Research Article |
Corresponding author: Takuma Yoshida ( togarihimebati@outlook.jp ) Academic editor: Ralph Peters
© 2015 Takuma Yoshida, Rikio Matsumoto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Yoshida T, Matsumoto R (2015) A revision of the genus Chlorocryptus Cameron (Hymenoptera, Ichneumonidae), with the first record of the genus from Japan. Deutsche Entomologische Zeitschrift 62(1): 81-99. https://doi.org/10.3897/dez.62.8975
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The genus Chlorocryptus is revised and two species are recognized: Chlorocryptus purpuratus (Smith, 1852) and C. coreanus (Szépligeti, 1916). Cryptaulax metallicus Szépligeti, 1916, which has been hitherto listed in catalogs as Chlorocryptus fuscipennis Townes et al., 1961, is shown as a new synonym of Chlorocryptus purpuratus. Chlorocryptus purpuratus and C. coreanus are redescribed and illustrated in detail and a key is provided. Chlorocryptus purpuratus is recorded from Japan and Vietnam for the first time and is considered to have recently been introduced into Japan.
Alien species, intraspecific variation, Limacodidae , natural enemy, new synonymy, taxonomy
Chlorocryptus Cameron, 1903 is a small genus presently comprising three species: C. purpuratus (Smith, 1852), C. coreanus (Szépligeti, 1916), and C. fuscipennis Townes et al., 1961. They are easily sighted because of their large body size (10–15 mm) and metallic blue, purple, or green luster throughout the body. Chlorocryptus purpuratus is widely distributed in the Oriental Region to northern China and is well known as a common parasitoid of limacodid moths, which are injurious to leaves of various trees, especially oil palms (
In 2010, one of us (RM) collected several specimens of Chlorocryptus purpuratus (Smith) at Isoshima in Osaka Prefecture. This finding was a surprise because Chlorocryptus species have never before been recorded from Japan, nor are any specimens collected in Japan known from older collections. However, specimens from other Southeast Asian countries are not rare in museum collections. Given the present known distribution of this species, it is presumed that it has recently been introduced into Japan.
Since this first discovery, we have collected additional specimens in Japan. Because its potential hosts, limacodid moths, are abundant in Japan (27 species from 19 genera are presently found;
Here, we study all three currently recognized species of the genus and revise their taxonomic status. We record Chlorocryptus purpuratus from Japan as an alien species to provide the basis for monitoring the future expansion of the distribution range of this species.
Collection and field survey of Chlorocryptus purpuratus in Osaka and adjacent area were conducted by the second author (RM). Two immature specimens were collected from a cocoon of Parasa consocia Walker (Lepidoptera, Limacodidae). Cocoons of the moth are easily found clustered on the ground at the base of certain trees such as Cerasus × yedoensis (Matsum.) A.N.Vassiljeva, Celtis sinensis Pers., and Salix spp. in the study area. RM also conducted successful rearing experiments by supplying C. purpuratus females with Parasa consocia cocoon.
Morphological observations of Chlorocryptus specimens collected by RM and other colleagues and those from museum collections were conducted by the first author (TY). Specimen depositories are abbreviated as follows: Natural History Museum, London (BMNH), Hungarian Natural History Museum, Budapest (HNHM); Muséum national d’Histoire naturelle, Paris (MNHN); Osaka Museum of Natural History, Osaka (OMNH); Systematic Entomology, Graduate School of Agriculture, Hokkaido University, Sapporo (SEHU), Taiwan Agricultural Research Institute in Taichung (TARI).
A part of the specimens were dissected for detailed observations. Genitalia and other body parts were detached from the specimens that were previously macerated in hot water, and the detached body parts were further dissected in 80% ethanol. The dissected body parts were heated in 10% KOH solution at 60 °C for a sufficient period of time depending on the condition of the material to remove muscles from the exoskeleton. Cleaned parts were then washed in diluted acetic acid and distilled water and observed in 80% ethanol or pure glycerol.
Larval exuviae of the parasitoid were extracted from the host cocoon and their cephalic structures and spiracles were observed. They were macerated and stretched in 10% KOH solution and processed as body parts of adult specimens. One 5th instar larva collected in the field was killed to obtain DNA barcode sequences and subsequently treated as the exuviae in morphological observations.
Stereomicroscopes (Nikon SMZ-10 and Olympus SZ40), a light-microscope (Olympus BX40), and a field emission scanning electron microscope (SEM) (JEOL JSM-6301F, Tokyo, Japan) were used for morphological observations. Dissections and observations were carried out under the Olympus stereomicroscope, line drawings were made with a drawing tube attached to the Nikon stereomicroscope, and images of the wings and genitalia were taken using a Nikon Coolpix 4500 digital camera attached to the Olympus stereomicroscope. Images of larval exuviae were taken using the same digital camera attached to the light-microscope. Specimens for SEM analysis were not coated and were observed with an accelerating voltage of 1.0 kV. Digital images were edited using Adobe Photoshop Elements® 6.0.
Terminology used for adult morphology follows
DNA barcoding was carried out by RM. The DNA barcode sequences of cytochrome c oxidase I (COI) were obtained from an adult and a larva collected in Japan. Amplification of COI was carried out using the primer set LCO1490 and HC02198 designed by
Chlorocryptus Cameron, 1903: 34. Type species: Chlorocryptus metallicus Cameron. Designated by Viereck (1914: 32).
Cochlidionostenus Uchida, 1936: 115. Type species: Cryptaulax coreanus Szépligeti. Original designation. Synonymized by
Cryptaulaxoides Uchida, 1940: 121. Type species: Cryptus purpuratus Smith. Original designation. Synonymized under Cochlidionostenus by Townes (1957: 104).
Large and stout species, fore wing length about 10–15 mm, with metallic blue, purple or greenish luster (Fig.
2–12. Chlorocryptus purpuratus; 13–21. C. coreanus. 2 & 13. Head, frontal view (surfacial sculpture partly shown on right half); 3 & 14. Apical margin of clypeus; 4 & 15. Head, dorsal view; 5 & 16. Head, lateral view; 6 & 17. Mandible; 7. Flagellum; 8 & 18. Mesoscutum; 9 & 19. Pronotum, anterior view, showing epomia; 10. Metasternum, posterior view; 11 & 20. First metasomal segment, lateral view; 12 & 21. First lateral segment, dorsal view. CxC – coxal cavity; PtC – petiolar cavity; Tg – tegula. Scale lines: 1 mm.
Epomia strong (Figs
Legs slender, hind femur about 6–8 times as long as median width, and hind tibia about 9–11 times as long as apical width. Male hind tarsal claws sharply bent, apical part covered with scale-like sculpture (Fig.
Wings infumate in various degrees (Figs
First metasomal tergite with baso-lateral tooth (Figs
Both Chlorocryptus purpuratus and C. coreanus are parasitoids of limacodid moths and are often reported in the context of biological control (Table
Host records of Chlorocryptus spp. (modified from
Chlorocryptus | Host | Locality | References |
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C. coreanus | Miresa inornata | not mentioned |
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Monema flavescens | Taiwan |
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C. purpuratus | Birthamula chara | Sumatra |
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Birthosea bisura | Sumatra |
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Darna sp. | Java |
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Monema flavescens | Tsushima | Present study | |
Parasa consocia | China, Osaka |
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Parasa lepida | China |
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Setora nitens | Sumatra, Java |
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Setothosea asigna | Indonesia, Sabah | Gonggrijp 1931; |
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Susica malayana | Indonesia |
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Thosea lutea | Sumatra |
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Thosea postornata | China |
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Thosea sinensis | China |
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Thosea vetusta | Indonesia |
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Trichogyia semifascia | Sumatra |
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Cryptus purpuratus Smith, 1852: 33. Holotype: ♀, China, Hong-Kong (BMNH), mentioned “Ning-po-foo” in original description [examined].
Chlorocryptus metallicus Cameron, 1903: 35. Holotype: ♀, India, Khasia Hill (BMNH) [examined]. Synonymized by
Chlorocryptus coeruleus Cameron, 1903: 36. Holotype: ♀, India, Khasia Hill (Oxford University Museum, UK). Synonymized by
Chlorocryptus reticulatus Cameron, 1907: 84. Holotype: ♂, India, Sikkim (BMNH) [examined]. Synonymized with coeruleus by
Cryptaulax cyaneus Szépligeti, 1916: 286. Lectotype: ♀, India, Sikkim (HNHM) designated by
Cryptaulax metallicus Szépligeti, 1916: 287. Lectotype: ♀, designated by
Cryptaulaxoides purpuratus (Smith):
Cryptaulaxoides metallicus (Cameron):
Cochlidionostenus purpuratus (Smith): Townes 1957: 104.
Chlorocryptus fuscipennis Townes et al., 1961: 142. Replacement name for Cryptaulax metallicus Szépligeti, 1916.
Chlorocryptus purpuratus (Smith):
Neodontocryptus hyalina Saxena, 1978: 216. Holotype: ♀, India, Manipur, Kanchipur (depository unknown; see “Remarks”). Synonymized with coeruleus by
Gonggrijp 1931: 8 (noted as parasitoid of Thosea asigna, photo);
Holotype of Cryptus purpuratus Smith: ♀, “56 113, Hong Kong”, BMNH (ID 3b-572). Holotype of Chlorocryptus reticulatus Cameron: ♂, “Sikkim”, BMNH (ID 3b-2013). Lectotype of Cryptaulax cyaneus Szépligeti: ♂, “India, Sikkim, ex coll. Fruhstorfer”, HNHM (ID 115215). Lectotype of Cryptaulax metallicus Szépligeti: ♀, “S.-Celebes, Patunuang, Jan. 1896, H. Fruhstorfer”, HNHM (ID 115222). One of the paralectotypes of Cryptaulax metallicus Szépligeti: ♀ same data as the lectotype, SEHU (Uchida collection).
Japan. Yamadaike Park, Hirakata, Osaka Pref., 1 ♀, 6.viii.2011, Y. Mori, OMNH. Isoshima, Hirakata, Osaka Pref., 34.82683°N/ 135.6450°E, R. Matsumoto, OMNH: 1 ♂, 18.x.2010; 1 ♀, 29.x.2010; 1 ♀, 8.xi.2010; 1 ♀, 3.x.2010; 3 ♀, 2 ♂, 24.ix.2011; 1 ♀, emerged from a cocoon of Parasa consocia Walker collected on 15.i.2013, emerged in iii.2013. Offspring of females collected at Isoshima, bred on Parasa consocia Walker, OMNH: 1 ♂, laid on 1.xi.2010, emerged on 20.xii.2010; 1 ♂, laid on 4.xi.2010, emerged on 22.xii.2010; 1 ♂, laid on 10.xi.2010, emerged on 24.xii.2010; 1 ♂, laid on 9.xi.2010, emerged on 28.xii.2010; 1 ♂, laid on 4.xi.2010, emerged on 6.i.2011. Oka, Hirakata, Osaka Pref., 34.8178°N/135.6415°E, R. Matsumoto, OMNH: 1 ♂, 28.ix.2011; 1 ♀, 16 ♂, 24.ix.2011 [1 ♂ for DNA extraction: DNA-ICH-002]. Tawaraguchicho, Ikoma, Nara Pref., 34.7027°N/135.6795°E, 1 ♀, 19.viii.2012, R. Matsumoto, OMNH. Hitakatsu, Tsusima Is., Nagasaki Pref., 1 ♂, emerged from a cocoon of Monema flavescens Walker collected on 28.iii.2013, emerged in iv.2013, K. Sasaki, OMNH. China. Wutaihsien, Shanxi Prov., 1 ♀, 12.viii. SEHU. Chinkiang, Kiangsu [= Jiangsu Prov.], 1 ♀, 12.xi.1918, O. Piel, SEHU. Tchefou [= Yantai] Shandong Prov., 1 ♀, MNHN (coll. de Gaulle). Ningpo, Zhejiang Prov.: 3 ♀, P. Buch, 1924, MHNM; 2 ♀, MNHN (coll. de Gaulle). Moupin, Sichuan Prov., 1 ♀, 1899, Chasseurs indigènes, MNHN (coll. Oberthür). Nepal. Balaju, Kathmandu, 1 ♀, 11.ix.1987, H. Takizawa, SEHU. Vietnam. Chu Yang Sin National Park, 12°27′13.74″N/108°20′21.75″E, Krong Bong District, Dak Lak Province, 1 ♂, 12.iii.2013, K. Konishi. Cuc Phuong, Ha Son Binh Prov. (SEHU): 1 ♂, 28.iv.1996, Y. Okushima, OMNH; 1 ♂, 200–300m alt., 24.iv.1998, R. Matsumoto, OMNH. Ba Be National Park, Ba Be, 200m alt., 22.23°N/ 105.37°E, R. Matsumoto, OMNH: 1 ♂, 4.v.2006; 1 ♂, 1.v.2006. Malaysia. Klapa Bali, 3 ♀, 3 ♂, 10.vi.1949, MNHN. Klapa Bali, “ds cage de Setora nitens”, “VI–VII 1949”, P. Vayssuère: 11 ♀, 5 ♂, 10.vi.1949; 2 ♀, 1 ♂, 11.vi.1949. Indonesia. Semarang, Java, 1 ♀, E. Jacobson, 1906, MNHN. Malang, Java, 1 ♀, MNHN. Gunung Lompobattang, 1250–1350m, South Sulawesi, 1 ♀, 16.xii.2010, K. Takasuka, OMNH. Unknown locality. 2 ♂, “Sina”, MNHN (coll. Sichel).
Fifth instar larva. 1 ex. Isoshima, Hirakata, Osaka Pref., in cocoon of Parasa consocia Walker, 24.ii.2012, R. Matsumoto [OMNH; DNA extraction: DNA-ICH-001].
Punctation on head finer than C. coreanus. Temple flat and narrower, occupying 0.2–0.3 of length of head in dorsal view (Fig.
Adult. ♀. Head 2.0–2.1 times as wide as long in dorsal view (Fig.
Epomia turns horizontally toward mesal line of pronotum at midway to upper edge of pronotum (Fig.
Legs slender. Hind femur 6.0–7.3 times as long as maximum width. Hind tibia 9.3–10.7 times as long as apical width.
Fore wing about 10–15 mm long. Nervellar index 1.8–2.8 (Figs
First metasomal tergite 1.8–2.1 times as long as apical width, with postpetiole 0.6–0.9 times as long as apical width; area between median longitudinal carinae distinctly raised at proximal margin of postpetiole (Figs
Body with metallic luster in blue, purple or green. Flagellum entirely black, without white band. Fore and middle tibiae and all tarsi dark brown to black. Ovipositor sheath and ovipositor black. Wings infumate in variable degrees (Figs
♂. Similar to female except as follows: face 1.2–1.3 times as wide as long; malar space 0.8–1.0 times as long as basal width of mandible; flagellum with 35–37 flagellomeres, with 5 or 6 tyloids which can be on 13th–20th flagellomeres; 1st flagellomere 2.7–3.3 times as long as apical width; 1st metasomal segment 1.6–2.1 times as long as apical width; hind femur 7.3–8.0 times as long as median depth; hind tibia 10.3–12.7 times as long as apical width; anterior side of fore femur, fore tibia and dorsal stripe of middle tibia light brown. Subgenital plate with posterior margin evenly convex and with postero-lateral corner gently rounded (Figs
28–35. Chlorocryptus purpuratus. 36–38. C. coreanus. 28. Second to seventh sterna (♀, Isoshima, Japan); 29. Second to eight sterna and ninth tergites (♂, Isoshima); 30. Gonosquama and basal ring (Isoshima); 31. Aedeagus, lateral view (Isoshima); 32. Aedeagus, ventral view (Isoshima); 33–38. Subgenital plate (33. Isoshima; 34. Cuc Phuong, Vietnam; 35. Klapa Bali, Malaysia; 36. Seonunsan, South Korea; 37. Tieling, Liaoning, China; 38. Keumsan, South Korea.).
Immature stages. Mandible, labral sclerite, epistoma, hypostoma, and labial sclerite well sclerotized through larval development (Figs
Larval morphology of Chlorocryptus purpuratus. 48. Head capsule of 1st instar larva (left mandible is detached); 49. Spiracle of 1st instar larva; 50. Head capsule of 5th instar larva, antennae broken off; 51. Antenna of 5th instar larva; 52 & 53. Spiracle of 5th instar larva. Atp – anterior tentorial pit; cl – clypeus; ep – epistoma; es – epistomal spur; hs – hypostoma; lm – labrum; mx – maxilla; ps – pleurostoma. Scale lines, 0.5 mm (Fig. 48); 0.05 mm (Fig. 49); 0.5 mm (Fig. 50); 0.1 mm (Fig. 51); 0.2 mm (Figs 52 & 53).
First instar larva (Fig.
Second instar larva. Prognathus. Narrow epistomal spur present. Two pairs of setae on labium of 1st instar remaining but upper most one situated just below salivary orifice present only as a hole. Spiracle with atrium differentiated.
Third and fourth instar larvae. Epistomal spur more developed than in 2nd instar and stipital sclerite present.
Final instar larva (Fig.
Several limacodid moths have been recorded as hosts. Some of the moths are serious pests of palm trees in the Oriental Region (
In this study, we observed females collected in Osaka ovipositing into cocoons of Parasa consocia Walker (Fig.
(Figs
Although this species shows a wide range of variation in density of the surface sculpture and setae, wing color (Figs
Despite these large intraspecific variations, this species is clearly distinct from Chlorocryptus coreanus with the above given diagnostic characters.
The distribution of Chlorocryptus purpuratus extends further south than that of C. coreanus although the distributions of both species largely overlap in China (Figs
This is the first record of Chlorocryptus purpuratus from Japan and Vietnam. Considering that C. purpuratus has never before been collected in Japan, most probably the Japanese populations have been introduced recently. Its potential hosts, limacodid moths, are abundant and some of them have been well studied as pests in Japan, including their natural enemies (
In 2012 and 2013, alongside the adults, we also collected two larvae in Parasa consocia cocoons in Osaka. This indicates that C. purpuratus has already been established in this area for two or three years.
One of the limacodid moths, Parasa lepida (Cramer), which had been originally distributed in South Asia, Southeast Asia, and southern China, invaded western Japan and became established in the late 1970’s (
The holotype of Neodontocryptus hyalina Saxena could not be located during the course of this study.
The holotype of the species was deposited in the V. K. Gupta collection, which was originally housed at the University of Delhi. Later, his collection was transferred to Florida, first to the University of Florida (
The lectotypes of Cryptaulax cyaneus Szépligeti and C. metallicus Szépligeti were designated by
INSD accession number: AB851419 for DNA-ICH-001 and AB851420 for DNA-ICH-002. Both have identical sequences.
Cryptaulax coreanus Szépligeti, 1916: 287. Holotype: ♀, Korea, Seoul (HNHM) [examined].
Cryptus trirrhogmaniformis Sonan, 1929: 424. Lectotype: ♂, Formosa, Chikurin (TARI). Synonymized by
Cochlidionostenus coreanus (Szépligeti):
Chlorocryptus coreanus (Szépligeti):
Holotype of Cryptaulax coreanus Szépligeti: ♀, “Korea, Sebul” [“Soeul” in the original description], HNHM (ID 115220). Paralectotype of Cryptus trirrhogmaniformis Sonan: ♂, “Shinchiku, Chikurin, ft. 3000” [= Chulin, Hsinchu], 10.ix.1928, J. Sonan, reared from a cocoon of Monema sp. on a cherry tree, SEHU.
South Korea. Poseoksa (N36°03.073’/E127°28.688’), Keumsan, Chungcheong-namdo, P. Tripotin, SEHU: 1 ♂, viii.1998; 1 ♀, 21.ix.2001. Seonunsan (N36°27’50˝/E126°34’28˝), Geochang, Jeollabuku-do, 1 ♂, 5.vi.2004, C. L. Young, SEHU. Suigen [= Suwon], Gyeonggi-do, K. Sato, SEHU: 1 ♂, 1925; 1 ♀, 4 ♂, 1.vi.1928; 1 ♀, 14.vi.1928. Shôyo-san, Keikido [= Soyosan, Gyeonggi-do], SEHU: 1 ♀, 15.vi.1941; 2 ♂, 10.ix.1943; 2 ♂, 17.ix.1943. Homyeongsan, Cheongpyeong, 1 ♂, 4.v, SEHU. Godaesan, Gyeonggi-do, 1 ♂, 21.vi.1942, SEHU. China. Tetsurei, Manchoukuo, [= Tieling, Liaoning Prov.], 1 ♀, 1 ♂, 11.vi.1938, I. Okada, SEHU. Domonrei, Manchoukuo [= Tumenling, Jiutai, Jilin Prov.], 1 ♀, 1 ♂, 19.viii.1939, H. Kôno, SEHU. Kaigen, Manchoukuo, [= Kaiyuan, Liaoning Prov.], I. Okada, SEHU: 1 ♀, 15.ix.1935; 1 ♀, 1.vi.1938. Ryôsuiji, Dalian, 1 ♀, 23.vi.1929, SEHU. “Nord Pekin”, 1 ♂, A. David, 1865, MNHN.
Punctation on head coarser than C. purpuratus. Temple swollen and wide, occupying 0.3–0.4 of length of head in dorsal view (Fig.
Adult. ♀. Head (Fig.
Epomia ends at midway to upper edge of pronotum without turning toward mesal line of pronotum (Fig.
Legs slender. Hind femur 6.0–7.7 times as long as maximum width. Hind tibia 8.5–9.5 times as long as apical width.
Fore wing about 11–14 mm long. Nervellar index 1.3–1.8 (Figs
First metasomal tergite 1.9–2.3 times as long as apical width, with postpetiole 0.7–1.0 times as long as apical width; dorsal face not distinctly raised; median longitudinal carina absent or very weak on its entire length (Figs
Body with metallic luster in blue, purple or green. Flagellum black with white band on 6th–9th flagellomeres. Fore and middle tibiae and all tarsi are dark brown to black. Ovipositor sheath and ovipositor black. Wings narrowly infumate apically (Fig.
♂. Similar to female except as follows: face 1.0–1.2 times as wide as long; flagellum with 37–39 flagellomeres, with 5 or 6 tyloids which can be on 14th–20th flagellomeres; 1st flagellomere 2.8–3.3 times as long as apical width; 1st metasomal segment 2.0–2.4 times as long as apical width; hind femur 7.0–8.5 times as long as median depth; hind tibia 9.3–10.0 times as long as apical width; stripe on anterior face of fore femur, fore tibia and dorsal stripe of middle tibia light brown. Subgenital plate with postero-lateral corner more angulated than in C. purpuratus, with posterior margin convex, with small concavity on middle of convexity (Figs
Monema flavescens Walker (
(Fig.
Similar to the preceding species, this species shows considerable intraspecific morphological variation. Only the Taiwanese specimens, namely the type series of Cryptus trirrhogmaniformis, have the fore wings entirely tinged with brown (Fig.
In the description of Cryptaulax coreanus,
Cryptus trirrhogmaniformis Sonan was described based on two male syntypes. One was deposited at TARI and the other was probably donated to Uchida at that time and now is located at SEHU. The TARI specimen was treated as “type” by
1 | Temple swollen and wide, occupying 0.3–0.4 of length of head in dorsal view (Fig. |
C. coreanus (Szépligeti). |
– | Temple flat and narrower, occupying 0.2–0.3 of length of head in dorsal view (Fig. |
C. purpuratus (Smith). |
We are indebted to the following people for the loan or gift of the material used in this study: Kimitaka Sasaki (Fukuoka), Yasutaka Mori (Shionogi & Co., Ltd.), Mika Sugimoto (The Kyushu University Museum), Keizo Takasuka (Kobe University), Claire Villemant (MNHN), Agnièle Touret-Alby (MNHN), Gavin R. Broad (BMNH), Gellért Puskás (HNHM), and Pierre Tripotin (Whitfield, Queensland). We also thank Jim Wiley (Florida State Collection of Arthropods) and Virendra K. Gupta (Gainesville, Florida) for information about the type of Neodontocryptus hyalina. The first author thanks Toshiaki Ito and Masanori Yasui (Electron Microscope Laboratory, Graduate School of Agriculture, Hokkaido University) for their advice on SEM photography and Yuta Ueno (Animal Ecology, Graduate School of Agriculture, Hokkaido University) for his help in literature search. His cordial thanks extend to Kazunori Yoshizawa (SEHU) and Masahiro Ôhara (SEHU) for their continuous guidance and encouragement. Kazuhiko Konishi (Ehime University Museum) and David R. Smith (National Museum of Natural History, Smithsonian Institution, Washington DC) have kindly reviewed our draft version of the manuscript.