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. 2016 Aug 29;(4):e9230. doi: 10.3897/BDJ.4.e9230

First report of Cheiloneurus exitiosus (Perkins, 1906) and Helegonatopus dimorphus (Hoffer, 1954) (Hymenoptera: Encyrtidae) from Japan, with remarks on their abundance in rice paddies

Toshiharu Mita ‡,✉, Hironobu Handa §, Yoshimitsu Higashiura |, George Japoshvili
PMCID: PMC5018112  PMID: 27660532

Abstract Abstract

Background

Encyrtid secondary parasitoids of Delphacidae have not been recorded in Japan. However, they may play an important role in the rice ecosystem because they can reduce the number of Dryinidae, the natural enemies of rice planthoppers.

New information

We found two encyrtid species, Cheiloneurus exitiosus (Perkins, 1906) and Helegonatopus dimorphus (Hoffer, 1954), from rice paddies and the surrounding environment. Haplogonatopus oratorius (Westwood, 1833) and Anteon sp. were newly recognized as hosts of He. dimorphus. Parasitism of C. exitiosus was rare, but He. dimorphus was common in Kumamoto Prefecture. The sex ratio (male proportion) and clutch size of He. dimorphus was estimated as 0.19 and 4.95, respectively.

Keywords: Distribution, Haplogonatopus oratorius, host record, Laodelphax striatellus, parasitoid wasp

Introduction

Some encyrtid wasps are known as parasitoids of Dryinidae (Guerrieri and Viggiani 2005, Olmi and Xu 2015 and Xu et al. 2013). There are two genera of encyrtids reported as parasitoids of Dryinidae, namely, Cheiloneurus Westwood and Helegonatopus Perkins. Hitherto, Helegonatopus is considered the specialist of Dryinidae. Among these, H. dimorphus (Hoffer, 1954) has been widely recorded from Europe to Sakhalin (Noyes 2016). This species exhibits a peculiar sexual dimorphism. The head of the male is compressed laterally, whereas that of the female is unmodified. As for Cheiloneurus, C. exitiosus (Perkins, 1906) is recorded widely from South Asia to Oceania (Xu et al. 2013). As is often the case with small parasitoid wasps, a substantial number of Encyrtidae show a cosmopolitan distribution. Furthermore, some of their primary hosts such as rice planthoppers are known as long-distance migrants (Otuka 2013), and dryinid larvae can also be transported (Mita et al. 2013). It is possible that those primary hosts carry not only dryinid larvae, but also their hyperparasitoids. In East Asian countries, the secondary parasitoid of rice planthoppers has seldom been investigated. However, a consideration of their distribution range and the host's dispersal ability suggests they should be found widely in East Asian countries including Japan, and they may play an indispensable role in the rice ecosystem. We herein report the occurrence of these encyrtid wasps in Japan, and present results of a preliminary survey of their field abundance.

Materials and methods

Materials used in the study are preserved in 99.5% ethanol. They were mounted on pieces of cardboard or glass slides when necessary. Original pictures were taken by a digital camera (Olympus E-5) attached to an Olympus SZX10 stereomicroscope. Photo images were processed using image-stacking software (Combine ZP). Materials are deposited in the Entomological Laboratory, Faculty of Agriculture, Kyushu University (ELKU). Distribution and host records were obtained from Guerrieri and Viggiani (2005), Xu et al. (2013) and Olmi and Xu (2015).

Some encyrtid wasps collected before 2014 could not be separated into each host individual. To confirm the number of encyrtid wasps per dryinid larva, the parasitism ratio, and the sex ratio of encyrtid hyperparasitoids, specimens of Laodelphax striatellus (Fallén, 1826) parasitized by Dryinidae and dryinid cocoons on leaves were collected from rice paddies in Kumamoto and Kagoshima prefectures on Kyushu Island during September 17–28, 2014 (Table 1). Two other species of rice planthoppers, Nilaparvata lugens (Stål, 1854) and Sogatella furcifera (Horváth, 1899), were seldom collected during the survey. Cocoons were additionally collected at Suya from September to October 2014. Parasitized planthoppers were reared separately in small glass tubes plugged by cotton with a stem of rice. Field cocoons were similarly treated, but a stem was not inserted. They were kept in an incubator (25°C, 16L/8D) or the laboratory at room temperature. When no parasitoid emerged, the cocoon was dissected and any dead wasps were identified.

Table 1.

Collection sites of field survey in 2014.

Prefecture Site name Locality Latitude Longitude Date
Kumamoto Shisui Shisui-machi, Kikuchi-Shi 32.927N 130.766E 21. IX. 2014
Kumamoto Suya NARO Kyushu Okinawa Agricultural Research Center, Suya, Koshi-Shi 32.876N 130.738E 17. IX. 2014
Kumamoto Hida Hida, Kita-ku, Kumamoto-Shi 32.849N 130.720E 18, 20. IX. 2014
Kagoshima Kimpo Kagoshima Prefectural Institute for Agricultural Development, Kimpo-cho, Minamisatsuma-Shi 31.482N 130.343E 26-28. IX. 2014
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Taxon treatments

Cheiloneurus exitiosus

(Perkins, 1906)

Materials

  1. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius; eventDate: 2014-09-20/2014-10; Record Level: modified: 2015-12-05; institutionID: ELKU

  2. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Nagasaki; locality: rice paddy, Nagasaki Plant Protection Office, Kobunakoshi-machi, Nagasaki, Japan; decimalLatitude: 32.837; decimalLongitude: 130.024; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parasitised Sogatella furcifera by Haplogonatopus apicalis and rearing of adult wasps; eventDate: 2009-08-26/2009-09; Record Level: modified: 2015-12-05; institutionID: ELKU

  3. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 1; sex: 1 male; lifeStage: adult; Location: country: Japan; stateProvince: Nagasaki; locality: rice paddy, Nagasaki Plant Protection Office, Kobunakoshi-machi, Nagasaki, Japan; decimalLatitude: 32.837; decimalLongitude: 130.024; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parasitised Sogatella furcifera by Haplogonatopus apicalis and rearing of adult wasp; eventDate: 2009-08-26/2009-09; Record Level: modified: 2015-12-25; institutionID: ELKU

Distribution

American Samoa, Australia, China, Fiji, Guam, India, Malaysia, Philippines, Western Samoa (Noyes 2016), Japan, new record: Kyushu (Figs 1, 2​).

Dorsal habitus of Cheiloneurus excitiosus. Scale bar: 0.5mm.

Figure 1a.

Figure 1a.

Female.

Figure 1b.

Figure 1b.

Male.

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Head of Cheiloneurus excitiosus in dorsal view. Scale bar: 0.25mm.

Figure 2a.

Figure 2a.

Female.

Figure 2b.

Figure 2b.

Male.

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Host

Palaearctic Region: Gonatopus camelinus Kieffer, 1904 (Spain). Oriental Region: Haplogonatopus apicalis Perkins, 1905 (Malaya; Japan); H. oratorius (Westwood, 1833) (China; Japan); G. flavifemur (Esaki & Hashimoto, 1932) (Philippines); G. nigricans (Perkins, 1905) (Malaya); G. nudus (Perkins, 1912) (India).

Helegoantopus dimorphus

(Hoffer, 1954)

Materials

  1. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Shisui-machi, Kikuchi-shi, Kumamoto, Japan; decimalLatitude: 32.927; decimalLongitude: 130.766; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-21/2014-10-05; Record Level: modified: 2015-12-05; institutionID: ELKU

  2. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Shisui-machi, Kikuchi-shi, Kumamoto, Japan; decimalLatitude: 32.927; decimalLongitude: 130.766; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-21/2014-10-09; Record Level: modified: 2015-12-05; institutionID: ELKU

  3. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 3; sex: 1 male, 2 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: sweeping of parsitised nymph host planthopper (Laodelphax striatellus) and rearing of adult wasp; eventDate: 2014-09-18/2014-10-05; Record Level: modified: 2015-12-25; institutionID: ELKU

  4. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 3; sex: 1 male, 2 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: sweeping of parsitised brachipterous adult host planthopper (Laodelphax striatellus) and rearing of adult wasp; eventDate: 2014-09-18/2014-10-04; Record Level: modified: 2015-12-25; institutionID: ELKU

  5. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-18/2014-09-27; Record Level: modified: 2015-12-25; institutionID: ELKU

  6. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-18/2014-10-04; Record Level: modified: 2015-12-25; institutionID: ELKU

  7. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-20/2014-09-30; Record Level: modified: 2015-12-25; institutionID: ELKU

  8. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 3; sex: 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-20/2014-09-27; Record Level: modified: 2015-12-25; institutionID: ELKU

  9. Type status: Other material. Occurrence: recordedBy: Hironobu Handa; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Hida, Kita-ku, Kumamoto, Japan; decimalLatitude: 32.849; decimalLongitude: 130.720; Identification: identifiedBy: Hironobu Handa; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and rearing of adult wasp; eventDate: 2014-09-20/2014-10-05; Record Level: modified: 2015-12-25; institutionID: ELKU

  10. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-30/2014-09-04; Record Level: modified: 2015-12-25; institutionID: ELKU

  11. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 6 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-30/2014-09-04; Record Level: modified: 2015-12-25; institutionID: ELKU

  12. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-30/2014-09-06; Record Level: modified: 2015-12-25; institutionID: ELKU

  13. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-30/2014-09-07; Record Level: modified: 2015-12-25; institutionID: ELKU

  14. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 3; sex: 1 male, 2 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-30/2014-09-08; Record Level: modified: 2015-12-25; institutionID: ELKU

  15. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-31/2014-09-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  16. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-31/2014-09-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  17. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 8; sex: 2 males, 6 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-31/2014-09-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  18. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-31/2014-09-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  19. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-08-31/2014-09-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  20. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09-01/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  21. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 9; sex: 3 males, 6 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09-01/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  22. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 7; sex: 3 males, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09-01/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  23. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09-01/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  24. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-17; Record Level: modified: 2015-12-25; institutionID: ELKU

  25. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-17; Record Level: modified: 2015-12-25; institutionID: ELKU

  26. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 1 male, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-17; Record Level: modified: 2015-12-25; institutionID: ELKU

  27. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-20; Record Level: modified: 2015-12-25; institutionID: ELKU

  28. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-20; Record Level: modified: 2015-12-25; institutionID: ELKU

  29. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 1 male, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-26; Record Level: modified: 2015-12-25; institutionID: ELKU

  30. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 6; sex: 1 male, 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-10-01; Record Level: modified: 2015-12-25; institutionID: ELKU

  31. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-10; Record Level: modified: 2015-12-25; institutionID: ELKU

  32. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-10; Record Level: modified: 2015-12-25; institutionID: ELKU

  33. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  34. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 3; sex: 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-12; Record Level: modified: 2015-12-25; institutionID: ELKU

  35. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 5; sex: 5 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-17; Record Level: modified: 2015-12-25; institutionID: ELKU

  36. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 3; sex: 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-17; Record Level: modified: 2015-12-25; institutionID: ELKU

  37. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: adult wasp emerged from coccoon of Haplogonatopus oratorius; eventDate: 2014-09/2014-09-26; Record Level: modified: 2015-12-25; institutionID: ELKU

  38. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 7; sex: 3 males, 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and examined dead adult wasp; eventDate: 2014-09-20/2014-10; Record Level: modified: 2015-12-25; institutionID: ELKU

  39. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 1; sex: 1 male; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and examined dead adult wasp; eventDate: 2014-10-02; Record Level: modified: 2015-12-25; institutionID: ELKU

  40. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 1; sex: 1 male; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and examined dead adult wasp; eventDate: 2014-10-02; Record Level: modified: 2015-12-25; institutionID: ELKU

  41. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 1; sex: 1 male; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, NARO Kyushu Okinawa Agricultural Research Center, Koshi, Kumamoto, Japan; decimalLatitude: 32.876; decimalLongitude: 130.738; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of Haplogonatopus oratorius and examined dead adult wasp; eventDate: 2014-10-02; Record Level: modified: 2015-12-25; institutionID: ELKU

  42. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 4; sex: 4 females; lifeStage: adult; Location: country: Japan; stateProvince: Kumamoto; locality: rice paddy, Kamo-cho, Yamaga-shi, Kumamoto, Japan; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting coccoon of rice planthopper and rearing of adult wasps; eventDate: 2009-08-19/2009-08; Record Level: modified: 2015-12-25; institutionID: ELKU

  43. Type status: Other material. Occurrence: recordedBy: Atsuhito Sakai; individualCount: 3; sex: 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kanagawa; locality: rice paddy, Funako, Atsugi-shi, Kanagawa, Japan; decimalLatitude: 35.434; decimalLongitude: 139.351; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parsitised host planthopper (Laodelphax striatellus) and rearing of adult wasps; eventDate: 2010-09-17/2010-10; Record Level: modified: 2015-12-25; institutionID: ELKU

  44. Type status: Other material. Occurrence: recordedBy: Atsuhito Sakai; individualCount: 5; sex: 2 males, 3 females; lifeStage: adult; Location: country: Japan; stateProvince: Kanagawa; locality: rice paddy, Funako, Atsugi-shi, Kanagawa, Japan; decimalLatitude: 35.434; decimalLongitude: 139.351; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parsitised host planthopper (Laodelphax striatellus) and rearing of adult wasps; eventDate: 2010-09-15/2010-10; Record Level: modified: 2015-12-25; institutionID: ELKU

  45. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 42; sex: 11 males, 31 females; lifeStage: adult; Location: country: Japan; stateProvince: Nagasaki; locality: rice paddy, Nagasaki Plant Protection Office, Kobunakoshi-machi, Nagasaki, Japan; decimalLatitude: 32.837; decimalLongitude: 130.024; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parasitised Sogatella furcifera by Haplogonatopus apicalis and rearing of adult was, pmultipul individuals of hosts kept in same tube; eventDate: 2009-08-26/2009-09; Record Level: modified: 2015-12-25; institutionID: ELKU

  46. Type status: Other material. Occurrence: recordedBy: Naomichi Ohara; individualCount: 4; sex: 3 males, 1 female; lifeStage: adult; Location: country: Japan; stateProvince: Saitama; locality: grassland, Ooasou-kouen, Kumagaya-shi, Saitama, Japan; decimalLatitude: 36.143; decimalLongitude: 139.348; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: sweeping of parasitised Hecalus sp. by Anteon sp. and rearing adult wasp; eventDate: 2008-10-20/2008-11; Record Level: modified: 2015-12-25; institutionID: ELKU

  47. Type status: Other material. Occurrence: recordedBy: Toshiharu Mita; individualCount: 2; sex: 2 females; lifeStage: adult; Location: country: Japan; stateProvince: Fukuoka; locality: fallow field, Sasaguri-machi, Fukuoka, Japan; Identification: identifiedBy: Toshiharu Mita; dateIdentified: 2014; Event: samplingProtocol: collecting of cocoon of Haplogonatopus sp. and rearing of adult wasp; eventDate: 2009-08-11/2009-08; Record Level: modified: 2015-12-25; institutionID: ELKU

Distribution

Widely distributed from western Palaearctic countries to Mongolia (Noyes 2016), Japan, new record: Honshu, Kyushu (Figs 3, 4).

Dorsal habitus of Helegonatopus dimorphus. Scale bar: 0.5 mm

Figure 3a.

Figure 3a.

Female.

Figure 3b.

Figure 3b.

Male.

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Head of Helegonatopus dimorphus in dorsal view. Scale bar: 0.25mm.

Figure 4a.

Figure 4a.

Female.

Figure 4b.

Figure 4b.

Male.

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Biology

Host

Palaearctic Region: Anteon sp., new record (Japan); Haplogonatopus oratorius (Westwood, 1833), new record (Japan); Gonatopus clavipes (Thunberg, 1827) (Italy); G. solidus (Haupt, 1938) (Italy); G. formicicolus (Richards, 1939) (Italy); G. pallidus (Ceballos, 1927) (Sweden); G. rosellae (Currado & Olmi, 1974) (Italy).

Discussion

Dryinidae and Encyrtidae collected by field survey in 2014

Through our survey in 2014, two dryinids, Gonatopus nigricans (Perkins) and Haplogonatopus oratorius (Westwood), emerged from Laodelphax striatellus (Fallén) and dryinid cocoons collected from the field. All hyperparasitoids were identified as Helegonatopus dimorphus, but a cocoon collected at Hida was parasitized by Cheiloneurus exitiosus. We found two other examples of C. exitiosus emergence from Ha. apicalis parasitizing Sogatella furcifera in Saga Prefecture. This species seems to be rare in Japan, or they simply might not prefer L. striatellus. On the other hand, He. dimorphus was widely found from central Honshu (Saitama and Kanagawa) to Kyushu (Fukuoka, Kumamoto). The rearing of parasitized planthoppers revealed that two dryinid larvae were parasitized by Encyrtidae in Hida (Table 2). The proportion of parasitized field cocoons differed greatly and depended on the site of collection (Table 3). The highest score of 87.9% was recorded in Suya. Since the proportion of G. nigricans in Kumamoto was very low (2.1%, compared to 50.0% in Kagoshima), dryinids attacked by encyrtids were regarded as Ha. oratorius. No hyperparasitoid was found in Kagoshima.

Table 2.

Parasitized Laodelphax striatellus and emerged parasitoids collected by field survey in 2014.

Laodelphax striatellus Haplogonatopus oratorius Gonatopus nigricans Helegonatopus dimorphus Cheiloneulus exitiosus
Suya 3 3 0 0 0
Shisui 30 30 0 0 0
Hida 73 70 1 2 0
Kimpo 54 28 26 0 0
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Table 3.

Field cocoons and emerged parasitoids collected by field survey in 2014.

Cocoon Haplogonatopus oratorius Gonatopus nigricans Helegonatopus dimorphus Cheiloneurus exitiosus
Suya 33 4 0 29 0
Shisui 26 24 0 2 0
Hida 17 9 2 5 1
Kimpo 2 0 2 0 0
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Clutch size and sex ratio of Helegonatopus dimorphus

Olmi and Xu (2015) reported that 10–12 individuals of He. dimorphus emerged from a cocoon of G. rosellae (Currado & Olmi, 1974), while 7 individuals were recorded as having emerged from G. solidus (Haupt, 1938) in Italy. According to our field survey, 3–8 (mean 4.95±1.40SD) individuals emerged from Ha. oratorius. The average male proportion is 0.19 (Table 4), and represents 0.95 per clutch. The smaller number relative to the other two dryinid species may be due to the smaller body size (2.0–3.1 mm for the females of Ha. oratorius, compared to 3.0–3.4 mm in G. solidus and 3.5–3.8 mm in G. rosellae). This number is similar to that of He. pseudophanes (Perkins, 1906) in Argentina where they attack Gonatopus bonaerensis Virla, 1997 (2.4–3.2 mm) and G. desantisi Olmi & Virla, 1992 (2.9–3.2 mm), and exhibit a clutch size of 6 and male proportion of 0.32 (De Santis and Virla 1991).

Table 4.

Two encyrtid species collected by field survey in 2014.

Clutch number Emerged number Sex ratio (male proportion)
Helegonatopus dimorphus 38 188 0.19
Cheiloneulus exitiosus 1 5 0.20
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Host stage

As for C. exitiosus, they attack the "later instar" larva of G. nudus (Perkins, 1912) (as Pseudogonatopus nudus) (Manickavasagam et al. 2009). According to the ovservations of De Santis and Virla (1991), both genera may have the ability to begin attacking from the larval-sac stage on the primary host to the pupa in the cocoon. In the present study, we confirmed that He. dimorphus can attack the larval sac, but the proportion of this parasitism is much smaller than that of the cocoon. The higher proportion of parasitism can be at least partially explained by the difference in developmental period. The developmental period of the larval sac of Ha. oratorius (as Ha. atratus, 4.5 days at 25°C) is shorter than the period from removal from the host planthopper to adult emergence (11.2 days) (Kitamura 1983). Our results indicate that L. striatellus possibly transports its primary and secondary parasitoid together, but the amount of secondary parasitoid should be very limited not only because of their scarcity. Host stage preference should be investigated to understand the effect on host-parasitoid dispersal dynamics.

Supplementary Material

XML Treatment for Cheiloneurus exitiosus
BDJ.4.e9230-treatment1.xml (15.3KB, xml)
XML Treatment for Helegoantopus dimorphus
BDJ.4.e9230-treatment2.xml (136.8KB, xml)

Acknowledgements

We are grateful to Masaya Matsumura, Reiko Otsu, Naomichi Ohara, Akihito Sakai, and Ken Teramoto for their help in field surveys, and the various land owners for allowing us to collect samples. This study was partly supported by the Grant-in-Aid for JSPS Fellows (26-3756) and KAKENHI (26850032).

References

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

XML Treatment for Cheiloneurus exitiosus
BDJ.4.e9230-treatment1.xml (15.3KB, xml)
XML Treatment for Helegoantopus dimorphus
BDJ.4.e9230-treatment2.xml (136.8KB, xml)

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