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RESEARCH ARTICLE Agricultural Science Digest, Volume Issue : () Species Diversity and Composition of Chalcidids (Chalcidoidea: ) on Tidal Swamp Rice Field in Indragiri Hilir, Indonesia

Zahlul Ikhsan1, Hidrayani2, Yaherwandi2, Hasmiandy Hamid2, Rosichon Ubaidillah3

ABSTRACT Background: Indragiri Hilir District has the most extensive rice harvest area and is the most significant contributor to rice production in Riau Province. Family is a parasitoid that can act as a biological agent to reduce pest attacks on rice. This research aimed to study the species diversity of Chalcididae on tidal swamp rice fields in Indragiri Hilir District. Methods: Sampling was carried out in two periods of rice planting. Samplings were conducted in 4 sub-districts of rice production centers, namely Batang Tuaka, Keritang, Reteh and Tembilahan Hulu, using three sampling techniques (i.e., insect net, malaise trap and yellow pan trap). Diversity index (H’), Species richness index (d), Species Evenness index (J’) and Similarity Index (Is) were calculated. Result: We found 127 individuals consisting of 5 genera and 11 species of Chalcididae were found in the four studied areas. Among them, Antrocephalus lugubris, A. maculipennis, Brachymeria excarinata, B. minuta and Dirhinus anthracia. B. excarinata and Antrocephalus sp. are reported as a new record to Indonesia and were found in all study locations. B. excarinata has the highest abundance of individuals. The shape of the landscape can influence the diversity index, species abundance and individual abundance of Chalcididae.

Key words: Brachymeria excarinata, Chalcididae, Species diversity, Tidal swamp rice.

INTRODUCTION 1Student of Postgraduate Program, Agriculture Faculty Andalas Rice harvested area in Riau province is 93.755 ha. Indragiri University, Sumatera Barat Province, Indonesia. Hilir Regency has the largest rice harvest area in Riau 2Agriculture Faculty Andalas University, Sumatera Barat. Indonesia, Province, 23.432 ha and is also the most significant 25163 Tel./Fax. +62-751-71181. contributor to Riau Province’s rice production, which is 3Research and Development Centre for Biology, LIPI-Museum 109.921 tons (BPS, 2018). One of the limiting factors in rice Zoologicum Bogoriense, Bogor, Indonesia. production is the pest attack. Corresponding Author: Zahlul Ikhsan, Agriculture Faculty, Islamic The application of synthetic insecticides is one of the University of Indragiri, Riau. Indonesia. efforts made to control pests. However, the use of synthetic Email: [email protected] pesticides will adversely affect the agricultural ecosystem. Therefore, we need to develop natural enemies of rice plant How to cite this article: Ikhsan, Z., Hidrayani, Yaherwandi, Hamid, pests, one of which is parasitoid . It is a dilemma for H. and Ubaidillah, R. (). Species Diversity and Composition of the farmers not to rely on insecticides even though their Chalcidids Wasps (Chalcidoidea: Hymenoptera) on Tidal Swamp negative impacts are known. For example, the pesticides Rice Field in Indragiri Hilir, Indonesia. Agricultural Science Digest. will also unintentionally eradicating the pest’s natural (): enemies (Hidrayani, et al., 2013). Submitted: 30-12-2020 Accepted: 25-05-2021 Online: The individuals of the family Chalcididae are parasitoids on Lepidoptera, Coleoptera, Diptera, Neuroptera insects and reported about 19 genera and 120 species from Indonesia part of Hymenoptera. Chalcididae is solitary and partly lives (Noyes, 2020). Sofyan and Ubaidillah (2017) found six in a colony. The distribution of Chalcididae exists throughout genera consisting of 8 morphospecies of Chalcididae on the world, but generally, only a few species can live in cold Eggplant (Solanum melongena) and Bitter Melon regions. Chalcididae is divided into five subfamilies, (Momordica charantia) in Bogor, West Java. including Helticellinae, Epitraninae, Dirhininae, Chalcidinae Chalcididae is one of the most exciting and complex and Smicromorphinae. At present, in Australia, there are 21 hymenopteran families to study taxonomically (Boucek genera, including nine genera from New Guinea and eastern 1988). They show morphological resemblances among China. The estimated number of genera globally is about genera and species, a phenomenon widely found in other 90 genera, with approximately 1.469 species and mainly in Chalcidoidea families as well – and it is not easy to separate the tropical region (Aguiar et al., 2013). There have been them at the species level and often at a generic class.

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Though many species of Chalcididae look very much alike, transect lines of 300 m. There were ten sampling plots (1x1 m) they differ widely inhabits (Narendran and Achterberg, 2016). in each line with a space between sample plots of 100 m. The Chalcididae family has a body character that is easy to So, in each transect line, there were ten sampling plots. In recognize compared to other families of the Hymenoptera, each plot, the sample plant was determined systematically including a sturdy body and partly large, black or red with a by making a diagonal line of sub-samples of 1x1 m. mark in the form of yellow strokes, has a femur on the Chalcididae was collected using the malaise trap, sweep enlarged hind legs, has a part serrated abdomen, arched net and yellow pan trap (Darnaedi and Noerdjito 2007). back tibia to support the femur, prepectus smaller than (i) Malaise trap tegula, propodeum mostly areolate, mesepisternum with protruding ventral portions in the anterior epocnemial carina. Malaise trap was installed at each research location, each This character is also found in other families such as with one malaise trap. The installation of the malaise trap Eurytomidae, Leucospidae and Torymidae, but there has was based on the direction of the wind, which was facing never been a combination of these characters (Boucek, north or south. Generally, insects that are actively flying and 1988; Lotfalizadeh, et al., 2012). foraging prefer light like sunlight. If these insects fly and Conserving and increasing the function of pest’s natural pass through these traps, the insect is more easily trapped enemies is one of the main components in Integrated Pest when compared to mounting according to the sun’s rise Management (IPM) to suppress pest attacks to below the because this trap is designed for insects from the side, not economic profitability threshold of agricultural production. from the front. Trapped insects were collected in a bottle Previous studies showed that the parasitic Hymenoptera that was filled with 96% alcohol. This trap was installed for has a high diversity index on tidal swamp rice in Indragiri one week in each phase of rice cultivation. Then the trapped Hilir District (Ikhsan et al., 2020). However, until now, there sample was transferred to the sample bottle and labeled. has been no further information about the presence of (ii) Sweep net Chalcididae in tidal land rice plantations in the Indragiri Hilir A sweep net was set up on each sample. We did ten double Regency. This research aims to study the species diversity swings. Insects that were caught immediately put into a film of Chalcididae on tidal swamp rice fields in Indragiri Hilir bottle containing 96% alcohol. In the laboratory, the pest’s District, Riau Province, Indonesia. natural enemies (i.e., parasitoids and predators) were separated from other insects. Each morphospecies was MATERIALS AND METHODS separated, then inserted into 2 ml Eppendorf, which Study area and period contained 96% alcohol for identification purposes. The study was conducted in four sub-districts of rice (iii) Yellow pan trap production centers in Indragiri Hilir District from January Yellow pan trap was used to catch insects interested in 2018 until March 2020. The four sub-districts are Batang yellow. Collecting insects with a yellow pan trap was done Tuaka (020’19" S,1032’53" E), Reteh (040’04" by placing one yellow pan trap on each sample bed. The S,10308’06" E), Tembilahan Hulu (024’05" S,10304’06" E), yellow pan trap was filled with detergent water to reduce Keritang (042’29" S, 1030’28" E). Chalcididae was carried the surface pressure of the water so that the insects that out at the Insect Bioecology Laboratory, Faculty of enter will sink and die. Installation of a yellow trap was done Agriculture, University of Andalas, West Sumatra Province in the morning before 09.00 A.M., then taken back in the and Pusat Penelitian Biologi LIPI, West Java Province, afternoon. The trapped insects were filtered and taken using Indonesia. a brush not to damage parts of the insect. Then the insects Insect collection were inserted into a film bottle that has been filled with 96% alcohol to be identified in the laboratory. The individuals of the Chalcididae family were collected at two planting periods at each location. In each planting period, Identification of chalcididae the collections were done three times at different stages of Insects were carried to the Insect Bioecology Laboratory, rice cultivation: before planting, vegetative stage and Faculty of Agriculture, University of Andalas, West Sumatra generative stage in every location. The condition before Province. All insects obtained were separated by order. planting was referred to as the stage before the land was Identification of the Chalcididae Family was carried out at cultivated and there was still vegetation. In the vegetative the Entomology Laboratory, Zoology Division of the Biology stage, Chalcididae was collected when the rice plants were Research Center, Indonesian Institute of Sciences, Bogor, about one month old. In the generative phase, the Chalcidids West Java. Insect identification was based on the main were collected when the ice plants were about two months morphological characteristics of the mouth, antennae, wings, old. In every sub-district, one area of peatland rice with a legs and skin color. The identification used various minimum size of 1.000 x 500 m was assigned as a sampling references, namely Hymenoptera of The World by Goulet location. Two transect lines (1.000 m length each) were and Huber (1993), Australasian Chalcidoidea (Hymenoptera) made in every area with a minimum distance between by Zdenek Boucek (1988), Oriental Brachymeria

2 AGRICULTURAL SCIENCE DIGEST - A Research Journal of Agriculture, and Veterinary Sciences Species Diversity and Composition of Chalcidids Wasps (Chalcidoidea: Hymenoptera) on Tidal Swamp Rice Field in... identification books written by Narendran (1989) and official of an individual that was collected belongs to Brachymeria websites http://www.bugguide.net. Also, identification was excarinata (25 individuals). This species was reported from confirmed with the help of Hymenoptera experts and was all studied areas. From an abundance aspect, Reteh (10 supported by basic books from the Entomology Laboratory individuals), Batang Tuaka (7 individuals), Keritang (4 of the Indonesian Institute of Sciences (LIPI). individuals), Tembilahan Hulu (4 individuals). Brachymeria Data analysis excarinata and Anthrocephalus sp. were collected from all of the studied areas. Several parameters were calculated in data analysis. The The structure of species composition and the relative diversity index (H’) was calculated using the Shannon- abundance of the Chalcididae family (all the collected Wiener formula. Species richness index (d) was using the samples using Sweep net, Yellow pan trap and Malaise traps) Margalef formula. Species Evenness Index was calculated in Indragiri Hilir Regency are shown Table 2. According to using the Pielou’s Evenness (J’) formula, which measured collected data (Table 2), Brachymeria excarinata (19,69%) the proportion of each species in a population at a certain has the highest relative abundance in Indragiri Hilir District, place and time according to the formula by Krebs (2000). followed by Anthrocephalus lugubris (15,75%) and Species Similarity Index was calculated to determine the Anthrocephalus sp. (11,02%). According to the table, in proportion of species similarity between two communities Batang Tuaka, the highest abundance value was for using the Jaccard species similarity index. Benchmark Brachymeria excarinata (5,51%), followed by Anthrocephalus values use the evenness index Krebs (2000). lugubris (2,36%). In Keritang, the highest value was for Antrocephalus maculipennis (5,51%), followed by RESULTS AND DISCUSSION Brachymeria lasus (3,94%). In Reteh, the highest value was The abundance of the Chalcididae family in the studied areas for Brachymeria excarinata (7,87%), followed by of Indragiri Hilir Regency is shown in Table 1. Most number Anthrocephalus sp. (4,72%). In Tembilahan Hulu, the highest

Table 1: The abundance of Chalcididae on tidal swamp rice field in Indragiri Hilir District, Indonesia. Sub-district (individuals) Total Species name Batang tuaka Keritang Reteh Tembilahan hulu (individuals) Anthrocephalus sp 2 4 6 2 14 Anthrocephalus lugubris (Masi,1932) 3 4 0 13 20 Antrocephalus phaeospilus (Waterston, 1922) 0 0 0 11 11 Antrocephalus maculipennis Cameron, 1905 0 7 0 1 8 Brachymeria excarinata Gahan, 1925 7 4 10 4 25 Brachymeria lasus (Walker, 1841) 2 5 0 3 10 Brachymeria minuta (Linnaeous, 1767) 0 0 3 2 5 Dirhinus anthracia Walker, 1846 2 4 5 0 11 Epitranus crassicornis Boucek, 1982 0 3 4 3 10 Haltichella sp.1 0 3 0 0 3 Haltichella sp. 2 0 4 3 3 10 Total 16 38 31 42 127

Table 2: Percentage of Chalcididae abundance on tidal swamp rice field in Indragiri Hilir District, Indonesia. Species Sub-district (%) Total name Batang tuaka Keritang Reteh Tembilahan hulu (%) Anthrocephalussp 1,57 3,15 4,72 1,57 11,02 Anthrocephalus lugubris (Masi,1932) 2,36 3,15 0,00 10,24 15,75 Antrocephalus phaeospilus (Waterston, 1922) 0,00 0,00 0,00 8,66 8,66 Antrocephalusmaculipennis Cameron, 1905 0,00 5,51 0,00 0,79 6,30 Brachymeria excarinata Gahan, 1925 5,51 3,15 7,87 3,15 19,69 Brachymeria lasus (Walker, 1841) 1,57 3,94 0,00 2,36 7,87 Brachymeria minuta (Linnaeous, 1767) 0,00 0,00 2,36 1,57 3,94 Dirhinus anthracia, Walker, 1846 1,57 3,15 3,94 0,00 8,66 Epitranus crassicornis Boucek, 1982 0,00 2,36 3,15 2,36 7,87 Haltichella sp 1 0,00 2,36 0,00 0,00 2,36 Haltichella sp 2 0,00 3,15 2,36 2,36 7,87 Total 12,60 29,92 24,41 33,07 100,0

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Table 3: Alpha diversity index of Chalcididae on tidal swamp rice field in Indragiri Hilir District, Indonesia. Please check the data in the table. Studied location Diversity index Batang Tuaka Keritang Reteh Tembilahan Hulu Total species 5 9 6 9 Total individuals 16 38 31 42 Diversity index shannon-wiener (H’) 1,46 2,16 1,70 1,89 Species richness margalef index (d) 1,44 2,20 1,46 2,14 Species evenness (J) 0,90 0,99 0,95 0,86 Simpson index (D) 0,76 0,90 0,82 0,83 value was for Anthrocephalus lugubris (10,24%), followed We found 127 individuals of Family Chalcididae by Antrocephalus phaeospilus (8,66%). consisting of 5 genera and 11 species were collected using The diversity index and species evenness index in the Sweep net, Yellow pan trap and Malaise traps. Among them studied localities were calculated and are presented in Table 3. are reported as a new record to Indonesia, namely A. According to the Shannon-Wiener index, Species richness Lugubris, A. maculipennis, B. excarinata, B. minuta and Margalef index (d) and Simpson index (D), it was indicated Dirhinus anthracia. Vegetation around rice plants has a that Keritang had a higher species diversity than the other significant influence on the presence of Chalcididae. studied localities. In the same way, Batang Tuaka had the Therefore, the landscape of an area is one of the main least species diversity. Based on the Shannon-Wiener index, factors in the distribution of Chalcididae. Tembilahan Hulu Keritang had the most species diversity, followed by and Keritang Districts have a higher diversity index than Tembilahan Hulu, Reteh and Batang Tuaka, respectively. Batang Tuaka and Reteh Districts (Table 3). Keritang Sub- The Species Evenness Pielou’s index (J) showed that district and Tembilahan Hulu Sub-district have the highest Keritang had the most amount of numerical, followed by number of morphospecies and individuals compared to Reteh, Batang Tuaka and Tembilahan Hulu, respectively. Batang Tuaka and Reteh. This is likely due to the Keritang Similarity levels of species of Chalcididae on tidal Sub-district implemented a polyculture planting system while swamp rice in the four studied areas were classified as low the other two applied monoculture farming. until high. The similarity of species is highest in the Keritang Consequently, each study site has a different chalcidoid and Tembilahan Hulu (0.64) and followed by the similarity species composition. Chalcididae species richness of species in the Keritang and Batang Tuaka (0.56), Keritang can be a predictor of rice management systems. Our finding and Reteh (0.50), Tembilahan Hulu and Batang Tuaka (0.50), strengthens the statement by Yaherwandi, et al. (2008) Tembilahan Hulu and Reteh (0.50), Batang Tuaka and Reteh reported that Nyalindung, which has a more complex (0.38). It means that the composition of Chalcididae is structure and consists of rice, pulses and vegetable relatively varied between one sub-district and another in ecosystems, has a higher number of individuals, species Indragiri Hilir District. Then, several species of Chalcididae and Hymenoptera families to Gasol and Selajambe, which only exist in one location and several species exist in various consists monoculture rice farming. locations (Table 4). In this study, we found eleven species within five genera The diversity of Chalcididae in this study showed a of chalcidids waps from the tidal swamp rice field in Indragiri higher diversity at the generative phase than before the Hilir (Table 1). Among those eleven species, five species, planting and vegetative phases (Table 5). This was likely namely A. lugubris, A. japonicus, A. maculipennis, B. caused by the many types of weeds and pests that existed excarinata and B. minuta, are reported as the first time before the planting and generative stage. Our finding is in recorded from Indonesia. There was not much information line with the result of the previous study that Hymenoptera on the biology and parasitization of Chalcidids wasp in diversity has a high diversity at the time before planting, Indonesia that makes it challenging to know the host. then decreases in the vegetative phase and increases in However, the wasps are so far known to be parasitoids of a the generative phase (Ikhsan et al. 2020). wide range of insect pests, mainly the order of Lepidoptera, however some as hyperparasitoids of Tachinidae (Diptera), Table 4: Similarity index of species of Chalcididae among the four Braconidae and Ichneumonidae (Boucek, 1988; Narendran, studied areas on tidal swamp rice field in Indragiri Hilir 1989; Noyes, 2020). District, Indonesia. The parasitoid species Brachymeria excarinata Gahan, Sub-district Batang Tuaka Keritang Reteh 1925 (Hymenoptera: Chalcididae), is recorded for the first Batang tuaka - - 0,38 time from Rawalpindi and Islamabad, Punjab (Pakistan) as Keritang 0,56 - 0,50 hyper-parasitoid of Cotesia plutella (Khaliq et al., 2016). Also, Moningka, et al. (2012) reported that there was Tembilahan hulu 0,50 0,64 0,50 found Brachymeria sp. that parasitized pests on Paddy Rice

4 AGRICULTURAL SCIENCE DIGEST - A Research Journal of Agriculture, Animal and Veterinary Sciences Species Diversity and Composition of Chalcidids Wasps (Chalcidoidea: Hymenoptera) on Tidal Swamp Rice Field in...

Table 5: Total of species, individuals, alpha diversity index of Chalcididae at three different stages on tidal swamp rice field in Indragiri Hilir District, Indonesia. First period Second period Diversity index Before Vegetative Generative Before Vegetative Generative planting phase phase planting phase phase Total species 7 3 9 8 4 10 Total individuals 39 6 30 26 5 21 Diversity index shannon-wiener (H’) 1,84 1,01 1,86 1,95 1,33 2,24 Species richness margalef index(d) 1,64 1,12 1,76 2,15 1,86 2,96 Species evenness pielou’s index (J) 0,95 0,92 0,96 0,94 0,96 0,97 Simpson index (D) 0,85 0,73 0,86 0,87 0,9 0,93 in South Minahasa District. Besides Brachymeria sp., other phase and then the diversity index increased in the rice pest parasitoids such as Telenomus sp.; Ooencyrtus generative phase. This happened at all research locations sp.; Tetrastichus sp.; Trichogramma sp.; Compsilura sp.; in the tidal land rice plantations of Indragiri Hilir Regency. Brachymeria sp.; Apanteles sp.; and Amauromorpha sp. In This was likely caused by the many types of weeds that another study by Daniel and Ramaraju (2018) reported 12 existed before the planting stage. Our finding is in line with species within nine genera of Chalcididae were collected the results of previous studies that complex agricultural from the rice ecosystem in the Cauvery delta zone in India. landscapes can increase parasitoid diversity (Yaherwandi Brachymeria excarinata and Antrocephalus sp. are species et al. 2008). Parasitoid diversity and parasitism depend on found in all study sites and Brachymeria excarinata has the many factors; those are location, season, host feeding niche highest individual abundance (Table 1 and Table 2). This and host diversity (Hamid, et al., 2003). reflects that B. excarinata can be spread well and comprehensively in all tidal rice planting locations in Indragiri ACKNOWLEDGEMENT Hilir Regency. That means B. excarinata is a potential parasitoid that can be developed for pest control in rice The authors are grateful to the Indonesian Ministry of cultivation. B. excarinata has been reported from Cameron, Research Technology and Higher Education and LPDP for Egypt, Iran, India, China, Japan, Taiwan, Vietnam, giving the scholarship and financial support for this research. Philippines, Papua New Guinea (Noyes, 2020) and the first We are grateful too to the student and lecturer of the record to Indonesia in this paper. The species has a very Agriculture Faculty, the Islamic University of Indragiri, for wide range of host, mainly the order of Lepidoptera at about support in our study. 23 species within eight families and one species of Coleoptera (Noyes, 2020). The species was recorded for REFERENCES the first time from Rawalpindi and Islamabad, Punjab Aguiar, Alexandre P. andrew R. Deans, Michael S. Engel, Mattias (Pakistan), as hyper-parasitoid of Cotesia plutellae. Besides, Forshage, John T. Huber, John T. Jennings, Norman F. B. excarinata was also found as a pupa parasitoid from Johnson, Arkady S. Lelej, John T. Longino, Volker Lohrmann, Craspedonta leayana (Coleoptera: Chrysomelidae) in North- István Mikó, Michael Ohl, Claus Rasmussen andreas East India (Singh et al., 2006). Although Brachymeria is Taeger and Dicky Sick Ki Yu. 2013. “Order Hymenoptera.” pretty well known and easily recognizable on the generic Zootaxa. 3703(1): 51-62. level, this cannot be said about the species within this genus, Boucek, Z. (1988). Australian Chalcidoidea (Hymenoptera) A which are very numerous in all warmer parts of the world Biosystematic Revision of Genera of Fourteen Families, (Ubaidillah, 1996). With a Reclassification of Spesies. Wallingford: CAB Similarity levels of species of Chalcididae on tidal International. swamp rice in the four studied areas were classified as low BPS. (2018). Luas Panen Dan Produksi Padi Di Provinsi Riau 2018. to high (Table 4). Tembilahan Hulu Sub-district with Keritang Pekanbaru. Sub-district has the highest similarity index (0.64). This high Daniel, J. Alfred and K. Ramaraju. (2018). Diversity of Chalcidids similarity can be caused by the landscape of rice plantations (Chalcididae: Hymenoptera) among Three Rice Growing in the Tembilahan Hulu and Keritang districts, which are both Zones of Tamil Nadu, India. Journal of Entomology and diverse, not a monoculture. Zoology Studies. 5(3): 541-46. Diversity index, species abundance and Chalcididae Darnaedi, Dedy and Woro Angga Noerdjito. (2007). Understanding individual abundance in rice plantations in the tidal land of Indonesian Natural Diversity/ : Insect-Collecting Methods Taught to Parataxonomists During DIWPA-IBOY Training Indragiri Hilir Regency showed the same up and down Courses. Pp. 245-250 in Proceedings of International pattern in the two planting periods (Table 5). 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