Journal Search Engine
Search Advanced Search Adode Reader(link)
Download PDF Export Citaion korean bibliography PMC previewer
ISSN : 1225-0171(Print)
ISSN : 2287-545X(Online)
Korean Journal of Applied Entomology Vol.56 No.1 pp.87-92
DOI : https://doi.org/10.5656/KSAE.2017.01.1.064

Host Records of Trissolcus (Hymenoptera: Platygasteridae: Telenominae) Parasitizing Eggs of Stink Bugs in Korea

Kyoung Young Kim, Deok-Soo Choi1, Jun-Yeol Choi2, Ki-Jeong Hong*
Department of Plant Medicine, Sunchon National University, Suncheon, Jeonnam 57922, Republic of Korea
1Environment-friendly Agriculture Research Center, Jellanamdo Agricultural Research & Extension Service, Naju, Jeonnam 58213, Republic of Korea
2Research Policy Bureau, Rural Development Administration, Jeonju, Jeonbuk 54875, Republic of Korea
Corresponding author:curcul@sunchon.ac.kr
October 8, 2016 January 8, 2017 February 22, 2017

Abstract

The Samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera: Platygasteridae) is recognized as a solitary parasitoid on eggs of the stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), an economic pest causing severe damage to fruits, in South Korea. The wasp appears to be a potential biological agent of the pest. In addition, T. itoi Ryu and T. nigripedius (Nakagawa) were found to parasitize eggs of Eurydema gebleri Kolenati and Dolycoris baccarum Linnaeus, respectively. Diagnostic characters and photographs are provided for identification, and host records of Korean Trissolcus species are also given.


노린재류의 알에 기생하는 Trissolcus 속(벌목: 납작먹좀벌과)의 숙주

김 경용, 최 덕수1, 최 준열2, 홍 기정*
순천대학교 식물의학과
1전라남도농업기술원 친환경농업연구소
2농촌진흥청 연구운영과

초록

납작먹좀벌과(Platygasteridae)의 큰검정알벌속(Trissolcus)에 속하는 T. japonicus (Ashmead) (썩덩큰검정알벌, 신칭)이 과수원에서 과일 에 심한 피해를 일으키는 해충인 썩덩나무노린재의 알에 기생하는 것으로 확인되었고, 생물적 방제인자로써 가능성이 기대된다. 또한 천마큰검정 알벌(T. itoi Ryu)이 북쪽비단노린재 알을, 검은다리큰검정알벌(T. nigripedius Nakagawa)이 알락수염노린재 알을 숙주로 각각 기생하는 것이 확 인되었다. 동정을 위한 진단형질 및 영상자료와 한국에 분포하는 큰검정알벌속(Trissolcus)의 종들에 관한 숙주목록을 제공하였다.


    Korea Institute of Planning and Evalution for Technology of Food, Agriculture, Forestry and Fisheries
    115091-2

    Trissolcus is a cosmopolitan genus in Platygasteridae (Hymenoptera) and a relatively large group including 161 described species worldwide (69 species in the Palearctic region) (Johnson, 1992). Most species of the genus are egg parasitoids of economically important pests in Pentatomoidea (Hemiptera). Therefore, they are generally considered as potential agents for biological control, and some of them had been used for biological controls in practice (e.g. Johnson, 1984; Corrêa-Ferreira and Moscardi, 1996).

    Trissolcus looks very similar to Telenomus but can be readily distinguished by 1) female antennal clava compact and composed of six segments, 2) frons sculptured throughout, and with preoccellar pit located below the median ocellus, 3) scutellum with surface sculpture, 4) second metasomatic tergite wider than long, and 5) eyes seeming glabrous under low magnification (Masner, 1980; Johnson, 1991). The two genera have different biological characteristics like that the former almost exclusively parasitizes the eggs of Pentatomoidea, and the latter predominantly the eggs of Lepidoptera (Ryu and Hirashima, 1984).

    To date six species of Trissolcus and their hosts have been known from Korea (Yasumastu, 1975; Ryu and Hirashima, 1984). In the present paper, we add the Samurai wasp, T. japonicus (Ashmead) as an egg parasitoid of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) to the Korean insect fauna, and newly confirm that T. itoi Ryu and T. nigripedius (Nakagawa) parasitize the eggs of Eurydema gebleri Kolenati and Dolycoris baccarum L., respectively.

    Materials and Methods

    Surveys for natural insect enemies of pentatomid pests were conducted mainly in soybean fields and deciduous forests in Jeonnam province, Korea from May to September, 2016. Egg masses of stink bugs laid on the underside of leaves were collected and kept individually in plastic dishes (10 cm in diameter and 4 cm in height). The egg masses were reared in the laboratory at room temperature (≒25°C) and checked daily until parasitoids emerged from the host eggs. Leica EZ4 HD binocular stereo microscope (Leica Microsystems, Wetzlar, Germany) was used for imaging and identification the parasitoids collected and CombineZM (Free software released from http://www.hadleyweb.pwp.blueyonder.co.uk/; UK) for photo-stacking. The voucher specimens are deposited in the insect collection room of Sunchon National University, Suncheon, Korea.

    The key to species by Ryu and Hirashima (1984) is referred for species identification of the parasitoids, and descriptive terminology for morphological characters is taken from Talamas et al. (2015). Acronyms used in the text are as follows: JN, Jeollanam-do (Province); JARES, Jeonnam Agricultural Research & Extension Services; SCNU, Sunchon National University; TL, type locality.

    Results

    Trissolcus japonicus (Ashmead) 썩덩큰검정알벌(신칭) (Figs. 1-a, b; 2-a, b; 3-a, b; 4-a, b, c)

    Dissolcus japonicusAshmead, 1904: 73 (TL: Japan).

    Asolcus plautiaeWatanabe, 1954: 18, 22 (TL: Japan).

    Trissolcus halyomorphae Yang, in Yang et al., 2009: 40 (TL: China).

    Diagnosis. Body length: 1.3-1.4 mm (♀) and 1.2 mm (♂).

    ♀: Black. Antennae dark brown to black except for scape and pedicel which are yellowish brown. Legs yellowish brown with coxae black and femora infuscated. Antennae 11-segmented; pedicel shorter than 1st funicular segment; 2nd funicular segment distinctly longer than broad. Oribital furrow present. Mesoscutum with notauli sharply defined posteriorly. Scutellum smooth and shining. ♂: Antennae 12-segmented, and brown except for sixth to tenth flagellar segments which are tinged with dark brown. Legs yellowish brown except for coxae and hind femora which are somewhat infuscated.

    Materials examined. 8♀♀, 1♂, emerged at 4-5. VIII. 2016, at room temperature from an egg-mass (28 eggs) of Halyomorpha halys (Pentatomidae) collected at 26. VII. 2016, Suwol-ri, Gwangui-myeon, Gurye, JN (SCNU); 8♀♀, 1♂, emerged at 6. VIII. 2016, at room temperature from egg-mass of Halyomorpha halys (Pentatomidae) collected at 2. VIII. 2016, Woesan-ri (Jicho), Sandong-myeon, Gurye, JN (JARES).

    Hosts.Plautia stali Scott, P. splendens Distant, Elasmucha putoni Scott, Halyomorpha halys Stål.

    Distribution. Korea (South), Japan (Kyushu, Honshu, Shikoku), China (Beijing, Shandong, Hebei).

    Remarks.Talamas et al. (2015) examined four Korean specimens (3♀♀ and 1♂) that kept in the Smithsonian National Museum of Natural History, Washington DC, USA. We have given this species a Korean name in this paper.

    Trissolcus itoi Ryu, 1984 천마큰검정알벌 (Figs. 1-c, d; 2-c, d; 3-c, d; 4-d)

    Trissolcus itoi Ryu in Ryu and Hirashima, 1984: 37, 52 (TL: Japan).

    Diagnosis. Body length: 0.9-1.0 mm (♀) and 0.9 mm (♂).

    ♀: Black. Antennae dark brown to black; basal and apical parts of scape tinged with yellowish brown and club somewhat darker. Legs brown with coxae black, femora remarkably infuscated. Antennae 11-segmented; pedicel about as long as 1st funicular segment. Mesoscutum without notauli. Scutellum strongly sculptured with irregular wrinkles as in posterior part of mesoscutum. ♂: Antennae 12-segmented, and brownish to dark brown. Legs brownish except for femora which are infuscated; hind femora darker than other femora.

    Materials examined. 6♀♀, 1♂, emerged at 2. VIII. 2016, at room temperature from an egg-mass of Dolycoris baccarum (Pentatomidae) collected at 28. VII. 2016, Sindae-ri, Haeryongmyeon, Suncheon, JN (SCNU); 5♀♀, 1♂, emerged at 15. VIII. 2016, at room temperature from an egg-mass of Dolycoris baccarum (Pentatomidae) collected at 6. VIII. 2016, ditto (SCNU).

    Hosts.Homalogonia obtusa (Walker), Elasmucha putoni Scott, Eurydema gebleri Kolenati.

    Distribution. Korea (Central, South), Japan (Honshu, Shikoku).

    Trissolcus nigripedius (Nakagawa, 1900) 검은다리큰검정 알벌

    (Figs. 1-e, f; 2-e, f; 3-e, f; 4-e)

    Asolcus nigripediusNakagawa, 1900: 17 (TL: Japan).

    Diagnosis. Body length: 1.1-1.2 mm (♀) and 1.0 mm (♂).

    ♀: Black. Antennae dark except for junction of scape and apex of pedicel which is somewhat yellowish brown. Legs yellowish brown except for coxae which are black; femora sometimes infuscated. Antennae 11-segmented; pedicel as long as 1st funicular segment. Mesoscutum without notauli. Scutellum weakly tessellate, much less strongly sculptured than in posterior part of mesoscutum. Mediotergite I with distinct longitudinal striae. ♂: Antennae 12-segmented, and brownish black; sixth to tenth flagellar segments somewhat darker than other segments.

    Materials examined. 22♀♀, 3♂♂, emerged at 24. VIII. 2016, at room temperature from an egg-mass of Nezara antennata (Pentatomidae) collected at 17. VIII. 2016, Namsandong, Gwangsan-gu, Gwangju, JN (SCNU); 21♀♀, 2♂♂, emerged at 5. VIII. 2016, at room temperature from an eggmass of Nezara antennata (Pentatomidae) collected at 2. VIII. 2016, Jigok-ri, Bonggang-myeon, Gwangyang, JN (SCNU).

    Host.Dolycoris baccarum L.

    Distribution. Korea (South), Japan (Kyushu, Honshu, Hokkaido, Shikoku).

    Discussion

    The most common stink bug are serious agricultural pests that has been readily causing damage to crops. To obtain their food, stink bugs use their stylets to pierce the plant tissue in order to extract the plant fluids. The most common signs of stink bug damage are pitting and scarring of the fruit, leaf destruction, and a mealy texture to the harvested fruits and vegetables. In most cases the signs of stink bug damage makes the plant unsuitable for sale in the market as the insides are usually rotten. They are a threat to soybeans, ornamental trees, shrubs, vines, weeds, and many cultivated crops. In Korea, several stink bugs such as Halyomorpha halys (Stal) and Plautia stali Scott have recently become serious pests of fruits such as persimmons and citruses (Kim et al., 2014; Park et al., 2015).

    Many species of Trissolcus are egg parasitoids of economically important pests in the superfamily Pentatomoidea (Hemiptera) in Korea and neighboring countries (Table 1). Three species of the genus found in the present work are confirmed as egg parasitoids of Halyomorpha halys (Stål), Eurydema gebleri Kolenati and Dolycoris baccarum L. that are severe pests to many cultivated crops. It is expected that these solitary endoparasitoids in the many pentatomid eggs are developed as excellent biological control agents through the investigation of biological characters including sex ratio, developmental time, parasitism rate, mass rearing, and so on.

    Especially, the brown marmorated stink bug (BMSB), Halyomorpha halys Stål (Hemiptera: Pentatomidae), was accidentally introduced into the United States from native area to China, Japan, Korea or Taiwan. The first documented specimen was collected in Allentown, Pennsylvania, in September 1998. A decade after its introduction into the United States, the BMSB has been detected in 39 US states as well as Cananda, Switzerland, Germany, France, and Italy, and has been intercepted in New Zealand (Xu et al., 2014). Due to the potential non-target effects of controlling the BMSB with pesticides, USDA conducted foreign exploration in Asia for natural enemies of BMSB in South Korea and China (Xu et al., 2014). As the result, two parasitoid, Trissolcus japonicus (Ashmead) and Trissolcus cultratus (Mayr) are considered with potential as classical biological control agents, and are presently studying the host preferences of these parasitoids and the ability of these parasitoids to successfully develop in BMSB eggs (Talamas et al., 2015).

    Acknowledgment

    This work was supported by a grant from the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) of Republic of Korea (Project No. 115091-2).

    KSAE-56-87_F1.gif

    Lateral habitus of Trissolcus species. T. japonicus (Ashmead) (a: female, b: male); T. itoi Ryu (c: female, d: male); T. nigripedius (Nakagawa) (e: female, f: male).

    KSAE-56-87_F2.gif

    Dorsal habitus of Trissolcus species. T. japonicus (Ashmead) (a: female, b: male); T. itoi Ryu (c: female, d: male); T. nigripedius (Nakagawa) (e: female, f: male).

    KSAE-56-87_F3.gif

    Dorsal view of the head of Trissolcus species. T. japonicus (Ashmead) (a: female, b: male); T. itoi Ryu (c: female, d: male); T. nigripedius (Nakagawa) (e: female, f: male).

    KSAE-56-87_F4.gif

    Host eggs of Trissolcus parasitoids. a. egg-mass of Halyomorpha halys (Stål); b-c. emergence of a male (b) and a female (c) of T. japonicus (Ashmead); d. egg-mass of Eurydema gebleri Kolenati, the host of T. itoi Ryu; e. egg-mass of Dolycoris baccarum L. with an emerged adult of T. nigripedius (Nakagawa).

    Species of Trissolcus and their hosts known from Korea, Japan and China

    Reference

    1. Ashmead WH (1904) Descriptions of new Hymenoptera from Japan , J. New York ent. Soc, Vol.12 (2) ; pp.86-99
    2. Corrêa-Ferreira BS , Moscardi F (1996) Biological control of soybean stink bugs by inoculative releases of Trissolcus basalis , Entomol. Exp. Appl, Vol.79 ; pp.1-7
    3. He J-H (2004) Hymenopteran insect fauna of Zhejiang, Science Press,
    4. Johnson NF (1984) Revision of the Nearctic species of the favipes group (Hymenoptera: Scelionidae) , Proc. Entomol. Soc. Wash, Vol.86 ; pp.797-807
    5. Johnson NF (1991) Revision of Australasian Trissolcus species (Hymenoptera: Scelionidae) , Invertebr. Taxon, Vol.5 ; pp.211-239
    6. Johnson NF (1992) Catalog of world species of Proctotrupoidea, exclude Platygasteridae (Hymenoptera), Memories of American Entomological Institute, ; pp.1-825
    7. Kim S , Kwon S , Chang Y , Yang Y , Hyun S , Song J , Kim D (2014) Damage and Control Strategy of Halyomorpha halys Stål in Citrus Orchard, Scientific Abstract of Spring Congress of the Korean Society of Applied Entomology, ; pp.269
    8. Masner L (1980) Key to genera of Scelionidae of the Holarctic Region, with descriptions of new genera and species (Hymenoptera: Proctotrupoidae) , Mem. Entomol. Soc. Can., ; pp.1-54
    9. Nakagawa H (1900) Illustration of some Japanese Hymenoptera parasitic on insect eggs , I. Spec. Rep. Agric. Exp. Stat, Vol.6 ; pp.l-26
    10. Park CG , Kwon JH , Lee DW (2015) An Illustrated Color Guide Book to Insect Pests and Diseases of Persimmon in Korea, Animal and Plant Quarantine Agency, ; pp.147
    11. Ryu J , Hirashima Y (1984) Taxonomic studies on the genus Trissolcus Ashmead of Japan and Korea (Hymenoptera, Scelionidae) , Journal of the Faculty of Agriculture Kyushu University, Vol.29 ; pp.35-58
    12. Talamas EJ , Johnson NF , Buffington M (2015) Key to Nearctic species of Trissolcus Ashmead (Hymenoptera, Scelionidae), natural enemies of native and invasive stink bugs (Hemiptera, Pentatomidae) , Journal of Hymenoptera Research, Vol.43 ; pp.45-110
    13. Watanabe C (1951) On five Scelionid egg-parasites of some Pentatomid and Coreid bugs from Shikoku, Japan (Hymenoptera:Proctotrupoidea) , Trans. Shikoku Ext. Sot, Vol.2 (2) ; pp.17-26
    14. Watanabe C (1954) Discovery of four new species of Telenominae, egg parasites of pentatomid and plataspid bugs, in Shikoku, Japan , Transactions of the Shikoku Entomological Society, Vol.4 ; pp.17-22
    15. Xu J , Foneseca DM , Hamilton GC , Hoelmer KA , Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys , Biological Invasions, Vol.16 ; pp.153-166
    16. Yang ZQ , Yao XY , Qiu LF , Li ZX (2009) A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology , Annals of the Entomological Society of America, Vol.102 ; pp.39-47
    17. Yasumastu K (1975) Preliminary studies on the taxonomy of natural enemies of agricultural pests for the development of integrated control programmes, FAO, ; pp.32