified by a pupal parasitoid B. lasus. Therefore, T. remus and Microplitis sp. are thus possible biological control agent options for use in control initiatives within the new association of biological control concepts equipped to regulate S. frugiperda.

5. Conclusions

This research supports Hokkanen and Pimentel’s theory of using the new association biological control approach for controlling S. frugiperda. In contrast to Kenis [53], who recommends a classical biological control approach since introducing natural enemies may lead to an environmental risk. Telenomus remus is the most dominant parasitoid with a high abundance and parasitism rate compared to other parasitoids. Telenomus remus is a promising opportunity because T. remus is an egg parasitoid. Parasitoids can control pests early in life, thereby avoiding further attacks.

Supplementary Materials

The following supporting information can be downloaded at the website of this paper posted on Preprints.org.

Author Contributions

Conceptualization, I.N., I.L.I.P. and D.B.; methodology, I.N., I.L.I.P. and D.B.; software, I.N. and F.S.; validation, I.N., I.L.I.P. and D.B.; formal analysis, I.N., I.L.I.P. and F.S.; investigation, I.N. and I.L.I.P.; resources, I.N., I.L.I.P. and F.S.; data curation, I.N. and F.S.; writing—original draft preparation, I.N., I.L.I.P. and F.S.; writing—review and editing, I.N., I.L.I.P., F.S. and D.B.; visualization, I.N. and F.S.; supervision, D.B.; project administration, I.N. and I.L.I.P.; funding acquisition, I.N. and I.L.I.P. All authors have read and agreed to the published version of the manuscript.

Funding

The Plant Protection Laboratory, UMY, and Zoology Laboratory UAD funded this research and publication. The publication process was also partially supported by the World Class Professor program from the Directorate General of Higher Education (Ditjen Dikti) of the Ministry of Education and Culture, Republic of Indonesia, in 2023.

Data Availability Statement

The data used in this study are available at https://doi.org/10.5281/zenodo.8351100 (accessed on September 16, 2023).

Acknowledgments

The authors thank M. Agung Faturohman, Annisa Harmaningtyas Novinda Putri, Siti Munawarah, Ahmad Nguzairon, Nuriya Laelatus Sifa’iyah, Anggarsih Triyono, and Izaz Hadaya Amajid for their help in collecting sample. The authors also thank Risa Rahma Dewi, Lidia Sari, and Meri Eliza for their assistance in imaging the parasitoid samples.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hill, M.P.; Clusella-Trullas, S.; Terblanche, J.S.; Richardson, D.M. Drivers, impacts, mechanisms and adaptation in insect invasions. Biological Invasion 2016, 18, 883–891. [Google Scholar] [CrossRef]
  2. Rizali, A.; Oktaviyani, O.; Putri, S.; Doananda, M.; Linggani, A. Invasion of fall armyworm Spodoptera frugiperda, a new invasive pest, alters native herbivore attack intensity and natural enemy diversity. Biodiversitas Journal of Biological Diversity 2021, 22, 3482–3488. [Google Scholar] [CrossRef]
  3. Nonci, N.; Kalqutny, S.H.; Muis, A.; Azrai, M.; Aqil, M. Pengenalan Fall Armyworm (Spodoptera frugiperda JE Smith) Hama Baru pada Tanaman Jagung di Indonesia (in Indonesian); Balai Penelitian Tanaman Serealia: 2019.
  4. Girsang, S.S.; Nurzannah, S.E.; Girsang, M.A.; Effendi, R. The distribution and impact of fall army worm (Spodoptera frugiperda) on maize production in North Sumatera. In Proceedings of the International Conference on Sustainable Cereals and Crops Production Systems in the Tropics Makassar, Indonesia; 2020; p. 012099. [Google Scholar]
  5. Maharani, Y.; Dewi, V.K.; Puspasari, L.T.; Rizkie, L.; Hidayat, Y.; Dono, D. Cases of fall army worm Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) attack on maize in Bandung, Garut and Sumedang district, West Java. CROPSAVER-Journal of Plant Protection 2019, 2, 38–46. [Google Scholar] [CrossRef]
  6. Subiono, T. Preferences of Spodoptera frugiperda (Lepidoptera: Noctuidae) in several feed sources (in Indonesian). Jurnal Agroekoteknologi Tropika Lembab 2020, 2, 130–134. [Google Scholar] [CrossRef]
  7. Noer, H. Population and attack rate Spodoptera frugiperda on corn plants in Tulo Village, Sigi Regency (in Indonesian). Jurnal Agrotech 2020, 10, 66–68. [Google Scholar] [CrossRef]
  8. Kumela, T.; Simiyu, J.; Sisay, B.; Likhayo, P.; Mendesil, E.; Gohole, L.; Tefera, T. Farmers' knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya. International Journal of Pest Management 2018, 65, 1–9. [Google Scholar] [CrossRef]
  9. Baudron, F.; Zaman-Allah, M.A.; Chaipa, I.; Chari, N.; Chinwada, P. Understanding the factors influencing fall armyworm (Spodoptera frugiperda JE Smith) damage in African smallholder maize fields and quantifying its impact on yield. A case study in Eastern Zimbabwe. Crop Protection 2019, 120, 141–150. [Google Scholar] [CrossRef]
  10. Day, R.; Abrahams, P.; Bateman, M.; Beale, T.; Clottey, V.; Cock, M.; Colmenarez, Y.; Corniani, N.; Early, R.; Godwin, J. Fall armyworm: impacts and implications for Africa. Outlooks on Pest Management 2017, 28, 196–201. [Google Scholar] [CrossRef]
  11. Lubis, A.A.N.; Anwar, R.; Soekarno, B.P.; Istiaji, B.; Dewi, S.; Herawati, D. Coray wood corn (Spodoptera frugiperda) caterpillars in corn crops in Petir Village, Daramaga Sub-District, Bogor District, and its control potential using Metarizhium rileyi (in Indonesian). Jurnal Pusat Inovasi Masyarakat 2020, 2, 931–939. [Google Scholar]
  12. Song, Y.; Yang, X.; Li, H.; Wu, K. The invasive Spodoptera frugiperda (JE Smith) has displaced Ostrinia furnacalis (Guenée) as the dominant maize pest in the border area of southwestern China. Pest Management Science 2023, 79, 3354–3363. [Google Scholar] [CrossRef]
  13. Trisyono, Y.A.; Suputa, S.; Aryuwandari, V.E.F.; Hartaman, M.; Jumari, J. Occurrence of heavy infestation by the fall armyworm Spodoptera frugiperda, a new alien invasive pest, in corn Lampung Indonesia. Jurnal Perlindungan Tanaman Indonesia 2019, 23, 156–160. [Google Scholar] [CrossRef]
  14. Megasari, D.; Putra, I.L.I.; Martina, N.D.; Wulanda, A.; Khotimah, K. Biology of Spodoptera frugiperda JE Smith on some types of feed in the laboratory (in Indonesian). Agrovigor: Jurnal Agroekoteknologi 2022, 15, 63–67. [Google Scholar] [CrossRef]
  15. Putra, I.L.I.; Martina, N.D. Life cycle of Spodoptera frugiperda with feeding kale and leeks in laboratory (in Indonesian). Jurnal Ilmu Pertanian Indonesia 2021, 26, 386–391. [Google Scholar]
  16. Nurkomar, I.; Trisnawati, D.W.; Fahmi, F.; Buchori, D. Survival, development, and fecundity of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) on various host plant species and their implication for the pest management. Insects 2023, 14, 629. [Google Scholar] [CrossRef] [PubMed]
  17. Sari, A.; Buchori, D.; Nurkomar, I. The potential of Telenomus remus Nixon (Hymenoptera: Scelinoidae) as biocontrol agent for the new fall armyworm S. frugiperda (Lepidoptera: Noctuidae) in Indonesia. Planta Tropika 2020, 8, 69–74. [Google Scholar] [CrossRef]
  18. Putra, I.L.I.; Wati, C.D.N.S. Parasicity level of Telenomus sp. parasitoid against Spodoptera frugiperda JE Smith eggs in the laboratory. Journal of Natural Sciences and Mathematics Research 2020, 6, 73–77. [Google Scholar] [CrossRef]
  19. Polem, E.S.N. Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae): Serangan dan Parasitoidnya di Nagan Raya, Aceh (in Indonesian). Undergraduate Thesis, IPB University, Bogor, 2021. [Google Scholar]
  20. Rongkok, H.T.; Pasaru, F. Identification of paracitoids of Spodoptera frugiperda (Lepidoptera: Noctuidae) and its paracity levels in farmer-owned corn plantation in District Sigi and in District Donggala (in indonesian). Jurnal Agrotekbis 2021, 9, 972–978. [Google Scholar]
  21. Minarni, E.W. Eksplorasi musuh alami hama Spodoptera frugiperda pada pertanaman jagung di lahan kelompok tani raden Kelurahan Pabuwaran Kecamatan Purwokerto Utara Kabupaten Banyumas (in Indonesia). In Proceedings of the Prosiding Seminar Nasional LPPM Unsoed; 2023; pp. 139–147. [Google Scholar]
  22. Sari, W.; Nelly, N. Natural enemies of Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) on corn plants in West Sumatera. In Proceedings of the 2nd Agrifood System International Conference Padang, Indonesia; 2023; p. 012045. [Google Scholar]
  23. Supeno, B.; Tarmizi, T.; Meidiwarman, M.; Haryanto, H. Keragaman parasitoid yang berasosiasi dengan telur hama baru Spodoptera frugiperda di Pulau Lombok (in Indonesian). Prosiding SAINTEK 2021, 3, 418–423. [Google Scholar]
  24. Suroto, A.; Soesanto, L.; Bahrudin, M. Attack rate and natural enemies of Spodoptera frugiperda JE Smith on corn plants in five districts in Banyumas regency (in Indonesian). Proceedings Series on Physical & Formal Sciences 2021, 2, 44–49. [Google Scholar] [CrossRef]
  25. Tarigan, S.; Maryana, N.; Mubin, N. Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae): Attacks and their natural enemies on corn plantations in Munte Village, Munte Sub-district, Karo District, North Sumatera. In Proceedings of the International Conference on Modern and Sustainable Agriculture 2022; 2023; p. 012030. [Google Scholar]
  26. Tawakkal, M.; Buchori, D.; Maryana, N. New association between Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) and native natural enemies: Bioprospection of native natural enemies as biological control agents. In Proceedings of the IOP Conference Series: Earth and Environmental Science; 2021; p. 012030. [Google Scholar]
  27. Wahyuningsih, R.D.; Harjaka, T.; Suputa, S.; Trisyono, Y.A. Parasitization levels of Spodoptera frugiperda eggs (Smith)(Lepidoptera: Noctuidae) in three different corn ecosystems in East Java. Jurnal Perlindungan Tanaman Indonesia 2022, 26, 28–39. [Google Scholar] [CrossRef]
  28. Waruwu, A.; Tobing, M.C.; Siregar, A.Z. Ekplorasi parasitoid telur Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) pada tanaman jagung di Desa Purwobinangun Kec. Sei Bingai, Kab. Langkat (in Indonesian). Jurnal Online Agroteknologi 2023, 11, 10–18. [Google Scholar] [CrossRef]
  29. Nurkomar, I.; Putra, I.; Trisnawati, D.; Saman, M.; Pangestu, R.; Triyono, A. The existence and population dynamic of new fall armyworm species Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) in Yogyakarta, Indonesia. In Proceedings of the 3rd International COnference on Sustainable Agriculture, Yogyakarta, Indonesia; 2021; p. 012023. [Google Scholar]
  30. Hajek, A.E. Natural Enemies: An Introduction to Biological Control; Cambridge University Press: 2012. [CrossRef]
  31. Caltagirone, L.E.; Doutt, R.L. The history of the vedalia beetle importation to California and its impact on the development of biological control. Annual Review of Entomology 1989, 34, 1–16. [Google Scholar] [CrossRef]
  32. Winston, R.; Schwarzländer, M.; Hinz, H.L.; Day, M.D.; Cock, M.J.; Julien, M. Biological control of weeds: A world catalogue of agents and their target weeds; USDA Forest Service, Forest Health Technology Enterprise Team: 2014.
  33. USAID. Environmental Assessment for Implementation of Biological Control for The Leucaena Psyllid in Asia and Africa: Case Studies from India, Indonesia, Laos, Malaysia, Nepal, the Philippines and Thailand; Center for the Environment: Washington DC, 1995. [Google Scholar]
  34. Wyckhuys, K.A.G.; Rauf, A.; Ketelaar, J. Parasitoids introduced into Indonesia: part of a region-wide campaign to tackle emerging cassava pests and diseases. Biocontrol News and Information 2014, 35, 35N–37N. [Google Scholar]
  35. Tjitrosemito, S. The establishment of Procecidochares connexa in West Java, Indonesia : a biological control agent of Chromolaena odorata. Biotropia - The Southeast Asian Journal of Tropical Biology 1999, 12, 19–24. [Google Scholar] [CrossRef]
  36. Buchori, D.; Rizali, A.; Lukvitasari, L.; Triwidodo, H. Insect communities associated with siam weed: evaluation after three decades of Cecidochares connexa release as biocontrol agent. Diversity 2020, 12, 344. [Google Scholar] [CrossRef]
  37. Lukvitasari, L.; Triwidodo, H.; Rizali, A.; Buchori, D. Effects of locations on gall fly Cecidochares connexa (Macquart) attacks on invasive exotic plant Chromolaena odorata (L.) King & Robinson and its interaction with local insect communities (in Indonesian). Jurnal Entomologi Indonesia 2021, 18, 127–139. [Google Scholar] [CrossRef]
  38. McFadyen, R.E.C.; Desmier de Chenon, R.; Sipayung, A. Biology and host specificity of the Chromolaena stem gall fly, Cecidochares connexa (Macquart)(Diptera: Tephritidae). Australian Journal of Entomology 2003, 42, 294–297. [Google Scholar] [CrossRef]
  39. Safi'i, I. Parasitisasi pada Cecidochares connexa di beberapa tempat di Jawa Barat. Undergraduate Thesis, IPB University, Bogor, 2006. [Google Scholar]
  40. Rauf, A. Liriomyza: hama pendatang baru di Indonesia (in Indonesia). Buletin HPT 1995, 8, 46–48. [Google Scholar]
  41. Rauf, A.; Shepard, B.M.; Johnson, M.W. Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids. International Journal of Pest Management 2000, 46, 257–266. [Google Scholar] [CrossRef]
  42. Tapahillah, T. Survei lalat pengorok daun Liriomyza spp. (Diptera: Agromyzidae) dan parasitoidnya pada berbagai tumbuhan inang dan ketinggian tempat di Jawa Barat. Undergraduate Thesis, IPB University, Bogor, 2002. [Google Scholar]
  43. Hokkanen, H.M.; Pimentel, D. New associations in biological control: theory and practice. The Canadian Entomologist 1989, 121, 829–840. [Google Scholar] [CrossRef]
  44. Agboyi, L.K.; Mensah, S.A.; Clottey, V.A.; Beseh, P.; Glikpo, R.; Rwomushana, I.; Day, R.; Kenis, M. Evidence of leaf consumption rate decrease in fall armyworm, Spodoptera frugiperda, larvae parasitized by Coccygidium luteum. Insects 2019, 10, 410. [Google Scholar] [CrossRef] [PubMed]
  45. Shylesha, A.; Jalali, S.; Gupta, A.; Varshney, R.; Venkatesan, T.; Shetty, P.; Ojha, R.; Ganiger, P.C.; Navik, O.; Subaharan, K. Studies on new invasive pest Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae) and its natural enemies. Journal of Biological control 2018, 32, 1–7. [Google Scholar] [CrossRef]
  46. Wei, Y.-W.; Zhou, Y.-B.; Zou, Q.-C.; Sheng, M.-L. A new species of Campoletis Förster (Hymenoptera, Ichneumonidae) with a key to species known from China, Japan and South Korea. ZooKeys 2020, 1004, 99–108. [Google Scholar] [CrossRef] [PubMed]
  47. Pimentel, D. Introducing parasites and predators to control native pests. The Canadian Entomologist 1963, 95, 785–792. [Google Scholar] [CrossRef]
  48. Richardson, D.M.; Pyšek, P. Elton, CS 1958: The ecology of invasions by animals and plants. London: Methuen. Progress in Physical Geography 2007, 31, 659–666. [Google Scholar] [CrossRef]
  49. Jindal, J.; Sharma, K.P.; Shera, P.S.; Cheema, H.K. Native Parasitoids of Fall Army Worm Spodoptera frugiperda (J E Smith) in Maize. Indian Journal of Entomology 2022, 84, 865–867. [Google Scholar] [CrossRef]
  50. Pu'u, Y.M.; Mutiara, C. Attacks of invasive pest Spodoptera frugiperda (J. E. Smith) (Lepidoptera:Noctuidae) on corn plantation in Ende District Flores, Indonesia [in Indonesian]. Jurnal Entomologi Indonesia 2021, 18, 153–153. [Google Scholar] [CrossRef]
  51. DinasPerindustrianPerdagangandanKoperasiKabupatenBantul. Prospektus Investasi Sektor Pangan Kabupaten Bantul (in Indonesian). Availabe online: https://dpmptsp.bantulkab.go.id/web/potensi_investasi/detail/19-sektor-pangan (accessed on 12 September).
  52. Kishinevsky, M.; Keasar, T.; Bar-Massada, A. Parasitoid abundance on plants: Effects of host abundance, plant species, and plant flowering state. Arthropod-Plant Interactions 2017, 11, 155–161. [Google Scholar] [CrossRef]
  53. Kenis, M. Prospects for classical biological control of Spodoptera frugiperda (Lepidoptera: Noctuidae) in invaded areas using parasitoids from the Americas. Journal of Economic Entomology 2023, 116, 331–341. [Google Scholar] [CrossRef]
  54. Abang, A.; Nanga, S.; Fotso Kuate, A.; Kouebou, C.; Suh, C.; Masso, C.; Saethre, M.; Fiaboe, K. Natural Enemies of Fall Armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Different Agro-Ecologies. Insects 2021, 12, 509. Insect 2021, 12, 509. [Google Scholar] [CrossRef]
  55. Sharanabasappa, S.; Kalleshwaraswamy, C.; Poorani, J.; Maruthi, M.; Pavithra, H.; Diraviam, J. Natural enemies of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae), a recent invasive pest on maize in South India. The Florida Entomologist 2019, 102, 619–623. [Google Scholar] [CrossRef]
  56. Kenis, M.; Du Plessis, H.; Van den Berg, J.; Ba, M.N.; Goergen, G.; Kwadjo, K.E.; Baoua, I.; Tefera, T.; Buddie, A.; Cafà, G. Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the continent. Insects 2019, 10, 92. [Google Scholar] [CrossRef]
  57. Liao, Y.-L.; Yang, B.; Xu, M.-F.; Lin, W.; Wang, D.-S.; Chen, K.-W.; Chen, H.-Y. First report of Telenomus remus parasitizing Spodoptera frugiperda and its field parasitism in southern China. Journal of Hymenoptera Research 2019, 73, 95–102. [Google Scholar] [CrossRef]
  58. Sari, A.; Nurkomar, I.; Buchori, D. Comparison of Spodoptera frugiperda parasitoid performance under laboratory conditions. In Proceedings of the 3rd International Symposium on Transdisciplinary Approach for Knowledge Co-Creation in Sustainability, Bogor, Indonesia; 2023; p. 012031. [Google Scholar]
  59. Junaedi, E.; Yunus, M.; Hasriyanty, H. Parasitoids and it is parasitisme on white rice stem borer (Scirpophaga innotata Walker) in two different altitudes of rice fields (Oryza sativa l.) in District of Sigi (in Indonesian). e-Journal Agrotekbis 2016, 4, 280–287. [Google Scholar]
  60. Legault, S.; Hébert, C.; Blais, J.; Berthiaume, R.; Bauce, E.; Brodeur, J. Seasonal ecology and thermal constraints of Telenomus spp.(Hymenoptera: Scelionidae), egg parasitoids of the hemlock looper (Lepidoptera: Geometridae). Environmental Entomology 2012, 41, 1290–1301. [Google Scholar] [CrossRef]
  61. Goulart, M.M.P.; Bueno, A.d.F.; Bueno, R.C.O.d.F.; Diniz, A.F. Host preference of the egg parasitoids Telenomus remus and Trichogramma pretiosum in laboratory. Revista Brasileira de Entomologia 2011, 55, 129–133. [Google Scholar] [CrossRef]
  62. Hernandez, D.; Ferrer, F.; Linares, B. Introducción de Telenomus remus Nixon (Hym.: Scelionidae) para controlar Spodoptera frugiperda (Lep.: Noctuidae) en Yaritagua-Venezuela. Agronomía Tropical 1989, 39, 45–61. [Google Scholar]
  63. Cave, R.D. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News and Information 2000, 21, 21N–26N. [Google Scholar]
  64. Colmenarez, Y.C.; Babendreier, D.; Ferrer Wurst, F.R.; Vásquez-Freytez, C.L.; de Freitas Bueno, A. The use of Telenomus remus (Nixon, 1937)(Hymenoptera: Scelionidae) in the management of Spodoptera spp.: potential, challenges and major benefits. CABI Agriculture and Bioscience 2022, 3, 1–13. [Google Scholar] [CrossRef]
  65. Copeland, R. Fall armyworm natural enemy of the day: Telenomus remus (Hymenoptera: Scelionidae). Availabe online: http://www.icipe.org/content/fall-armyworm-natural-enemy-day-telenomus-remus (accessed on 12 September).
  66. Chandler, A.C.; Read, C. Introduction to Parasitology; John Willey and Sons: New York, USA, 1961. [Google Scholar]
  67. Polaszek, A.; Kimani, S.W. Telenomus species (Hymenopetra: Scelionidae) attacking eggs of pyralid pests (Lepidoptera) in Africa: A review and guide to identification. Bulletin of Entomological Research 1990, 80, 57–71. [Google Scholar] [CrossRef]
  68. Kalyanasundaram, M.; Kamala, I.M. Parasitoids. In Ecofriendly Pest Management for Food Security, 2016; pp. 109-138. [CrossRef]
  69. Buhl, P.N. Species of Platygastrinae and Sceliotrachelinae from rainforest canopies in Tanzania, with keys to the Afrotropical species of Amblyaspis, Inostemma, Leptacis, Platygaster and Synopeas (Hymenoptera, Platygastridae). Tijdschrift voor Entomologie 2011, 154, 75–126. [Google Scholar] [CrossRef]
  70. Buhl, P.N. Key to Platygaster (Hymenoptera: Platygastridae) from Denmark, with descriptions of new species. Steenstrupia 2006, 29, 127–167. [Google Scholar]
  71. McCutcheon, G.S.; Salley, W.; Turnipseed, S. Biology of Apanteles ruficrus, an imported parasitoid of Pseudoplusia includens, Trichoplusia ni, and Spodoptera frugiperda (Lepidoptera: Noctuidae). Environmental Entomology 1983, 12, 1055–1058. [Google Scholar] [CrossRef]
  72. Rajapakse, R.H.; Ashley, T.R.; Waddill, V.H. Biology and host acceptance of Microplitis manilae (Hymenoptera: Braconidae) raised on fall armyworm larvae Spodoptera frugiperda (Lepidoptera: Noctuidae). Florida Entomologist 1985, 68, 653–657. [Google Scholar] [CrossRef]
  73. Alam, M. Attempts at the biological control of major insect pests of maize in Barbados, WI. Proceeding of the Caribbean Food Crops Society 1978, 15, 127–135. [Google Scholar]
  74. Whitfield, J.B.; Austin, A.D.; Fernandez-Triana, J.L. Systematics, biology, and evolution of microgastrine parasitoid wasps. Annual Review of Entomology 2018, 63, 389–406. [Google Scholar] [CrossRef]
  75. Tawakkal, M.; Buchori, D.; Maryana, N. New association between Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae) and native natural enemies: Bioprospection of native natural enemies as biological control agents. In Proceedings of the 2nd International Symposium on Transdisciplinarity Approach for Knowledge Co-Creation in Sustainability - Understanding Complexity and Transdisciplinarity for Environmental Sustainability Bogor, Indonesia; 2021; p. 012030. [Google Scholar]
  76. Gross, H.R. Little-known fly-promising biocontrol weapon. Agricultural Research 1985, 33, 12. [Google Scholar]
  77. Deshmukh, S.S.; Kiran, S.; Naskar, A.; Pradeep, P.; Kalleshwaraswamy, C.; Sharath, K. First record of a parasitoid, Megaselia (M) scalaris (Diptera: Phoridae) of fall armyworm, Spodoptera frugiperda (JE Smith)(Lepidoptera: Noctuidae) from India. Egyptian Journal of Biological Pest Control 2021, 31, 94. [Google Scholar] [CrossRef]
  78. Tang, Y.; Li, Q.; Xiang, L.; Gu, R.; Wu, Y.; Zhang, Y.; Bai, X.; Niu, X.; Li, T.; Wei, J. First report on Megaselia scalaris Loew (Diptera: Phoridae) infestation of the invasive pest Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) in China. Insects 2021, 12, 65. [Google Scholar] [CrossRef]
  79. Ruíz-Nájera, R.E.; Molina-Ochoa, J.; Carpenter, J.E.; Espinosa-Moreno, J.A.; Ruíz-Nájera, J.A.; Lezama-Gutierrez, R.; Foster, J.E. Survey for hymenopteran and dipteran parasitoids of the fall armyworm (Lepidoptera: Noctuidae) in Chiapas, Mexico. Journal of Agricultural and Urban Entomology 2007, 24, 35–42. [Google Scholar] [CrossRef]
  80. Disney, R.H.L. Natural history of the scuttle fly, Megaselia scalaris. Annuual Review of Entomology 2008, 53, 39–60. [Google Scholar] [CrossRef] [PubMed]
  81. Daif, M.K.; Mosallam, A.; Ebrahim, A. The scuttle fly, Megaselia scalaris (Loew, 1866)(Diptera: Phoridae): A new threat on laboratory aass production of fruit flies. Journal of Plant Protection and Pathology 2023, 14, 109–113. [Google Scholar] [CrossRef]
  82. Rajan, R.; Shamsudeen, R. First record of Megaselia scalaris (Diptera: Phoridae) as a parasitoid of Thyas coronata (Lepidoptera: Erebidae). Indian Journal of Entomology, 1251. [Google Scholar] [CrossRef]
  83. Acevedo-Alcalá, A.; Lomeli-Flores, J.R.; Rodríguez-Leyva, E.; Rodríguez-Rodríguez, S.E.; Ortiz-Andrade, E. Does Megaselia scalaris (Diptera: Phoridae) have potential as a biological control agent of fall armyworm? Florida Entomologist 2023, 106, 56–58. [Google Scholar] [CrossRef]
  84. Nagoshi, R.N.; Meagher, R.L. The Spodoptera frugiperda host strains: What they are and why they matter for understanding and controlling this global agricultural pest. Journal of Economic Entomology 2022, 115, 1729–1743. [Google Scholar] [CrossRef] [PubMed]
  85. Wibowo, L. The abundance and diversity of the parasitoid of banana leaf skipper pest (Erionota thrax L.) in South Lampung Regency (in Indonesian). Jurnal Hama dan Penyakit Tumbuhan Tropika 2015, 15, 26–32. [Google Scholar] [CrossRef]
  86. Fawzi, F.S.; Iman, I.a.-S.; Adil, A.H.; Muhammad, A.a.-S. Survey and distribution density of genus Brachymeria species (Hymenoptera : Chalcididae) in Egypt. Egyptian Journal of Plant Protection Research Institute 2020, 3, 415–432. [Google Scholar]
  87. Agboyi, L.K.; Goergen, G.; Beseh, P.; Mensah, S.A.; Clottey, V.A.; Glikpo, R.; Buddie, A.; Cafà, G.; Offord, L.; Day, R. Parasitoid complex of fall armyworm, Spodoptera frugiperda, in Ghana and Benin. Insects 2020, 11, 68. [Google Scholar] [CrossRef]
  88. Buchori, D.; Herawati, E.; Sari, A. The effectiveness of Telenomus remus (Nixon)(Hymenoptera: Scelionidae) for controlling welsh onion pest Spodoptera exigua Hübner (Lepidoptera: Noctuidae) (in indonesian). Jurnal Entomologi Indonesia 2008, 5, 81–95. [Google Scholar] [CrossRef]
  89. Ratna, E.S. Efficiency of parasitization on larval host, Spodoptera litura (F.), by an endoparasitoid Snellenius (=Microplitis) manilae Ashmead in the laboratory (in Indonesian). Jurnal Hama dan Penyakit Tumbuhan Tropika 2008, 8, 8–16. [Google Scholar] [CrossRef]
Preprints 89072 g001
Figure 1. Sampling point of S. frugiperda parasitoid in Yogyakarta.
Figure 1. Sampling point of S. frugiperda parasitoid in Yogyakarta.
Preprints 89072 g001
Preprints 89072 g002
Figure 2. Egg parasitoid of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Hymenoptera sp.1, b. Hymenoptera sp.2, c. Trichogramma sp., and d. Telenomus remus.
Figure 2. Egg parasitoid of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Hymenoptera sp.1, b. Hymenoptera sp.2, c. Trichogramma sp., and d. Telenomus remus.
Preprints 89072 g002
Preprints 89072 g003
Figure 3. Larval parasitoid (Hymenoptera) of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Apanteles sp., b. Campoletis sp., c. Coccygidium sp., d. Eupelmus sp., e. Microplitis sp., and e. Stenobracon sp.
Figure 3. Larval parasitoid (Hymenoptera) of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Apanteles sp., b. Campoletis sp., c. Coccygidium sp., d. Eupelmus sp., e. Microplitis sp., and e. Stenobracon sp.
Preprints 89072 g003
Preprints 89072 g004
Figure 4. Larval parasitoid (Diptera) of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Archytas marmoratus and b. Megaselia scalaris.
Figure 4. Larval parasitoid (Diptera) of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Archytas marmoratus and b. Megaselia scalaris.
Preprints 89072 g004
Preprints 89072 g005
Figure 5. Morphological characters of Megaselia scalaris. a. female, b. male, c. head, d. wing, e. halter, f. hind tibia, g. female terminalia, and h. male terminalia.
Figure 5. Morphological characters of Megaselia scalaris. a. female, b. male, c. head, d. wing, e. halter, f. hind tibia, g. female terminalia, and h. male terminalia.
Preprints 89072 g005
Preprints 89072 g006
Figure 6. Pupal parasitoid of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Brachymeria femorata, b. Brachymeria lasus.
Figure 6. Pupal parasitoid of Spodoptera frugiperda in Special Region Yogyakarta, Indonesia. a. Brachymeria femorata, b. Brachymeria lasus.
Preprints 89072 g006
Preprints 89072 g007
Figure 7. Distribution of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Figure 7. Distribution of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Preprints 89072 g007
Preprints 89072 g008
Figure 8. Distribution of Telenomus remus in Special Region Yogyakarta, Indonesia.
Figure 8. Distribution of Telenomus remus in Special Region Yogyakarta, Indonesia.
Preprints 89072 g008
Table 1. Diversity of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Table 1. Diversity of Spodoptera frugiperda’s parasitoid in Special Region Yogyakarta, Indonesia.
Order Family Species Abundance
Bantul Gunung Kidul Kulonprogo Sleman
Egg parasitoid
Hymenoptera Unknown Hymenoptera sp.1* 49
Unknown Hymenoptera sp.2* 21
Platygasteridae Telenomus remus* 8536 831 476 2324
Trichogrammatidae Trichogramma sp. 198
Larval parasitoid
Hymenoptera Braconidae Apanteles sp.* 27 12 110
Ichneumonidae Campoletis sp.* 1 1
Braconidae Coccygidium sp.* 1 1
Eupelmidae Eupelmus sp.* 6
Braconidae Microplitis sp.* 15 19
Braconidae Stenobracon sp.* 3
Diptera Tachinidae Archytas marmoratus 1
Phoridae Megaselia scalaris 1
Pupal parasitoid
Hymenoptera Chalcididae Brachymeria femorata* 5
Chalcididae Brachymeria lasus* 3
Ichneumonidae Charops sp.* 1 2
Species richness 8 6 3 7
Total abundance 8748 924 494 2478
* New association.
Table 2. Parasitoid associated with Spodoptera frugiperda based on the time of observation.
Table 2. Parasitoid associated with Spodoptera frugiperda based on the time of observation.
Order Family Species Parasitoid 2019 2020 2021 2022
Egg parasitoids
Hymenoptera Unknown Hymenoptera sp.1 v
Unknown Hymenoptera sp.2 v
Platygasteridae Telenomus remus v v v v
Trichogrammatidae Trichogramma sp. v
Larval parasitoids
Hymenoptera Braconidae Apanteles sp. v v v
Ichneumonidae Campoletis sp. v
Ichneumonidae Coccygidium sp. v
Eupelmidae Eupelmus sp. v
Braconidae Microplitis sp. v v
Braconidae Stenobracon sp. v
Diptera Tachinidae Archtyas marmoratus v
Phoridae Megaselia scalaris v
Pupal parasitoids
Hymenoptera Chalcididae Brachymeria lasus v
Chalcididae Brachmymeria femorata v
Ichneumonidae Charops sp. v
Accumulated number of parasitoid species found 1 8 13 15
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.
Prerpints.org logo

Preprints.org is a free preprint server supported by MDPI in Basel, Switzerland.

facebook logotwitter logolinkedin logo
MDPI Initiatives
Important Links
Subscribe

Disclaimer

Terms of Use

Privacy Policy

© 2024 MDPI (Basel, Switzerland) unless otherwise stated