Appl. Entomol. Zool. 41 (2): 247–267 (2006) http://odokon.org/

A taxonomic review of the Japanese (: ) with descriptions of three new

Jeffrey Y. HONDA,1,2,* Laurel TAYLOR,1 Josephine RODRIGUEZ,1,† Naoya YASHIRO3 and Yoshimi HIROSE2,‡ 1 Department of Biological Sciences, San Jose State University; CA 95192–0100, USA 2 Institute of Biological Control, Faculty of Agriculture, Kyushu University; Fukuoka 812–8581, 3 Naruo Senior High School; Nishinomiya 663–8182, Japan (Received 16 August 2005; Accepted 24 December 2005)

Abstract Numerous errors and confusion in the literature concerning the Trichogramma in Japan have necessitated a for- mal review of this genus. This review corrects and updates Trichogramma host and distribution records from Hokkaido to the Ryukyu Islands, redescribes and designates a lectotype for T. jezoense Ishii, records two Tri- chogramma species new to Japan (T. ostriniae Pang and Chen and T. lingulatum Pang and Chen) and describes three new species (T. yabui Honda and Taylor, T. okinawae Honda, and T. aomoriense Honda). Additionally a key to the species is provided for the 14 known Japanese species as are ITS-2 DNA sequences and SEM micrographs of male genital capsules for the majority of the species to aid biocontrol workers in Trichogramma identification.

Key words: ; species description; Japanese Trichogramma; DNA sequence; male genital capsule

of Trichogramma japonicum Ashmead precluded it INTRODUCTION from being an effective biological control agent Egg parasitoids of the genus Trichogramma (Iyatomi, 1943; Shibuya and Iyatomi, 1950). More Westwood (Hymenoptera: Trichogrammatidae) recent releases of Trichogramma species against parasitize pests in over 32 million hectares the diamond back , Plutella xylostella (Lin- of agricultural land and forests yearly (Li, 1994), naeus) (Iga, 1987; Miura et al., 2001; Miura, 2003) and have been utilized as biological control agents and the tobacco budworm, Helicoverpa armigera for more than 100 years (Smith, 1996). Of the ap- Hübner (Kakimoto et al., 1998) have been per- proximately 180 species described worldwide, formed, but their use is still being evaluated. Three about 70 species have been employed in biological other species have been apparently imported into control programs concentrating on various crops Japan. Iwasaki et al. (1998) released Trichogramma (corn, rice, wheat, sorghum, sugarcane, sugar beet, evanescens Westwood imported from France for cotton, and soybean); fruits (apple, plum, citrus, the control of Mamestra brassicae (Linnaeus) in avocado, and vineyards); and forest trees (pines sugar beet fields in Hokkaido in 1997, but it is un- and spruce) (Li, 1994; Pinto, 1999). known if these releases became established. In Japan, Trichogramma were first used against Trichogramma ostriniae Pang and Chen was im- the rice stem borer, Chilo suppressalis (Walker), in ported from Taiwan in Japan in 1987 (Hirashima et paddy fields during 1930–1940 with little success. al., 1990), but it was not released in the field In separate field trials, it was concluded that Tri- (Miura, pers. communication). However, Hirai chogramma chilonis Ishii parasitism rates were too (2004) recorded T. ostriniae as an indigenous natu- low for controlling C. suppressalis (Shibuya and ral enemy of Ostrinia furnacalis (Guenée) and Yamashita, 1936), while high superparasitism rates some tortricids from Japan, but this record was

*To whom correspondence should be addressed at: E-mail: [email protected] † Present address: Department of Entomology, 320 Morrill Hall, University of Illinois, 505 S. Goodwin Ave., Urbana, IL 61801, USA ‡ Present address: 349 Asano, Munakata 811–3415, Japan DOI: 10.1303/aez.2006.247

247 248 J. Y. HONDA et al. never verified. Test releases using Hirai’s cultured species such as the dorsal lamina were not ade- material was later used for O. furnacalis control in quately described. Minamikawa (1964) later listed corn fields in 1992–93 (Yoshizawa, 1995). Tri- the following Trichogramma species from Japan: chogramma brassicae Bezdenko, another imported Trichogramma australicum Girault, T. chilonis species of Trichogramma, was used in test releases Ishii, T. dendrolimi Matsumura, T. evanescens for the control of M. brassicae in sugar beet fields Westwood, T. japonicum and T. jezoensis Ishii. A in 1997 (Iwasaki et al., 1998) and for the control of seventh Trichogramma species, T. papilionis Na- P. xylostella in greenhouses in 1999 (Miura et al., garkatti, was added to the Japanese fauna (Na- 2001). Again their establishment has not been con- garkatti, 1974). Since this time the status of Japan- firmed. ese Trichogramma taxonomy has changed greatly. Despite the considerable international attention Nagarkatti and Nagaraja (1979) concluded that that Trichogramma has received as an important bi- Asian populations originally identified as T. aus- ological control agent, its taxonomy remains inade- tralicum were actually T. chilonis and were subse- quately understood for a number of reasons. For quently synonymized. Pinto et al. (1982) later des- example, the collection and curation of these ignated a lectotype for T. australicum and stated it minute (approximately 0.5 mm) parasitic wasps has remains known only from Girault’s original mate- proven difficult and greatly slowed the accumula- rial collected in Queensland, . Thus, T. tion of study material (Platner et al., 1999). More- australicum should no longer be considered a over, the early disregard of type specimens has species found in Japan. Questions regarding the caused much confusion in the literature. Because a exact identity of T. evanescens were brought to number of type specimens are lost, unusable, or de- light by Sugonyaev (1986) and Pinto (1999). It scribed inadequately, many species names have may be impossible to accurately assign this name been applied incorrectly and inconsistently in the to a specimen since the holotype of this species is a literature (Pinto et al., 1978; Pinto and Stouthamer, damaged female. Although both Ishii (1941) and 1994; Pinto, 1999). Finally, Trichogramma taxon- Nagarkatti and Nagaraja (1971) recorded T. omy also suffered from an absence of consistent evanescens from Japan, their identifications may be distinguishing morphological characters (Pinto, erroneous as is discussed later in this paper. The 1999). This dilemma was partially resolved by Na- status of T. jezoensis has also been questioned. garkatti and Nagaraja (1971) who discovered the Thought to be lost, we have found Ishii’s original importance of the male genitalia as a diagnostic material and designate a lectotype herein. Finally, taxonomic character. DNA sequences have also four new species recently have been described been proposed as an aid to identification and used from Japan: T. yawarae Hirai and Fursov (1998), T. in a number of studies to characterize Trichogramma kurosuae Taylor, Yashiro, Hirose, and Honda (Tay- species (Pinto et al., 1997; Silva et al., 1999; lor et al., 2005), T. cultellus Jose, and T. umerus Stouthamer et al., 1999). Jose (Jose et al., 2005). The history of Trichogramma taxonomy in Japan This paper represents the first revision of Japan- exemplifies many of the taxonomic difficulties ese Trichogramma. Herein we describe three new prevalent in the genus. For example, Nakagawa species and confirm two Trichogramma species (T. (1900) was the first to record Trichogramma from ostriniae Pang and Chen and T. lingulatum Pang Japan by describing in morphological detail, the and Chen) new to Japan. We provide a species key adult of a Trichogramma species parasitic on eggs for all the known species of Japan, in addition to of the rice stem borer. Although it has been sus- photomicrographs, and diagnostic descriptions of pected that this first description may be of T. japon- male genital capsules for most of the previously icum, it can not be confirmed as none of the origi- described Trichogramma species except for T. nal material exists. Much later, Ishii (1941) was the kurosuae, T. cultellus, and T. umerus that were re- first to produce a key to six Japanese Trichogramma cently covered in detail. Additionally, ITS2-DNA species based on male genitalia; however, it proved sequences that may aid workers in properly identi- little value as it lacked quantitative measures to aid fying Trichogramma have been identified, and we in species discrimination. Moreover, morphologi- document reliable host records that we have veri- cally important characters presently used to define fied through examination of preserved Tri- The Trichogramma of Japan 249 chogramma material including some material from raja (1971): 18–20. Ishii’s original collections. Although the literature Diagnosis. This species appears to be common has recorded many hosts of Trichogramma species in disturbed agricultural settings and is most likely from Japan, most of the host records including to be confused with T. evanescens and T. brassicae. those of Ishii (1941) and Minamikawa (1964) may However, as Pinto (1999) points out, there is much be unreliable as their Trichogramma identifications confusion as to what constitutes either species as may have been inaccurate. some researchers consider them conspecific. To We feel such a treatment is necessary at this time further confuse matters, both Ishii (1941) and not only because many new species are being de- Nagarkatti and Nagaraja (1971) reported that T. scribed in Japan, but also because of the apparent evanescens occurs in Japan. We examined material introduction of species into Japan. Accurate from Ishii’s collection and determined what he de- species identification is the most critical aspect of scribed as T. evanescens was actually T. dendrolimi any biological control program and several biologi- (see below), while Nagarkatti’s Japanese material is cal control failures can be traced to incorrect natu- most likely T. yabui. Based on European material ral enemy identifications (Gordh, 1976). Knowing previously examined (Honda, unpublished data), which species occur in Japan may allow biocontrol we feel that both T. evanescens and T. brassicae are workers to do two things: study any potential risks different species and also distinct from T. yabui. of future adventive Trichogramma species as advo- Discrimination between T. evanescens and T. yabui cated by Hirose (2002), and choose the best possi- can be based primarily on the posterior expansion ble Trichogramma species for a given biological of the dorsal lamina as it is primarily delta shaped control program. It is hoped that this work will pro- and very pointed at its apex in T. evanescens, but vide information for biocontrol workers to identify more rounded in T. yabui. The only noticeable dif- field collected material. ference between T. brassicae and T. yabui is that the volsellae in T. yabui are longer and almost reach the apex of the parameres while they are sig- MATERIALS AND METHODS nificantly shorter in T. brassicae, and occupy ap- Species descriptions and specimens prepared for proximately half the distance of the parameres (see scanning electron microscopy (SEM) and DNA Pinto, 1999). Probably the most reliable way to dis- analysis were based on methods previously de- criminate between these three species is to com- scribed (Taylor et al., 2005). Specimens used for pare their DNA sequences (see DNA Sequence SEM were obtained from type localities for T. section). Trichogramma yabui also resembles T. yabui, and T. okinawae. Species descriptions and okinawae n. sp. and is distinguished from it in the measurements follow anatomical terminology, following Diagnosis section. morphological measurements (SEM), and ratios Description. Based on 4 slide-mounted males, 2 used in Pinto (1999). Illustrations for T. yabui, T. slide-mounted females, reported as a mean. Color okinawae, T. jezoense, and T. aomoriense were de- appearing dark in mounted material. Forewing rived from holotypes. Types are deposited at the 0.13 mm0.13 wide; FWW/FWL0.430.09; 8– Entomological Laboratory, Faculty of Agriculture, 9 setae between 4th and 5th tracks; longest fringe Kyushu University (ELKU) (Fukuoka, Japan), with setae 0.150.08 FWW. Hind wing with 2 and 5 the exception of T. jezoense which is deposited at setae in anterior and posterior track, respectively, the Laboratory of Systematics, National In- the latter attaining 0.2 distance from the hamuli to stitute of Agro-Environmental Sciences (NIAES) wing apex. Scutellum with anterior pair of setae (Tsukuba, Japan). Most of the other material exam- equal in length to posterior pair. ined is located at ELKU. Male: Flagellum of antennae elongate, slightly curved, 2.6 as long as scape, FL/FW6.31.18, FL/HTL1.130.06; moderately elongate, fili- TAXONOMY form setae taper gradually to apex, FSL/FW Trichogramma yabui Honda and Taylor sp. nov. 3.900.7; BPS formula 1-2(1)-1-1(0)-1-1; PLS (Figs. 1–3) only very slightly curved, terminal PLS with apical Trichogramma evanescens: Nagarkatti and Naga- 0.15 extending beyond flagellum. Genital capsule 250 J. Y. HONDA et al.

Fig. 1. Dorsal view of T. yabui n. sp. male genital capsule. Fig. 2. Ventral view of T. yabui n. sp. male genital capsule. Scale bar50 mm. Scale bar50 mm.

Fig. 3. T. yabui n. sp. (Holotype). (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital cap- sule. (d) Hind wing. Scale bars0.05 mm. moderately broad, 0.360.24 as wide as long; DA1.50.21 AD and 0.490.06 GC; spine of slightly constricted at base of IVP, PM slightly sin- VS ovoid, VS slightly bowed, occupying 0.65 uate and acuminate, convergent at apex; AD/GL 0.06 of AD; IVP spinose occupying 0.570.14 0.210.03; AW/GW0.590.06; DAL/GL0.57– AD; VR extremely broad at posterior half, narrow- 0.58; DLA originating from just below center of ing anteriorly, occupying ca. 0.40 of BD. VP not genital capsule, distinctly notched with rounded obviously protuberant, positioned at base of IVP. shoulders that do not approach sides of GC, form- Aedeagus subequal (0.990.06) of GL. AL/HTL ing a moderately broad linguiform posterior exten- 1.070.09; apodemes 0.450.04 AL. sion, acuminate at apex, whose width at IVP level Female: Funicle of antennae 1 and 2 BPS on F1 is 1.50.23 more than that of aedeagus, DLA and F2, respectively. OL/HTL0.93–1.2. 2.130.5 as long as wide, its length from apex of Variation. 1 male exhibited 17 setae between the The Trichogramma of Japan 251 100 100 84 merus okinawae T. ivelae T. 100 76 74 100 74 82 82 100 75 68 80 78 100 79 89 70 82 79 100 76 81 72 64 77 76 species. NCBI database accession codes are found beneath each species in the rows richogramma 100 77 82 81 84 73 82 82 T 100 76 77 74 83 71 63 76 75 richogramma T 100 72 78 73 77 75 79 76 83 91 100 79 77 97 76 83 81 85 73 82 83 100 71 68 74 71 75 72 78 67 62 75 72 ercentage of ITS-2 sequence similarity between selected ercentage of ITS-2 sequence similarity between .P 100 79 82 78 80 82 83 84 87 79 70 85 81 e1 brassicae cacoeciae T. evanescens T. brassicae nr. T. oleae T. papilionis T. cordubensis T. ostriniae T. turkestanica T. yabui T. u T. bl T. Ta okinawae yabui umerus papilionis cordubensis ostriniae turkestanica oleae nr. brassicae nr. evanescens cacoeciae brassicae ivelae Y518696 Y520559 Y244463 Y518694 Y518695 Y163006 Y166700 Y163006 Y244468 A T. U74601 T. A T. U74675 T. A T. AF043615 T. A T. A T. A T. AF043618 T. A T. A T. T. A 252 J. Y. HONDA et al.

4th and 5th vein tracks. nawae and distinctly sinuate and acuminate in T. Types. Holotype (male), allotype (female), and yabui. Finally, the dorsal lamina length from the paratypes (12 males). JAPAN. Ishikawa Prefecture: apex of the dorsal aperture is approximately 1.50 Saita-cho, Kanazawa, vi-30-1997, collected by T. times that of the apical distance in T. yabui and the Ya bu; ex eggs of Ostrinia furnacalis (Guenée) vosellae occupy 0.65 of the apical distance while (: Pyralidae) on sweet corn. the dorsal lamina length from the apex of the dor- Etymology. Named for the collector, Tetsuo sal aperture is approximately 1.18 times that of the Ya b u . apical distance and the vosellae occupy 0.650.06 Host/plant associations in Japan. LEPI- of the apical distance for T. okinawae. DOPTERA. Pyralidae: Ostrinia furnacalis (see Trichogramma umerus has also been recorded types); : ex Samia cynthia pryeri (But- from the Okinawa Prefecture and may be confused ler) host trap card placed in vegetable garden with T. okinawae. Although the size and dimen- (Takamori, Nagano Pref.). sions of T. umerus and T. okinawae are similar in Distribution. Known only in Japan (Honshu). most instances, there are a few key differences be- Material studied. 4 males, 2 females; 1 record. tween the two species. In females the ovipositor Records in Japan. Honshu: Ishikawa Prefecture, length is only 0.82–0.85 that of the HTL for T. Saita-cho, Kanazawa (see types); Nagano Prefec- umerus in contrast to 0.99 for T. okinawae. Differ- ture, Takamori, vi-30-1997, 4 males and 2 females, ences in male antennae also exist as the flagellum M. Fukumoto. length vs. flagellum width measures 6.85 and 5.40 DNA sequence. An ITS-2 DNA sequence has for T. umerus and T. okinawae, respectively. Flagel- been deposited in the NCBI database (accession lum setal length vs. forwing width ratios are longer AY518696). DNA sequences range between 485– (3.55 vs. 3.00) in T. okinawae than T. umerus. One 491 bp and 425–438 bp for T. yabui and T. evanse- of the most striking differences between the two cens (Silva et al., 1999), respectively. When a T. species is the length of the aedeagus in T. okinawae evanescens (accession AF043618) sequence was as it is longer than the hind tibia (1.10) whereas it aligned with T. yabui, they showed 85% similarity is shorter in T. umerus (0.77). The shoulders of the in base pair composition (Table 1). Interestingly, T. dorsal lamina are more pronounced and rounded in evanescens sequences are most similar to T. papil- T. umerus than T. okinawae. ionis (see under T. papilionis). A DNA sequence Description. Based on 3 slide-mounted males obtained from T. brassicae (accession AY163006) (HTL0.120.01 mm) and 5 females (HTL also was different from T. yabui as T. brassicae 0.120.01 mm). Color, olive yellow, mesoscutum usually measures 406–407 bp and are 79% similar suffused with brown, metasomal segments suffused to T. yabui. Out of our sample comparison, T. yabui with brown; vertex dark yellow with gena suffused is most similar to T. ostriniae (89%). Collection with dark brown. Forewing (n5) 0.200.01 mm data: Ishikawa Prefecture: Saita-cho, Kanazawa; wide; FWW/FWL0.460.02; longest fringe setae vi-30-1997, ex Ostrinia furnacalis, T. Yabu. 0.200.01 FWW. Male: Flagellum of antennae moderately long Trichogramma okinawae Honda sp. nov. (Figs. and straight, FL/FW5.400.07, FL/HTL1.19 4–6) 0.09; elongate, filiform setae tapering towards Diagnosis. This species closely resembles T. apex, FSL/FW3.550.07; BPS, formula 1-1-2-0- yabui n. sp. As with most Trichogramma species in 1-1; PLS short, terminal PLS ending well before the Exiguum section, this species is characterized apex of flagellum. Genital capsule narrow, 0.33 by a fairly broad genital capsule, and notched dor- 0.01 as wide as long; slightly constricted at base of sal lamina with rounded shoulders. The most obvi- IVP, PM straight, not convergent towards apex; ous difference is body coloration as T. yabui is very AD/GL0.300.03; AW/GW0.640.001; DAL/ dark in contrast to T. okinawae which is more yel- GL0.570.03; DLA originating from middle of lowish. Moreover, the aedeagus is much longer in genital capsule, slightly notched with slight shoul- T. okinawae as it exceeds the genital capsule in ders not extending beyond sides of genital capsule, contrast to T. yabui where it is subequal in length. narrowing posteriorly to a narrow linguliform pos- The parameres are straight and parallel in T. oki- terior extension whose width at level of IVP is less The Trichogramma of Japan 253

Fig. 4. Ventral view of T. okinawae n. sp. male genital Fig. 5. T. okinawae n. sp. Aedeagus (AD). Scale bar capsule. Scale bar50 mm. 30 mm.

Fig. 6. T. okinawae n. sp. (Holotype). (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital capsule. (d) Hind wing. Scale bars0.05 mm. than that of aedegus. DLA 1.520.06 as long as meres. AL/HTL1.100.02. Apodemes occupy- wide, its length from apex of DA 1.180.01 AD ing 0.230.01 AL. and 0.320.001 GL, occupying 0.520.02 AD ap- Female: OL/HTL0.990.01. proaching PM apex and ending just prior or to VS; Types. Holotype (male), allotype (female), and IVP fairly long, narrow, and spindle shaped, attain- paratypes (2 males). JAPAN. Okinawa Prefecture: ing 0.450.007 AD. VR narrow occupying 0.33 Takachiho, Shimoji; iii-05-2003; Y. Sadoyama col- 0.007 BD; VP small, not noticeably protuberant, lector; ex eggs of Tetramoera schistaceana (Snellen) and placed at base of IVP; spine of VS ovoid, VS (Lepidoptera: ) on sugar cane. straight, occupying 0.630.01 of AD; aedeagus Etymology. Named for the Japanese island on longer than GL, extends dramatically past para- which it was collected. 254 J. Y. HONDA et al.

Fig. 7. T. aomoriense n. sp. (Holotype). (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital capsule. (d) Hind wing. Scale bars0.05 mm.

Distribution. Known only from Okinawa Prefec- shoulders in T. aomoriense are very narrow and ture, Japan. arise anteriorly of the genital capsule. Additionally, Host/plant association in Japan. LEPIDOPTERA. the shoulders extend distinctly beyond the edges Tortricidae: Tetramoera schistaceana (see types). of the genital capsule. The ventral processes are Material studied. 11 males, 5 females; 5 records. very pronounced and heavily scerlotized in T. ao- Records in Japan. Ryukyus: Okinawa Prefec- moriense and are highly protuberant. They are less ture, Takachiho, Shimoji (see types); Yoza, xi-4- distinct in the other species. 1997, 5 males, J. Honda; Kumadake, Hirara, iii-5- Description. Based on 1 slide-mounted male 2003, 1 male, Y. Sadoyama; Nagama, Gusukube, (HTL0.13 mm) and female (HTL0.13 mm). iii-5-2003, 3 males and 2 females, Y. Sadoyama; Color appearing dark brown in slide mounted ma- Fukukita, Gusukube, iii-5-2003, 2 males and 3 fe- terial. Forewing (male only) 0.25 mm wide; FWW/ males, Y. Sadoyama. FWL0.56; longest fringe setae 0.10 FWW. DNA sequence. An ITS-2 DNA sequence has Male: Flagellum of antennae short, slightly been deposited in the NCBI database for reference curved and inflated towards apex, FL/FW4.0, (accession AY518695). The sequence measures FL/HTL0.92; elongate, filiform setae taper 430 bp in length vs. 485–491 bp for T. yabui (82% abruptly at apex, FSL/FW2.67; BPS formula ap- similar) and 530 bp (74% similar) for T. umerus parently 1-1-2-0-1-1; PLS straight, terminal PLS (accession AY518694). Sequence comparison shows with apex extending slightly beyond flagellum. that T. okinawae is most similar (85%) to T. brassi- Genital capsule moderately broad, 0.45 as wide as cae (Table 1). Collection data: Okinawa Prefecture, long; slightly constricted at base of IVP, PM Takachiho, Shimoji; iii-05-2003, ex Tetramoera slightly arcuate, slightly convergent at apex; AD/ schistaceana, Y. Sadoyama. GL0.21; AW/GW0.60; DAL/GL0.61; DLA originating from anterior half of genital capsule, Trichogramma aomoriense Honda sp. nov. (Fig. 7) highly sclerotized, notched with prominent shoul- Diagnosis. Possessing prominent lobed shoul- ders extending beyond sides of genital capsule, ders at the posterior extension of the dorsal lamina, narrowing posteriorly to a narrow linguliform pos- this species possibly can be confused with T. je- terior extension whose width at level of IVP is zoensis, T. dendrolimi, and T. chilonis. However, T. equal or slightly greater than that of aedeagus. aomoriense can be discriminated between all three DLA 1.11 as long as wide, its length from apex of based on two main characters: the shape of the dor- DA 2.08 AD and 0.42 GL, occupying 0.87 AD ap- sal lamina shoulder and the ventral processes. The proaching PM apex and ending prior to VS; IVP The Trichogramma of Japan 255 distinct and triangular, attaining 0.39 AD. VR nar- hamuli to wing apex. Scutellum with anterior pair row, occupying 0.55 BD; VP prominent, highly, of setae subequal to posterior pair. sclerotized, and protuberant. Somewhat extended Male: Flagellum of antennae slightly curved, into AD, positioned at base or slightly interior to 0.170.06, about twice as long as scape, FL/FW IVP. VS straight, occupying 0.88 of AD. Aedeagus 6.130.4, FL/HTL =1.04–1.25 (n=6); moderately slightly longer than GL. AL/HTL0.92. Apodemes elongate, filiform setae taper gradually to apex, occupying 0.52 AL. FSL/FW3.30.4 (3.0–4.0); unsocketed setae ab- Female: OL/HTL1.03. sent; BPS subglobose, PS formula 1-1(2)-1-(0)-1- Types. Holotype (male), and allotype (female). 1; terminal PLS does not extend beyond tip of fla- JAPAN. Aomori Prefecture: Ipponmatsu, Towada gellum. Genital capsule widest at anterior of center City; xii-4-1975; K. Mori collector; ex eggs of of capsule, 0.370.05 as wide as long; sides grad- Neozephyrus taxila japonicus (Murray) (Lepi- ually convergent from widest aspect, slightly con- doptera: Lycaenidae) on alder. stricted at base of IVP, PM relatively straight and Etymology. Named after the Japanese prefecture acuminate, slightly convergent at apex; AD/GL Aomori from which this species was first collected. 0.250.01; AW/GW0.590.03; DAL/GL0.6 Distribution. Known only from type locality in 0.05; DLA originating from anterior third of cap- Aomori Prefecture, Japan. sule, with a slight notch that never attains the sides Host/plant association in Japan. LEPIDOPTERA. of the capsule and with poorly developed shoul- Lycaenidae: Neozephyrus taxila japonicus (see ders, gradually tapering to a sublinguiform poste- types). rior extension whose width at IVP level is 0.86 Material studied. 3 males, 2 females; 1 record. 0.22 that of aedeagus, and subequal to length of Two additional dissected male genital capsules and volsellae. DLA 1.70.10 as long as wide, its an additional female collected with the type speci- length from apex of DA 1.280.16 X AD; VS mens were found mounted on separate slides and slightly bowed, narrowing apically, occupying were also examined. 0.590.07 AD, volsellar spines prominent, sub- Record in Japan. Honshu: Aomori Prefecture, conical, asymmetrical, typically spine on right VS Ipponmatsu, Towada City, 3 males, 2 females (see directed more dorsolaterally, longer and more arcu- types). ate than spine on opposing volsellae. IVP spinose, subequal to VS, occupying 0.460.10 of AD; VR Trichogramma ostriniae Pang and Chen New elongate, parallel, extends from base of IVP, ca. Japan Record (Figs. 8–10) 0.33 of BD. VP prominent, protuberant, positioned Trichogramma ostriniae Pang and Chen (1974): ventrolateral and dorsolateral at base of IVP. 448, 453; Oatman et al. (1982): 7–9; Sorokina Aedeagus subequal0.06 GL. AL/HTL 0.750.25; (1993): 41, 45; Pinto (1999): 174; Chan and Chou apodemes ca. 0.470.09 AL. (2000): 145–146. Female: Funicle of antennae typically 1 BPS on Diagnosis. A thorough diagnosis can be found in F1 and F2. OL/HTL1.060.14. Oatman et al. (1982), Pinto (1999), and Chan and Type. Holotype male. CHINA. Beijing; Ostrinia Chou (2000). The adenate ventral processes and nubilalis; viii-3-63; Chen Tai-lu; Beijing Institute dark coloration in T. ostriniae are unique to this of Zoology; not examined. species in Japan. A description of T. ostriniae is Distribution. China (Pang and Chen, 1974), given below from Japanese collected specimens. Hawaii (Oatman et al., 1982), and introduced into Description. Based on cultured material. Unless USA in 1990 (Pinto, 1999). Japan new record. otherwise indicated, quantitative data taken from Host/plant association in Japan. LEPIDOPTERA. seven males (HTL0.1–0.16) and six females Pyralidae: Ostrinia furnacalis on corn. (HTL0.14–0.16). Forewing 0.180.05 mm wide; Material studied. 7 males, 6 females; 1 record. FWW/FWL0.500.04; 6–8 setae between 4th Record in Japan. Honshu: Shimane Prefecture, and 5th vein tracks; longest fringe setae 0.150.04 Izumo, 1990, 7 males, 6 females, ex Ostrinia fur- FWW, ca. 1.2 times the HTW. Hind wing with 0–3 nacalis, T. Murai. and 0–6 setae in anterior and posterior track, re- DNA sequence. DNA sequences were obtained spectively, the latter attaining 0.2 distance from the from specimens collected in Izumo, Shimane Pre- 256 J. Y. HONDA et al.

Fig. 8. Dorsal view of T. ostriniae male genital capsule. Fig. 9. Ventral view of T. ostriniae male genital capsule. Scale bar50 mm. Scale bar50 mm.

Fig. 10. T. ostriniae male. (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital capsule. (d) Hind wing. Scale bars0.05 mm. fecture on Ostrinia furnacalis eggs. An ITS-2 Trichogramma lingulatum Pang and Chen New DNA sequence has been deposited in the NCBI Japan Record (Figs. 11 and 12) database for reference (accession AY518695). The Trichogramma lingulatum Pang and Chen (1974): sequence measures 445 bp in length and was found Sorokina (1993): 19–20. to be 98% identical to a T. ostriniae sample Diagnosis. This species is closely allied to the previously submitted from China (accession Indian species T. hesperidis Nagaraja, T. flandersi AY244463). The sequence of T. ostriniae appears Nagaraja and Nagarkatti, and T. achaeae Nagaraja to be most similar to T. yabui (89% [Table 1]). Col- and Nagarkatti in addition to T. kurosuae in Japan. lection data: Shimane Prefecture, Izumo; 1990, ex All are characterized by a broad, linguiform poste- Ostrinia furnacalis, T. Murai. rior extension of the dorsal lamina. This extension obscures the parameres and volsellae dorsally in T. The Trichogramma of Japan 257

flandersi and T. hesperidis as well as T. lingulatum, from one male. Forewing 0.17 mm wide; FWW/ however, the two former species possess distinct FWL0.47; longest fringe setae 0.21 FWW, ca. notches at the base of the dorsal lamina which is 1.9 the HTW. not present in T. lingulatum. The dorsal lamina of Male: Flagellum of antennae short, fairly T. achaeae while not notched at its base, does not straight, 0.100.02, about 1.5 times the length of obscure the parameres and volsellae. Trichogramma the scape, FL/FW4.70.5, FL/HTL0.820.04, kurosuae is yellow with a notched base whose dor- moderately elongate, filiform setae taper gradually sal lamina obscures the volsellae, but not the para- to apex, FSL/FW1.850.06; unsocketed setae meres and can be easily distinguished from the absent; BPS subglobose, BPS formula apparently darker T. lingulatum. 1-1-1-1-1-0; terminal PLS does not extend beyond Description. Quantitative data taken from four tip of flagellum. Genital capsule widest at anterior males (HTL0.10–0.14 mm). Forewing data taken of center of capsule, 0.380.01 as wide as long; sides gradually convergent from widest aspect, slightly constricted at base of IVP, PM relatively straight, slightly convergent at apex; AD/GL 0.170.01; AW/GW0.470.06; DAL/GL0.66 0.03; DLA originating near middle of capsule, not notched basally and without shoulders, not narrow- ing towards posterior and forming a broad lin- guiform posterior extension whose width at apex of IVP is ca. 0.9 that of aedeagus, elongate obscuring both PM and VS in dorsal view. DLA 1.80.20 as long as wide, its length from apex of DA 2.67 0.12 X AD and 0.470.02 GL, occupying 1.19 0.12 AD; VS slightly bowed, occupying 0.730.06 AD. IVP short, spinose, subequal to VS, occupying 0.190.2 of AD; VR elongate, parallel, occupying 0.580.06 BD. VP prominent, protuberant and lo- cated considerably anterior to base of IVP. Aedea- gus equal to GL. AL/HTL 0.990.08; apodemes Fig. 11. Dorsal view of T. ostriniae male genital capsule. ca. 0.510.03 AL. Scale bar50 mm. Types. Holotype male. CHINA. Shantung; un-

Fig. 12. T. lingulatum male. (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital capsule. (d) Hind wing. Scale bars0.05 mm. 258 J. Y. HONDA et al.

Fig. 13. T. jezoense (Lectotype). (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital cap- sule. (d) Hind wing. Scale bars0.05 mm. known Lepidoptera host; v-1-1958; Mao Jing-long; 2000) as is the female OL/HTL ratio which aver- Beijing Institute of Zoology; not examined. ages 1.16 and 1.05 for T. jezoense and T. chilonis, Distribution. China (Pang and Chen, 1974). respectively. Japan new record. Description. Unless otherwise indicated, quanti- Host/plant association in Japan. LEPI- tative data taken from two males (HTL0.11– DOPTERA. Saturniidae: ex. Samia cynthia pryeri 0.14 mm). Color unknown but described as dark by (Butler) host trap card on mulberry. Ishii (1941) for both males and females. Forewing Material studied. 4 males; 1 record. slightly fumate behind venation. Forewing 0.24 Record in Japan. Honshu: Nagano Prefecture, 0.03 mm wide; FWW/FWL0.550.01; longest Takamori, ix-4-2002, 4 males, ex. Samia cynthia fringe setae 0.140.02; FWW, ca. 1.5 the HTW. pryeri, M. Fukumoto. Male: Flagellum of antennae slightly curved, 0.140.01 long, about two times as long as scape, Trichogramma jezoense Ishii (Fig. 13) FL/FW4.370.3, FL/HTL1.10–1.21; moder- Trichogramma jezoensis Ishii (1941): 175. ately elongate, filiform setae taper gradually to Diagnosis. Trichogramma jezoense is closest to apex, FSL/FW2.90.1 (2.27–2.29); BPS subglo- T. chilonis in that they both possess prominent lat- bose, BPS formula apparently 2-1-2-1-0-1 (only eral lobes that do not extend to the edge of the gen- holotype examined); terminal PLS does not extend ital capsule as in T. dendrolimi. Trichogramma je- beyond tip of flagellum. Genital capsule markedly zoense differs from T. chilonis having a darker tear-shaped; widest at anterior of center of capsule, color as Ishii (1941) has stated that this is a darker 0.610.01 as wide as long; sides convergent from species and T. chilonis is a yellow species with a widest aspect, slightly constricted at base of IVP, brownish abdomen. The male flagella also have a PM tapering slightly and convergent at apex; higher width to length ratio range (0.21–0.24) than AD/GL0.280.01; AW/GW0.650.06; DAL/ T. chilonis (0.15–0.19) (Chan and Chou, 2000). GL0.640.03; DLA originating at middle of The general shape of the genital capsules is also capsule, with a deep notch that never reaches the different. The capsule of T. jezoense is smaller and sides of the capsule and with well developed, more tear-shaped (0.610.01 as wide as long) rounded shoulders, gradually tapering to apex while T. chilonis is robust and oval in shape forming a subtriangular posterior extension whose (0.47–0.59 as wide as long) according to the data width at IVP level is subequal to that of aedeagus of Chan and Chou (2000) for T. chilonis. The width, apex of extension generally pointed, and AL/HTL ratio is also higher in T. jezoense ranging subequal to length of volsellae. DLA 1.00.05 as from 0.81–1.07 vs. 0.66–0.80 (Chan and Chou, long as wide, its length from apex of DA 0.92 The Trichogramma of Japan 259

Fig. 14. T. yawarae male. (a) Forewing. (b) Antenna. (c) Dorsal (left) and ventral (right) view of the male genital capsule. (d) Hind wing. Scale bars0.05 mm.

0.10 AD and 0.260.05 GL, occupying ca. 0.50 35. AD; VS slightly bowed, occupying 0.710.01 AD; Diagnosis. Trichogramma yawarae displays all IVP subtriangular, subequal to VS, occupying the critical characters which define the Retorridum 0.440.01 of AD; VR broad, parallel, extends Section. This small species group is exemplified by from base of IVP tapering slightly anteriorly, ca. straight volsellae and a comparatively short inter- 0.40 of BD (visible in holotype only); VP promi- volsellar process. As in most of these species, hind nent, protuberant, positioned at base of IVP. wings of T. yawarae have complete anterior and Aedeagus subequal to GL. AL/HTL 0.800.02; posterior setal tracks. Like the North American apodemes ca. 0.490.02 AL. species, T. retorridum (Girault), T. yawarae is dis- Female: OL/HTL1.160.66 (n3). tinguished by an elongate VR, almost 0.75 of BD, Types. Lectotype male, designated herein circled with the ventral processes positioned distinctly an- in ink. Japan. Sapporo: ix-8-1937; collected from terior of the intervolsellar process and laterally to the eggs of Leguminivora (=) glycini- the ventral ridge. The slender, subsinuate dorsal vorella (Matsumura) by H. Kono. lamina most closely resembles that of the nominal Distribution. Known only from Japan (Hokkaido species but the elliptical DA is not as narrow at its and Honshu). apex as in T. retorridum. Host/plant associations in Japan. LEPI- Description. Based on two slide-mounted males DOPTERA. Pyralidae: punctiferalis originating from a culture initiated from a single, (Guenée); Tortricidae: Leguminivora glycinivorella, unmated female. Color appearing light gray in Grapholita molesta (Busck). mounted material; area of forewing behind vena- Material studied. 7 males, 4 females; 3 records. tion noticeably darkened. Forewing 0.18 mm wide; Records in Japan. Hokkaido: Sapporo, 3 males FWW/FWL0.46–0.47; 9–13 setae between 4th (see types). Honshu: Kanagawa Prefecture, Hira- and 5th tracks; longest fringe setae 0.02–0.03 tsuka, viii-20-1963, 2 males, 2 females, ex FWW. Hind wing with 1 and 6 setae in anterior and Grapholita molesta, N. Shinkaji; Ichinomiya, posterior track, respectively, the latter attaining Naka-gun, viii-11-1965, 2 males, 2 females, ex 0.03 distance from the hamuli to wing apex. Conogethes punctiferalis, N. Shinkaji. Scutellum with anterior pair of setae long, equal in length to posterior pair. Trichogramma yawarae Hirai and Fursov (Fig. Male: Flagellum of antennae elongate, very 14) slightly curved, 0.17–0.18 mm, slightly longer than Trichogramma yawarae Hirai and Fursov (1998): scape, FL/FW5.8–6.3, FL/HTL1.02–1.08; 260 J. Y. HONDA et al. moderately elongate, filiform setae taper abruptly viii-27-1997, 5 males, ex Marasmia exigua, J. at apex, FSL/FW2.4–2.5; unsocketed setae pres- Honda. ent on F1; formula 2-1-1-1(0)-1(0)-1; terminal PLS DNA sequence. An ITS-2 DNA sequence has does not extend beyond apex of flagellum. Genital been deposited in the NCBI Database (accession capsule widest in anterior half just below center of AY518697). The sequence measures 496 bp and is capsule, 0.35–0.36 as wide as long; sides gradually only 42% and 47% similar to T. japonicum and T. convergent from widest aspect, moderately con- brevicapillum Pinto and Platner, respectively. We stricted at base of IVP, PM straight and acuminate, chose these comparisons as they all belong to the very slight convergent at apex; AD/GL0.22– Retorridum Section; however, T. yawarae neither 0.24; AW/GW0.47–0.50; DAL/GL0.59–0.61; resembles these two species morphologically nor DLA originating from anterior half, not notched at does it share similarity in ITS-2 sequence. Collec- base but immediately narrowing posteriorly, form- tion data: Fukuoka Prefecture, Nagai, Ikuhashi, ing a slender linguiform posterior extension whose viii-27-1997, ex Marasmia exigua, J. Honda. width at IVP level is ca. a half less than that of aedeagus, elongate and subequal to length of Trichogramma chilonis Ishii (Figs. 15 and 16) volsellae. DLA 1.6–1.9 as long as wide, its length Trichogramma chilonis Ishii (1941): 173; Na- from apex of DA1.0–1.25 AD; VS subrectangu- garkatti and Nagaraja (1979): 115; Oatman et al. lar in shape and truncate, occupying 0.75–0.86 (1982): 22; Sorokina (1993): 68; Chan and Chou AD; VS spines oval, some sclerotization on median (2000): 136. surface of volsellae, parallel to apex of IVP. IVP Trichogramma australicum Nagarkatti and Na- short, subtriangular, less than half the length of VS, garaja (1971): 15–17. occupying only 0.35–0.47 of AD; VR elongate, ex- Trichogramma confusum Hayat and Viggiani tends from base of IVP to 0.75 BD. VP papilliform, (1984): 34. positioned distinctly anterior to base of IVP, lateral Diagnosis. A thorough diagnosis and description to VR. Aedeagus 1.05–1.07 times greater than is given by Oatman et al. (1982), and Chan and GL. AL/HTL 0.72; apodemes ca. 0.50–0.57 AL. Chou (2000). The SEM images depict several char- Female: OL/HTL1.000.01. acters defining T. chilonis: prominent lateral lobes Types. Holotype male labeled: “Collection of K. (not extending to the edge of the genital capsule), Hirai, culture from eggs of Mamestra brassicae L. the dorsal lamina the sublinguiform posterior ex- emerged 27.03.1997, originally reared from eggs tension abruptly narrowing above the shoulders of Chilo suppressalis Walk., Ibaraki, near Tsukuba, which reach the level of the volsellae, an elongate Yawara”. No. 1075. National Agriculture Research and narrowly subtriangular intervolsellar process Center, Tsukuba, Japan. Not examined. Apparently and papilliform ventral processes just basal to the lost along with paratypes (Hirai, pers. communica- intervolsellar process. See remarks above to distin- tion). guish from T. jezoense. Distribution. Known only from Japan (Honshu, Types. Lectotype male designation; National In- Shikoku, and Kyushu). stitute of Agro-Environmental Sciences, Tsukuba, Host/plant associations in Japan. LEPI- Japan; examined. DOPTERA. Hesperiidae: Paranara guttata guttata Distribution. Japan (Hokkaido, Honshu, Shikoku, (Bremer et Grey) on rice; Hypsidae: Asota ficus Kyushu and Ryukyus) (Ishii, 1941), , China, (Fabricius) on fig; Pyralidae: Chilo suppressalis on Hawaii, Guam (Oatman et al., 1982), Pakistan, rice (Hirai and Fursov, 1998), Marasmia exigua , New Guinea, Philippines, Madagascar, (Butler) on rice. Mauritius (Sorokina, 1993), China (Pang and Material studied. 7 males, 4 females; 3 records. Chen, 1974) and Taiwan (Chan and Chou, 2000). Records in Japan. Honshu: Aichi Prefecture, Host/plant associations in Japan. LEPI- Furo-cho, Chikusa-ku, Nagoya, vi-16-1977, 1 DOPTERA. Danaidae: Anosia chrysippus chrysip- male, ex. Parnara guttata guttata, F. Nakasuji. pus (Linnaeus); Hypsidae: Asota ficus on fig; Ly- Shikoku: Ehime Prefecture, Shimoidaicho, Ma- caenidae: Zizeeria maha argia (Menetries) (Hirose, tsuyama, ix-7-2003, 1 male, ex Asota ficus, M. 1976); Lymantriidae: Euproctis similis (Fuessly) on Aono. Kyushu: Fukuoka Prefecture, Nagai, Ikuhashi, mulberry; : Autographa nigrisigna The Trichogramma of Japan 261

Theretra silhetensis (Walker) on ; Tortricidae: Leguminivora glycinivorella on soybean (Hirai, 1987); Yponomeutidae: Plutella xylostella on cab- bage (Iga, 1985; Hirashima et al., 1989). Material studied. 34 males, 1 female; 19 records. Records in Japan. Hokkaido: Nat. Agr. Res. Center Hokkaido Reg., Sapporo, vii-23-2004, 4 males, ex Mamestra brassicae, J. Honda. Honshu: Ibaraki Prefecture, Kannondai, Tsukuba, viii-1–10- 1984, ex Spodoptera litura, R. Hamada; Tokyo Pre- fecture, Edogawa Br. Tokyo Agr. Exp. Sta., Edo- gawa-ku, vii-19-1982, 3 males, ex Autographa ni- grisigna, M. Iga; Do., vii-12, 22-1982, 3 males, ex Mamestra brassicae, M. Iga; Do., vii-22-1982, 4 males, ex Plutella xylostella, M. Iga; Gifu Prefec- ture, Gifu, 1981, 3 males, ex Cephonodes hylas, M. Tanaka; Do., 1981, 5 males; ex Papilio machaon Fig. 15. Dorsal view of T. chilonis male genital capsule. Scale bar50 mm. hippocrates, M. Tanaka; Mie Prefecture, Isshinden, Tsu, ix-16-1975, 1 male, ex Plutella xylostella, H. Yamada; Kyoto Prefecture, Matsugasaki, Kyoto, vii-8-1979, 3 males, ex. Euproctis similis, Y. Nagao; Hiroshima Prefecture, Kanu, viii-6, 25- 1969, 6 males, ex Helicoverpa assulta, K. Nakazawa; Shimane Prefecture, Izumo, vii-9-1986, 1 male, ex Plutella xylostella, unknown collector; Izumo, x-1-1986, 7 males, ex Mamestra brassicae, unknown collector. Shikoku: Ehime Prefecture, Ichiba, Iyo, vii-29-2003, 1 male, 1 female, ex Asota ficus, M. Aono; Shimomitani, Iyo, x-2-2003, 10 males, ex A. ficus, M. Aono; Kochi Prefecture, Kotohira, Nangoku, viii-28-1980, 1 male, ex Pa- pilio protenor demetrius, K. Nozato. Kyushu: Fukuoka Prefecture, Nagai, Ikuhashi, viii-27-1997, 3 males, ex Malasmia exigua, J. Honda; Kagoshima Prefecture, Hosoyamada, Kushira, ix- 19-1975, 2 males, ex silhetensis, A. Fig. 16. Ventral view of T. chilonis male genital capsule. Tanaka; vii-30, viii-2, 1984, 2 males, ex Agrius Scale bar50 mm. convolvuli, K. Nakagawa; Onoma, Yakushima Is.; xi-1966, 1 male, ex Anosia chrysippus, H. Tanaka. (Walker) on cabbage, Mamestra brassicae on sugar Ryukyus: Okinawa Is., xii-1953, 2 males, ex Leu- beet and cabbage, Helicoverpa assulta on green cinodes orbonalis, N. Tamashiro. pepper, Spodoptera litura (Fabricius) on taro DNA sequences. DNA sequences were obtained (Hamada, 1992); Papilionidae: Papilio machaon from many T. chilonis populations throughout hippocrates C. et R. Felder, Papilio protenor Japan (Kagoshima, Fukuoka, and Okinawa) and demetrius Stoll on Zanthoxylum ailanthoides Korea (Cheju Do) and ranged from 410–414 bp. (Watanabe et al., 1984); Papilio xuthus (Linnaeus) One 413 bp long sequence was deposited in the on citrus (Hirose et al., 1980); Pyralidae: Leucin- NCBI Database for reference (accession AY89017). odes orbonalis Guenée on eggplant, Marasmia ex- Comparisons were made with a T. chilonis se- igua on rice; : Agrius convolvuli (Lin- quence obtained from the NCBI database (acces- naeus) on taro, Cephonodes hylas (Linnaeus), sion U74674) and were found to be 98% identi- 262 J. Y. HONDA et al. cal. Collection data: Fukuoka Prefecture, Nagai, Ikuhashi; viii-27-1997, ex Malasmia exigua, J. Honda.

Trichogramma dendrolimi Matsumura (Figs. 17 and 18) Trichogramma dendrolimi Matsumura (1926): 45; Ishii (1941): 172; Nagarkatti and Nagaraja (1971): 17; Pang and Chen (1974): 444; Hayat and Vig- giani (1984): 35; Sorokina (1993): 69; Chan and Chou (2000): 140. Trichogramma evanescens Ishii (1941): 173. Diagnosis. A thorough diagnosis and description is given by both Nagarkatti and Nagaraja (1971) and Chan and Chou (2000). The SEM photographs clearly represent the distinguishing characters of T. dendrolimi: a dorsal lamina with prominent shoul- Fig. 17. Dorsal view of T. dendrolimi male genital cap- ders extending to the edge of the genital capsule sule. Scale bar50 mm. with deep notching, and a prominent subtriangular intervolsellar process (equal in length to the volsel- lae) occupying about 75% of the apical distance. Types. No type specimen exists for T. dendrolimi. Distribution. Japan (Hokkaido, Honshu, Shikoku, and Kyushu) (Ishii, 1941), Russia, Belarus, Ukraine, Moldavia, Kazakhstan, Western Europe (Sorokina, 1993), China (Pang and Chen, 1974), and Taiwan (Chan and Chou, 2000). Host/plant associations in Japan. LEPI- DOPTERA. Hypsidae: Asota ficus on fig; Lasio- campidae: Dendrolimus spectabilis (Butler) on pines (Nagarkatti and Nagaraja, 1971), D. superans (Butler) on Himalayan cedar; Limacodidae: Mon- ema flavescens Walker on , Scopelodes con- tracus Walker on willow; Lymantriidae: Euproctis pseudoconspersa (Strand) on camellia (Mizuta, 1981); Noctuidae: Autographa gamma (Linnaeus) on sugar beet, Spodoptera litura on taro (Hamada, Fig. 18. Ventral view of T. dendrolimi male genital cap- 1992); Notodontidae: Clostera anatomosis (Lin- sule. Scale bar50 mm. naeus) on poplar; : Inachis io geisha Stichel on Humulus lupulus (Hondo et al., 1995); Center Hokkaido Reg., Sapporo, vii-23-2004, 2 Papilionidae: Papilio xuthus on citrus (Hirose et males, ex Autographa gamma, J. Honda. Honshu: al., 1980), P. protenor demetrius on Zanthoxylum Ibaraki Prefecture, Kannondai, Tsukuba, 1 male, ailanthoides (Watanabe et al., 1984); Pyralidae: viii-1–10-1984, R. Hamada, ex Spodoptera litura; Notarcha (=Sylepta) derogata Fabricius (Ishii, Chiyoda-cho, v-1980, 1 male, ex japonica 1941), Ostrinia furnacalis; Saturniidae: Caligula japonica, K. Sekiguchi; Nagano Prefecture, japonica japonica (Moore); Tortricidae: Grapholitha Nishiminowa, Ina, vii-11-1992, 3 males, ex Inachis molesta (Ishii, 1941), Homona magnanima Di- io geisha, M. Hondo; Kisofukushima, vii-12-1992, akonoff. 2 males, ex I. io geisha, M. Hondo; Aichi Prefec- Material studied. 25 males, 1 female; 16 records. ture, Nagoya, vi-1974, 2 males, ex Ostrinia fur- Records in Japan. Hokkaido: Nat. Agr. Res. nacalis, E. Yano; Kyoto Prefecture, Ujigawa, Uji, The Trichogramma of Japan 263 ix-6-1984, 2 males, ex Monema flavescens, Y. Ya- mada; Ujigawa, Uji, ix-6-1984, 2 males, ex Scopelodes contracus, Y. Yamada. Shikoku: Ehime Prefecture, Shimomitani, Iyo, viii-12-2003, 5 males, ex Asota ficus, M. Aono; Kochi Prefecture, Monobe, Nangoku, x-3-1980, 2 males, ex Den- drolimus superans, K. Nozato; Kotakasayama, Kochi, vi-3, 15-1979, 3 males, ex Papilio protenor demetrius, K. Nozato; Monobe, Nangoku, viii-23- 1980, 4 males, ex P. xuthus, K. Nozato; Kagawa Prefecture, Shikoku Agr. Exp. Sta., Zentsuji, vii- 1976, 2 males, ex. O. furnacalis, E. Yano; Tokushima Prefecture, Itanishi, Itano, xi-4, 7, 10- 1976, 9 males, ex Homona magnanima, M. Yuki- nari. Kyushu: Fukuoka Prefecture, Hakozaki, Fukuoka; ix-30-1960, 2 males, 1 female, ex Clostera anatomosis, T. Kawarabata. DNA sequence. DNA sequences were obtained Fig. 19. Dorsal view of T. papilionis male genital capsule. Scale bar50 mm. from cultured material and measured around be- tween 399–403 bp. One 399 bp long sequence was deposited in the NCBI Database for reference (ac- cession AY895013). Comparisons were made with T. dendrolimi sequences obtained from the NCBI data base (accession AF422845 and AY244464) and were found to be 98% identical. Collection data: Shikoku: Ehime Prefecture, Shimomitani, Iyo, viii-12-2003, ex Asota ficus, M. Aono.

Trichogramma papilionis Nagarkatti (Figs. 19 and 20) Trichogramma papilionis Nagarkatti (1974): 391; Oatman et al. (1982): 9; Sorokina (1993): 44. Diagnosis. A thorough diagnosis and description can be found in both Nagarkatti (1974) and Oat- man et al. (1982). The SEM photos represent a few distinctive features of T. papilionis: rectangular and truncate volsellae clearly separate from the para- Fig. 20. Ventral view of T. papilionis male genital cap- meres, an obviously robust intervolsellar process sule. Scale bar50 mm. with adnate and prominent ventral processes and a dorsal lamina with slightly developed shoulders DOPTERA. Lycaenidae: Neozephyrus taxila and a sublinguiform posterior extension. These fea- japonicus on alder; Zizeeria maha argia; Noctu- tures coupled with a distinctly orange yellowish idae: albostriata (Bremer et Grey) on color distinguish it from T. ostriniae (below). altissima; Nymphalidae: Types. Holotype male, Japan; Hakozaki, nesimachus nesiotes Fruhstorfer; Papilionidae: Pa- Fukuoka Prefecture; Papilio xuthus; x-1970; Y. Hi- pilio memnon thunbergii von Siebold (Nagarkatti, ; U.S. National Museum, Washington, D.C. 1974), P. xuthus on citrus (Hirose et al., 1980); Registered USNM No. 37107; not examined. Pieridae: Pieris rapae crucivora Boisduval on cab- Distribution. Japan (Honshu and Kyushu) (Na- bage; Sphingidae: Theretra silhetensis on taro. garkatti, 1974) and Hawaii (Oatman et al., 1982). Material studied. 27 males, 5 females; 9 records. Host/plant associations in Japan. LEPI- Records in Japan. Honshu: Aomori Prefecture, 264 J. Y. HONDA et al.

Gonohe, iv-22-1975, 4 males, ex Neozephyrus tax- (Pang and Chen, 1974), and Taiwan (Chan and ila japonicus, K. Mori; Towadako-cho, iii-28-1975, Chou, 2000). 2 males, ex N. taxila japonicus, K. Mori; Ippon- Host/plant associations in Japan. LEPI- matsu, Towada, xii-4-1975, 1 male, ex N. taxila DOPTERA. Hesperiidae: Parnara guttata guttata japonicus, K. Mori. Kyushu: Fukuoka Prefecture, on rice (Nakasuji, 1982); Pyralidae: Chilo suppres- Hakozaki, Fukuoka, vii-6-1997, 3 males, 4 fe- salis on rice (Ishii, 1941), Marasmia exigua on males, ex Papilio xuthus, J. Honda; v-30-1976, vi- rice. 3-1976, 3 males, ex Ctenoplusia albostriata, H. Material studied. 5 males, 4 females; 2 records. Uematsu; x-1973, 1 male, ex Zizeeria maha argia, Records in Japan. Honshu: Aichi Prefecture, Y. Suzuki; vi-9-1975, x-8, 13-1975, 6 males, ex Furo-cho, Chikusa-ku, Nagoya, vi-13-1978, 2 Pieris rapae, Y. Suzuki. Kagoshima Prefecture, males, ex Parnara guttata guttata, F. Nakasuji. Hosoyamada, Kushira, x-2-1975, 8 males, ex Kyushu: Fukuoka Prefecture, Nagai, Ikuhashi, viii- Theretra silhetensis, A. Tanaka; Miyazaki Prefec- 27-1997, 3 males, 4 females, ex Marasmia exigua, ture, Hyuga Line, v-15-1966, 1 male, 1 female, ex J. Honda. nesiotes, H. Tanaka. DNA sequence. An ITS-2 DNA sequence has KEY TO THE TRICHOGRAMMA SPECIES been deposited for reference in the NCBI database OF JAPAN (accession AY520559). The sequence measures 427 bp and is remarkably close (97% similarity) to (Proper identification requires slide-mounted that of T. evanescens. However, T. papilionis is eas- specimens and refers to male specimens only; SEM ily differentiated from the latter due to its lighter photographs may also aid in identification.) orange-yellow color. Compared to T. ostriniae it is 1. Dorsal lamina broad and rounded with a 82% similar (Table 1). Collection data: Fukuoka linguiform posterior extension obscuring Prefecture, Hakozaki, Fukuoka; vii-6-1997, ex Pa- at least the volsellae in dorsal view 2 pilio xuthus, J. Honda. 1. Dorsal lamina not as above3 2(1). Body light yellow, dorsal lamina notched Trichogramma japonicum Ashmead at base with posterior extension obscur- Trichogramma japonicum Ashmead (1904): 165; ing the volsellae in dorsal view Ishii (1941): 171; Nagarkatti and Nagaraja (1971): T. kuosuae 22; Pang and Chen (1974): 450; Oatman et al. 2. Body dark brown, dorsal lamina not (1982): 16; Hayat and Viggiani (1984): 36; Sorokina notched at base with posterior extension (1993): 38; Hirai and Fursov (1998): 37; Pinto obscuring both volsellae and parameres (1999): 217; Chan and Chou (2000): 140. T. lingulatum Diagnosis. A thorough diagnosis and description 3(1). Intervolsellar process short, poorly de- can be found in Nagarkatti and Nagaraja (1971), veloped, and occupying 0.20 (or less) the Oatman et al. (1982), Hirai and Fursov (1998), apical distance 4 Pinto (1999), and Chan and Chou (2000). See 3. Intervolsellar process prominent, well Pinto (1999) for SEM photographs. The anatomi- developed, and occupying greater than cal features distinguishing T. japonicum include: a 0.33 the apical distance 5 uniformly wide dorsal lamina base, elongate nearly 4(2). Dorsal lamina broad at base, parameres parallel parameres and an exceptionally long apical elongate and straight; apical distance distance (0.340.01 the genital length) (Pinto, 0.34 the genital capsule length 1999). T. japonicum Types. Lectotype male (designated by Oatman et 4. Dorsal lamina narrow with a sharply ta- al., 1982). Japan Gifu; “bred... from unknown lepi- pering posterior extension; parameres dopterous eggs’’; Y. Nawa; USNM (no. 7218); not slightly convergent at apex; apical dis- examined. tance 0.19 the genital capsule length Distribution. Japan (Ishii, 1941), India, Vietnam, T. cultellus Thailand, Hawaii, Malaysia, Philippines (Sorokina, 5(3). Intervolsellar process with adnate ven- 1993), Canada, and Australia (Pinto, 1999), China tral processes 6 The Trichogramma of Japan 265

5. Intervolsellar process without adnate proximately 1.50 times that of the apical ventral processes7 distance and the vosellae occupy 0.65 of 6(5). Volsellae truncate, rectangular, and the apical distance T. yabui sp. nov. clearly separate from parameres; inter- ACKNOWLEDGEMENTS volsellar process with slightly curved sides, light colored T. papillionis We thank John Pinto and Gary Platner for their suggestions 6.Volsellae not as above and appear at- and comments. We also thank the following people for provid- ing the specimens: Mitsuo Aono, Fujio Aoyama, Masashi tached to parameres; intervolsellar Fukumoto, Ryoichi Hamada, Masaru Hondo, Mikio Iga, process with straight sides. Darkly col- Takeshi Kawarabata, Kazuhiko Mori, Kojin Nakagawa, Fusao oredT. ostriniae Nakasuji, Keiichi Nakazawa, Kazuo Nozato, Yasutsune 7(5). Genital capsule relatively broad, 0.4–0.6 Sadoyama, Katsui Sekiguchi, Norizumi Shinkaji, Yoshito as wide as long; lobes of dorsal lamina Suzuki, Nobuhiro Tamashiro, Akira Tanaka, Hiroshi Tanaka, Masahiro Tanaka, Hideo Uematsu, Tetsuo Yabu, Hideo Ya- pronounced 8 mada, Yoshihiro Yamada, Eiji Yano, and Masaaki Yukinari. 7 . Genital capsule not as broad, only 0.35 We are grateful to Kazuki Miura and Tamotsu Murai for pro- (or less) as wide as long11 viding information on T. ostriniae. This work was partially 8(7). Lobes of dorsal lamina reach or surpass funded through a JSPS fellowship award to JYH. the edge of the genital capsule9 REFERENCES 8. Lobes of dorsal lamina do not reach the edge of the genital capsule10 Ashmead, W. H. (1904) Descriptions of new Hymenoptera 9(8). Lobes of dorsal lamina narrow and ex- from Japan II. J. New York Entomol. Soc. 12: 146–165. Chan, M. L. and L. Y. Chou (2000) The Trichogramma (Hy- tending beyond genital capsule; ventral menoptera: Trichogrammatidae) of Taiwan. Chinese J. processes prominent, bulbous, and highly Entomol. 20: 135–151. sclerotized T. aomoriense sp. nov. Gordh, G. (1976) Biosystematics of natural enemies. In Bio- 9. Lobes of dorsal lamina and ventral logical Control by Augmentation of Natural Enemies (R. processes not as aboveT. dendrolimi L. Ridgway and S. B.Vinson eds.). Plenum Press, New York, pp. 125–148. 10(8 ). Body yellow with brownish abdomen; Hamada, R. (1992) Egg parasitoids of common cutworm, genital capsule ovalT. chilonis Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). 10. Body dark; genital capsule distinctly Jpn. J. Appl. Entomol. Zool. 36: 258–259 (in Japanese tear-shapedT. jezoense with English summary). 11(7). Apical width (AW) approximately 0.50 Hayat, M. and G. Viggiani (1984) A preliminary catalogue the maximum genital capsule (GC) of the Oriental Trichogrammatidae (Hym: Chalcidoidea). Boll. Lab. Entomol. Agric. ‘Filippo Silvestri’ Portici 41: widthT. yawarae 32–51. 11. Apical width (AW) 0.55 (or more) the Hirai, K. (1987) Biology and parasitism of Trichogramma maximum genital capsule (GC) width chilonis Ishii (Hymenoptera, Trichogrammatidae), as an 11 egg parasite of the soybean podborer, Leguminivora 12(11). Aedeagus length exceeding 1.00 times glycinivorella Matsumura (Lepidoptera, Tortricidae). Bull. Tohoku Natl. Agric. Exp. Sta. 75: 41–64 (in Japa- the hind tibial length13 nese with English summary). 12 . Aedeagus length only 0.77 times the Hirai, K. (2004) Trichogamma ostriniae. In An Encyclopedia hind tibial length T. umerus of Natural Enemies. Vol. 1 (Rural Culture Association 13(12). Body light in color; aedeagus exceeds ed.). Rural Culture Association, Tokyo, pp. 245–248 (in genital capsule length; parameres straight Japanese). and parallel; dorsal lamina length from Hirai, K. and V. N. Fursov (1998) Trichogramma yawarae sp. n. from Japan and a redescription of T. japonicum apex of the dorsal aperture is approxi- Ashmead (Hymenoptera: Trichogrammatidae). J. Ukr. mately 1.18 times that of the apical dis- Entomol. Soc. 4: 35–40. tance and the vosellae occupy 0.52 of the Hirashima, Y., M. Abe, O. Tadauchi, K. Konishi and K. Maeto apical distance T. okinawae sp. nov. (1989) The hymenopterous parasitoids of the diamond- 13. Body dark in color; aedeagus subequal back moth, Plutella xylostella (Lepidoptera, Yponomeuti- dae) in Japan. Esakia 28: 63–73. to genital capsule length; parameres sin- Hirashima, Y., K. Miura, T. Miura and K. Shiro (1990) Stud- uate and acuminate; dorsal lamina length ies on the biological control of the diamondback moth, from apex of the dorsal aperture is ap- Plutella xylostella (Linnaeus) 2. Effect of temperature on 266 J. Y. HONDA et al.

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