Diptera: Cecidomyiidae: Asphondyliini) from Palaearctic and Oriental Regions, with Descriptions of Two New Species That Induce Stem Galls on Lauraceae in Japan

SYSTEMATICS First Records of Genus Bruggmanniella (Diptera: Cecidomyiidae: Asphondyliini) from Palaearctic and Oriental Regions, with Descriptions of Two New Species That Induce Stem Galls on Lauraceae in Japan

1, 2 3, 4 MAKOTO TOKUDA AND JUNICHI YUKAWA Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 Ann. Entomol. Soc. Am. 99(4): 629Ð637 (2006) ABSTRACT Two new species of the genus Bruggmanniella, Bruggmanniella actinodaphnes and Bruggmanniella cinnamomi (Diptera: Cecidomyiidae: Asphondyliini: Asphondyliina) are described from Japan. The former species induces stem galls on Actinodaphne lancifolia (Siebold et Zucc.) (Lauraceae) in the Palaearctic Region, and the latter species induces stem galls on Cinnamomum japonicum (Lauraceae) in the Oriental Region. Bruggmanniella, previously known to occur only in the Neotropical and southern Nearctic regions, is recorded for the Þrst time from the Palaearctic and Oriental regions. The number of genera, their components, and morphological features of Asphon- dyliina are compared between different zoogeographical regions.

KEY WORDS Asphondyliini, Bruggmanniella, Cecidomyiidae, gall midge, Lauraceae

THE TRIBE ASPHONDYLIINI IS a well circumscribed mono- Many species of the subtribe Asphondyliina have phyletic group sharing unique characteristics of the been known to induce various galls on broad-leaved adult postabdomen and is divided into two subtribes, evergreen trees of Lauraceae in the Oriental and Asphondyliina and Schizomyiina (Gagne´ 1994, 2004). eastern Palaearctic regions, such as India (Kieffer The tribe is a taxonomically and phylogenetically 1905), southwestern Japan (through which the well studied group compared with other tribes of boundary of the Palaearctic and Oriental regions ex- Cecidomyiidae (Mo¨hn 1961, Gagne´ 1994), but many tends; Fig. 1) (Yukawa 1974, Yukawa and Masuda species are still unnamed in various parts of the world. 1996), Taiwan (Yang et al. 1999), and Indonesia and In addition, Asphondyliini exhibit various unique eco- Thailand (Yukawa et al. 2005). Accordingly, we have logical and life history traits, such as host alternation been paying special attention to Lauraceae trees in our (Harris 1975; Orphanides 1975; Yukawa et al. 2003; search for galling species of Asphondyliina at various Uechi et al. 2004, 2005), polyphagy (Gagne´ and Woods localities in Japan. In recent Þeld surveys, we have 1988, Tokuda et al. 2005), prolonged diapause (Maeda collected several galls of Asphondyliina on Lauraceae et al. 1982, Takasu and Yukawa 1984, Tabuchi and from Japan. In this article, we describe two new spe- Amano 2003), and association with fungal symbionts cies of the genus Bruggmanniella that induce stem galls (Meyer 1987, Bissett and Borkent 1988, Yukawa and on trees of Lauraceae. We compare generic compo- Rohfritsch 2005). Therefore, further taxonomic, phy- nents and morphological features of Asphondyliina, logenetic, and ecological studies of Asphondyliini are including Bruggmanniella, between the Neotropical required to elucidate the evolution of these traits, in and Palaearctic regions. particular the processes of host range expansion, including host plant shift and galled organ shift (Tokuda and Yukawa 2005). Materials and Methods Collection of Galls and Gall Midges. Some of the collected galls were dissected under a stereoscopic 1 Entomological Laboratory, Graduate School of Bioresources and microscope to obtain larval and pupal specimens. Bioenvironmental Sciences, Kyushu University, Fukuoka 812-8581, When some of the dissected galls contained mature Japan. larvae or pupae, the rest of the collected galls were 2 Corresponding author, address: Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and maintained in plastic bags (350 by 250 mm) to obtain Technology, Tsukuba, Ibaraki 305-8566, Japan (e-mail: tokuda- adults and pupal exuviae. All specimens collected in [email protected]). this study were preserved in 75% ethanol or 99.5% 3 Entomological Laboratory, Faculty of Agriculture, Kyushu Uni- acetone. versity, Fukuoka 812-8581, Japan. 4 Current address: Matsuzaki 1-5-12, Higashi-ku, Fukuoka 813-0035, Preservation of Specimens Examined. All speci- Japan. mens examined, including holotypes and paratypes,

0013-8746/06/0629Ð0637$04.00/0 ᭧ 2006 Entomological Society of America 630 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 99, no. 4

Table 1. B. actinodaphnes sp. n.: frontoclypeal and thoracic (for each sex 7 ؍ setal counts (n

Male Female Mean SD Range Mean SD Range Frontoclypeal setae 25.0 2.94 21Ð28 21.3 4.72 18Ð28 ADL setaea 73.0 19.76 61Ð108 69.6 5.13 65Ð76 PDL setaeb 96.2 12.03 83Ð112 91.8 17.63 81Ð118 Mesopleural setae 56.0 8.00 45Ð65 55.0 12.37 46Ð76 Mesepimeral setae 57.0 4.98 50Ð63 60.4 7.16 52Ð71

a Anterior dorsolateral setae. b Posterior dorsolateral setae. Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 Hemibruggmanniella Mo¨hn, 1961: 6. Type species Bruggmanniella oblita Tavares 1920 The genus Bruggmanniella belongs to the subtribe Asphondyliina and comprises six known species in the world (Gagne´ 2004, Gagne´ et al. 2004). Among them, Þve species occur in the Neotropical Region and one in the southern parts of the Nearctic Region. Because Fig. 1. Collection records of B. actinodaphnes and the morphological features of Bruggmanniella were B. cinnamomi based on Yukawa (1976), Usuba (1977), Yama- summarized and discussed in Gagne´ (1994) and uchi et al. (1982), Yukawa (1988), Yukawa and Masuda Gagne´ et al. (2004), we refer in this article only to (1996), and the present results. The broken line illustrates morphological differences between Bruggmanniella the boundary between Oriental and Palaearctic zoogeo- and allied genera in the Palaearctic Region as fol- graphical regions. lows: Bruggmanniella is similar to Pseudasphondylia Monzen, 1955 in most male morphological features are preserved in the collection of the Entomological such as the presence of parameres and the two sep- Laboratory, Kyushu University, Fukuoka, Japan. arate teeth of the gonostylus. However, Bruggman- Morphological Studies and Terminology. For mi- niella can be distinguished from Pseudasphondylia by croscopic study, some of the ethanol-preserved spec- the presence of setae on the larval cervical papillae imens were mounted on slides in Canada balsam by and on all papillae of the ventral surface (Tokuda and using the techniques outlined in Gagne´ (1989). Draw- Yukawa 2005). Bruggmanniella, with its two separate ings were made with the aid of a drawing tube. Some teeth on the gonostylus, is distinguishable from Pro- important structures of the pupae were examined with bruggmanniella Mo¨hn, 1961, which has a single tooth. a scanning electron microscope (S-3000N, Hitachi, It differs from Illiciomyia Tokuda, 2004 by having Tokyo, Japan) by using the acetone-preserved spec- several morphological features such as less constricted imens. male ßagellomeres, convolute male circumÞla, pres- Adult morphological terminology, except for that of ence of an apical spur on the Þrst tarsomeres, and thoracic plates, follows use in McAlpine (1981) and absence of asetose lateral papillae on larval thoracic that of thoracic plates follows use in Tokuda (2004) segments (Tokuda 2004). and Tokuda et al. (2004b). Counts of setae and scales were based on the setal and scale insertions because Bruggmanniella actinodaphnes many setae and scales become lost through the pro- Tokuda & Yukawa sp. n. cesses of collection, preservation, and preparation. (Figs. 2A and B, 3A and B; Tables 1 and 2) Morphological terminology of the immature stages follows use in Mo¨ hn (1955, 1961), which was orig- Male. Eye bridge four to six facets long. Frontocly- inally written in German and later translated into peal setal count as in Table 1. Palpus two-segmented; English in Yukawa (1971), but terminology of the Þrst palpal segment Ϸ38 ␮m long, Ϸ1.3 times as long pupal antennal horn follows that in Gagne´ (1994). as basal width; second Ϸ2.0 times as long as Þrst. In addition, the term “anterior dorsal papillae” (To- Antenna with 12 ßagellomeres; scape and pedicel with kuda et al. 2004a,b) is applied to pupal abdominal rather dense setae; Þrst and second ßagellomeres not papillae that are situated in the anterior fourth of fused; Þrst ßagellomere Ϸ215 ␮m long, 4.3 times as the dorsal surface and distinctly anterior to the row long as wide, 1.2 times as long as second, Þfth ßag- of “dorsal papillae.” ellomere Ϸ160 ␮m long, 3.3 times as long as wide. Thoracic setal counts as in Table 1. All legs covered with many blackish scales; length of respective seg- Taxonomy ments as in Table 2; Þrst tarsomeres of all legs each Genus Bruggmanniella Tavares with a short apical spur; claw simple on all legs, bent Bruggmanniella Tavares, 1909: 19. Type species: Brugg- nearly at right angle; empodium well developed, as manniella braziliensis Tavares 1909 long as claw; pulvillus much shorter than empodium. July 2006 TOKUDA AND YUKAWA: Bruggmanniella,NEW TO PALAEARCTIC/ORIENTAL REGIONS 631

(for each sex 7 ؍ Table 2. B. actinodaphnes sp. n.: measurements of legs (micrometers, n

Male Female Mean SD Range Mean SD Range Foreleg Femur 1,272 53.8 1,197Ð1,344 1,118 91.2 985Ð1,241 Tibia 1,154 94.1 1,083Ð1,348 1,016 113.5 837Ð1,154 Tarsomere I 174 13.7 154Ð192 178 30.4 141Ð210 Tarsomere II 970 157.8 763Ð1123 889 156.8 641Ð1,053 Tarsomere III 441 25.6 415Ð475 366 46.4 314Ð410 Tarsomere IV 320 40.6 281Ð375 249 22.9 224Ð269 Tarsomere V 207 12.8 194Ð224 200 39.9 158Ð254 Mid-leg Femur 1,212 131.3 941Ð1324 1,163 114.9 961Ð1,269 Tibia 1,018 75.2 904Ð1109 956 104.7 773Ð1,063 Tarsomere I 172 18.6 151Ð206 178 17.0 148Ð193 Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 Tarsomere II 933 78.4 885Ð1071 719 91.7 609Ð883 Tarsomere III 445 44.5 410Ð522 331 28.8 303Ð381 Tarsomere IV 312 30.3 280Ð359 269 39.9 210Ð323 Tarsomere V 208 20.8 183Ð227 172 18.1 149Ð196 Hindleg Femur 1,279 54.5 1,203Ð1,350 1,247 65.3 1,173Ð1,362 Tibia 1,063 89.3 931Ð1198 1,018 118.5 904Ð1,184 Tarsomere I 184 18.4 167Ð222 173 24.8 143Ð212 Tarsomere II 935 163.4 721Ð1118 713 66.7 652Ð831 Tarsomere III 446 9.7 437Ð458 334 27.7 297Ð368 Tarsomere IV 332 23.5 303Ð354 255 28.5 207Ð280 Tarsomere V 224 18.5 198Ð242 183 37.4 150Ð256

Wing length 2.8Ð3.4 mm, Ϸ2.2 times as wide, densely 13 ␮m long, 1.3 times as long as basal width; cervical clothed in dark grayish hairs; R5 joining costa a little papillae each with seta. Number and position of spi- beyond wing apex. racles normal; four dorsal papillae present on all tho- Tergites without anterior pair of trichoid sensilla; racic and Þrst through seventh abdominal segments, Þrst through seventh tergites rectangular; Þrst through each with seta; eighth abdominal segment with two sixth tergites with double row of posterior setae, dorsal papillae, each with seta; two pleural papillae seventh tergite with mostly triple row of posterior present on each side, each with seta; two terminal setae; anterior portion of eighth tergite pigmented, papillae present, each with minute seta. Sternal spat- without setae; some lateral setae present on Þrst to ula (Fig. 2B) 190Ð230 ␮m long, anteriorly with two seventh tergites; elsewhere covered with scales on triangular lobes; two inner and two outer lateral pa- Þrst through seventh tergites. Sternites without ante- pillae present on all thoracic segments, each with seta; rior pair of trichoid sensilla; Þrst through sixth sternites sternal papillae each with seta on all thoracic seg- rectangular, 0.25Ð0.34 times as long as wide; seventh ments; inner pleural papillae probably absent; anterior and eighth sternites a little elongated, 0.44 and 0.57 and posterior ventral papillae not apparent; anal pa- times as long as wide, respectively. Genitalia (Fig. 2A): pillae not apparent. Each abdominal segment, except cerci setose, each usually rounded at apex, rarely com- terminal one, ventrally with many transverse rows of pletely fused; hypoproct incised deeply by V-shaped minute spines and with many small triangular spines emargination, each lobe with two apical setae; gono- ventro- and dorsolaterally. stylus suboval, distally with two sclerotized teeth, the Pupa. Pupal skin not pigmented except for apical teeth 8.5 ␮m apart from one another; gonocoxite horn. Body length Ϸ3.6 mm. Apical horn broad, dor- rather elongate, ventrally extending a little beyond soventrally ßattened, with three Þngerlike projec- insertion of gonostylus; paramere relatively large, usu- tions, the mesalmost longest, lateralmost shortest, ally with distinct seta; aedeagus laterally sclerotized, length from the base of antennal sheath to the tip of distally tapering. apical horn 300Ð370 ␮m (Fig. 3A); apical papillae Female. Distal ßagellomeres shortened and termi- without setae; upper and lower frontal horns absent; nal one subglobular; Þfth ßagellomere 150 ␮m long, usually a pair of lower facial papillae and two pairs of Ϸ3.0 times as long as wide. Wing length Ϸ3.65 mm, lateral facial papillae present, each without setae; pro- Ϸ2.2 times as long as wide. Seventh sternite Ϸ1.2 times thoracic horn 150Ð180 ␮m long; stigmatal tubercles as long as wide; eighth sternite without setae. Ovipos- present on second to sixth abdominal segments, each itor protractile, slender, aciculate, basally with a bi- 35Ð50 ␮m long; those on seventh and eighth abdominal lobed cerci-like structure. Needle part of ovipositor segments rudimentary; Þrst abdominal segment Ϸ1.05 mm long, Ϸ1.6 times as long as the length of densely covered with minute spines; second to eighth seventh sternite; minute apical lobe of ovipositor with- abdominal segments densely covered with minute out setae. Otherwise as in male. spines on ventral surface and on middle third of dorsal Mature Larva. Body color pale green, length 2.6Ð surface; second to eighth abdominal segments with 3.1 mm. Second antennal segment short, conical, Þve to seven transverse rows of rather long spines on 632 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 99, no. 4 Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021

Fig. 2. (A) Male genitalia (dorsal view) of B. actinodaphnes sp. n. (B) Larval sternal spatula of B. actinodaphnes. (C) Male genitalia (dorsal view) of B. cinnamomi. (D) Larval sternal spatula of B. cinnamomi. Scale bar ϭ 0.1 mm.

Fig. 3. (A) Pupal head and frontal area of B. actinodaphnes sp. n. (B) Pupal abdominal segments (dorsal view) of B. actinodaphnes. (C) Pupal head and frontal area of B. cinnamomi sp. n. (D) Pupal abdominal segments (dorsal view) of B. cinnamomi. July 2006 TOKUDA AND YUKAWA: Bruggmanniella,NEW TO PALAEARCTIC/ORIENTAL REGIONS 633 Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 Fig. 4. (A) Stem galls caused by B. actinodaphnes on A. lancifolia. (B) Stem galls caused by B. cinnamomi on C. japonicum. anterior third of dorsal surface (Fig. 3B), each spine ethanol), Izuhara, Tsushima Island, Nagasaki, galls col- 8Ð20 ␮m long; six dorsal papillae present on Þrst to lected 27-IV-2001, M. Shoubu; one pupa (in acetone), seventh abdominal segments, outermost pair each Izuhara, Tsushima Island, Nagasaki, galls collected 28- with seta, remaining four usually without setae, rarely IV-2001, M. Shoubu, adults emerged 5-10-V-2001, each with minute seta; two anterior dorsal papillae reared by M. Tokuda; 4 larvae (in ethanol) and 4 larvae present on second to eighth abdominal segments, each (in acetone), Kamiyama, Tokushima, Shikoku, 22-XI- with a seta; a pleural papilla present on each side, 2001, M. Yukinari. usually each with two minute setae, rarely with one Distribution. This gall midge was previously col- minute seta. lected from Honshu and Kyushu, Japan (Fig. 1) Host Plant. Actinodaphne lancifolia (Sieb. and (Yukawa 1976, Usuba 1977, Yukawa 1988) and is re- Zucc.) Meissn. (Lauraceae). corded for the Þrst time from Shikoku, Japan, in this Gall. Subconical swelling on the stem, rounded api- article. It has not yet been found in the southwest cally; usually many galls occurring together; mono- islands of Japan. thalamous (Fig. 4A; see also Gall No. C-250 in Yukawa Remarks. This species is distinguishable from the and Masuda 1996). other congeners in the Neotropical and Nearctic re- Biological Notes. The life history of this species has gions by the two-pointed anterior lobes of the larval not yet been intensively studied. It seems to be uni- sternal spatula (Fig. 2B), whereas the spatula has voltine, but some individuals may require 2 yr for one three- or four-pointed lobes in the Neotropical and generation (Yukawa and Masuda 1996). Stem galls Nearctic species (Gagne´ 1994, 2004). The pupal apical collected in December contained mature larvae and horn (Fig. 3A) is also unique by having three apical most adults emerged from the galls on the host plant Þngerlike projections. between early April and early May in the following A congener, which is morphologically very similar year. to B. actinodaphnes was collected several times in Holotype. Male (on slide, Cecid. No. B4001; Type Japan so far (Yukawa 1976; Usuba 1977; Yukawa 1979, No. 3228, kept in the Entomological Laboratory, 1988; unpublished data) but has been left unnamed Kyushu University, Fukuoka, Japan). JAPAN: Galls because of the inadequate number of specimens for were collected on 27-IV-1984 by J. Yukawa from Shi- description. It induces stem galls (Yukawa and royama, Kagoshima, Kyushu. The holotype emerged Masuda 1996) on Actinodaphne acuminata (Bl.) on 4-V-1984. Meissn. (ϭA. longifolia). Paratypes. JAPAN: 5 ((,6&&, and 6 pupae (on slides, Cecid. Nos. B4002Ð12, 405Ð56) same data as Bruggmanniella cinnamomi holotype; 1 (,1&, and 1 pupa (on slides, Cecid. Nos. Tokuda & Yukawa sp. n. B4013Ð14, B4057), Iso, Kagoshima, Kyushu, galls col- (Figs. 2C and D, 3C and D; Tables 3 and 4) lected 1-V-1969, A. Mori, adults emerged 1-3-V-1969, reared by J. Yukawa; two larvae (on slides, Cecid. Nos. Male. Eye bridge six to eight facets long. Fronto- B4076Ð77), Ishiki, Kagoshima, Kyushu, 13-XII-1969, clypeal setal count as in Table 3. Palpus three-seg- J. Yukawa; 10 larvae (on slides, Cecid. Nos. B4078Ð mented; Þrst palpal segment Ϸ45 ␮m, Ϸ1.4 times as 87), Kamiyama, Tokushima, Shikoku, 22-X-2001, M. long as basal width; second Ϸ1.4 times as long as Þrst; Yukinari. third Ϸ1.1 times as long as second. First ßagellomere Other Material Examined. JAPAN: 2 ((,3&&, and 200Ð250 ␮m long, Ϸ4.5 times as long as wide, Ϸ1.2 8 pupae (in ethanol), same data as holotype; many times as long as second, Þfth ßagellomere 160Ð185 ␮m, larvae (in ethanol), Ishiki, Kagoshima, Kyushu, 13- Ϸ3.4 times as long as wide. Wing length Ϸ2.6 mm, XII-1969, J. Yukawa; 1 larva (in ethanol) and 1 larva (in Ϸ2.3 times as long as wide. First through sixth sternites acetone), Mount Mukabaki, Miyazaki, Kyushu, 18-XI- 0.38Ð0.48 times as long as wide, seventh sternite 2000, M. Tokuda & J. Yukawa; 3 && and 2 pupae (in Ϸ0.63 times as long as wide, and that of eighth sternites 634 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 99, no. 4

Table 3. B. cinnamomi sp. n.: frontoclypeal and thoracic setal terolaterally with small lobe, outer margin of the small -males and 5 females) lobe Þnely denticulate, length from the base of an 6 ؍ counts (n tennal sheath to the tip of apical horn 410Ð470 ␮m Male Female (Fig. 3C); apical papilla with 80 ␮m long seta; upper Mean SD Range Mean SD Range and lower frontal horns absent; lower and lateral facial Frontoclypeal setae 18.7 3.08 16Ð24 16.3 4.35 12Ð20 papillae not visible; prothoracic horn 270Ð290 ␮m ADL setaea 37.2 4.07 30Ð41 43.8 1.71 42Ð46 b long; stigmatal tubercles on second to sixth abdominal PDL setae 34.7 4.46 30Ð40 38.2 3.77 34Ð44 ␮ Mesopleural setae 33.0 2.83 31Ð35 32.7 4.16 28Ð36 segments 25Ð32 m long; Þrst abdominal segment Mesepimeral setae 36.2 4.92 30Ð42 29.7 2.08 28Ð32 densely covered with minute spines on ventral and dorsal surface; second to eighth abdominal segments a Anterior dorsolateral setae. b densely covered with minute spines on ventral surface Posterior dorsolateral setae. and on posterior half of dorsal surface; second to eighth abdominal segments with nine to 11 transverse Ϸ0.48 times as long as wide, respectively. Genitalia rows of rather short spines on anterior one-half of Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 (Fig. 2C): cerci setose, each usually triangular at apex, dorsal surface (Fig. 3D), each spine 12Ð23 ␮m long; rarely completely fused; hypoproct incised very shal- usually eight dorsal papillae present on Þrst to seventh lowly by U-shaped emargination, each lobe with one abdominal segments, most outer and second inner or two apical setae. Otherwise as in B. actinodaphnes. pairs each with minute seta, sometimes most inner and Female. First ßagellomere 210 ␮m long, 5.6 times as second inner papilla more or less fused; anterior dorsal long as wide, 1.3 times as long as the second; Þfth papillae absent; each segment with one pleural papilla, ßagellomere 140 ␮m long, 3.7 times as long as wide. with a seta. Otherwise as in B. actinodaphnnes. Wing length Ϸ3.1 mm, 2.4 times as long as wide. Host Plant. Cinnamomum japonicum Sieb. ex Nees Seventh sternite Ϸ1.4 times as long as wide. Needle (Lauraceae). part of ovipositor 0.88 mm, Ϸ1.7 times as long as the Gall. Massive subglobular or elongated subglobular length of seventh sternite. Otherwise as in the female swelling on the stem, diameter 10Ð40 mm, containing of B. actinodaphnes. many small larval chambers (Fig. 4B; see also Gall No. Mature Larva. Body color pale yellow. Body length C-264 in Yukawa and Masuda 1996). 2.7Ð3.5 mm. Second antennal segment 11 ␮m long, Biological Notes. The life history of this species is 1.8 times as long as basal width. Sternal spatula still unclear although this species is suspected to be (Fig. 2D) 290Ð320 ␮m long, anteriorly with two tri- univoltine (Yamauchi et al. 1982, Yukawa and Masuda angular lobes, additional sclerotized portion present 1996). Stem galls that were collected in December had laterally to each triangular lobe. Otherwise as in already developed to full size but contained Þrst in- B. actinodaphnes. stars. Adults emerged from the galls between mid- Pupa. Head and thoracic parts of pupal skin slightly March and early April the following year. pigmented. Body length 3.5Ð4.3 mm. Apical horn dor- Holotype. Male (on slide; Cecid. No. C7101; Type soventrally ßattened, anterior margin narrowed, pos- No. 3229, kept in the Entomological Laboratory,

(males and 5 females 6 ؍ Table 4. B. cinnamomi sp. n.: measurements of legs (micrometers, n

Male Female Mean SD Range Mean SD Range Foreleg Femur 1,071 64.9 986Ð1,134 1,136 110.1 1,014Ð1,312 Tibia 1,100 56.3 1,010Ð1,169 1,226 51.9 1,158Ð1,291 Tarsomere I 135 19.8 104Ð157 157 19.8 125Ð176 Tarsomere II 905 58.3 824Ð962 934 35.6 895Ð972 Tarsomere III 516 20.3 487Ð531 494 30.0 466Ð524 Tarsomere IV 376 23.8 344Ð397 338 11.6 322Ð349 Tarsomere V 211 12.2 200Ð230 227 15.9 209Ð243 Mid-leg Femur 958 40.7 890Ð1020 993 74.4 899Ð1088 Tibia 920 6.3 911Ð928 955 43.7 908Ð1,002 Tarsomere I 127 18.7 107Ð157 160 19.4 134Ð188 Tarsomere II 669 61.8 584Ð771 611 40.3 560Ð649 Tarsomere III 433 16.0 407Ð453 400 38.0 364Ð465 Tarsomere IV 307 24.5 273Ð336 276 8.9 265Ð284 Tarsomere V 206 21.9 173Ð233 208 14.7 192Ð224 Hindleg Femur 1,132 104.5 989Ð1,295 1,157 162.5 906Ð1,359 Tibia 1,053 52.7 978Ð1,106 1,071 105.7 893Ð1,177 Tarsomere I 127 22.5 105Ð162 147 28.7 99Ð176 Tarsomere II 731 69.6 641Ð830 693 60.8 620Ð754 Tarsomere III 486 31.9 458Ð532 436 85.2 380Ð586 Tarsomere IV 373 15.4 358Ð394 315 40.4 264Ð356 Tarsomere V 239 22.4 207Ð269 214 16.0 192Ð235 July 2006 TOKUDA AND YUKAWA: Bruggmanniella,NEW TO PALAEARCTIC/ORIENTAL REGIONS 635

Kyushu University, Fukuoka, Japan). JAPAN: Naka- have been designated for the subtribe (Gagne´ 2004, gusuku, Okinawa, galls collected on 25-II-2001 by Tokuda 2004, Tokuda et al. 2004a). J. Yukawa and S. Yamauchi. The holotype emerged The genus Bruggmanniella was previously recorded 15-III-2001, reared by M. Tokuda. from the Neotropical and Nearctic regions, but this Paratypes. JAPAN: 5 ((,5&&, eight pupae, and article reveals that it occurs also in the Palaearctic and three larvae (on slides, Cecid. No. C7102Ð11, C7151Ð Oriental regions. As a result, eight genera of Asphon- 58, C7176Ð78), same data as holotype except emer- dyliina have been recorded from the Palaearctic Re- gence dates (between 15- and 21-III-2001); 3 ( and 6 gion, compared with ten genera in the Neotropical pupae (on slides, Cecid. No. C7112Ð14, C7159Ð64), Region (Gagne´ 2004, Tokuda 2004). In contrast to the Aha, Kunigami, Okinawa, 5-III-2002, M. Tokuda and Neotropical and Palaearctic regions, the Nearctic Re- H. Kuratomi, adults emerged between 10- and 19-III- gion is a genus-poor area, where only two genera of 2002. Asphondyliina, Asphondylia H. Loew, 1850 and Brugg- Other Material Examined. JAPAN: many adults and manniella, occur (Gagne´ 1989, 2004). Asphondyliina pupae (in acetone or ethanol), same data as holotype; have been relatively well-studied taxonomically in the Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 many adults and pupae (in acetone or ethanol), Aha, Nearctic (Gagne´ 1989), Neotropical (Mo¨hn 1961, Kunigami, Okinawa, galls collected 5-III-2002, Gagne´ 1994), and Palaearctic regions (Mo¨hn 1961; M. Tokuda & H. Kuratomi, adults emerged 10Ð19-III- Kovalev 1964; Yukawa 1971, 1974; Tokuda 2004; To- 2002, reared by M. Tokuda. kuda and Yukawa 2005), but only a few species have Distribution. The southwest islands, Japan (from been described from the other zoogeographical re- Kikaijima Island to Ishigakijima Island, included in the gions: for example, Coutin (1980) and Kolesik (1995) Oriental Region; Fig. 1) (Yukawa and Masuda 1996). in the Australian; Kieffer (1913) in the Afrotropical; Galls caused by this gall midge are commonly seen on and Kieffer (1905), Gagne´ (1973), Yukawa (1981), Okinawa Island and have been collected once in 1978 and Uechi and Yukawa (2004) in the Oriental regions. from Mount Omoto, Ishigakijima Island (Yamauchi et So, further studies are needed to discuss generic com- al. 1982). Current and old galls could not be found in ponents of Asphondyliina in these regions. March 2000 and March 2001 on Ishigakijima and Although there is no big difference in the numbers Iriomotejima islands, although at least 50 large trees of genera between the Neotropical (10 genera) and and many saplings were surveyed on respective is- Palaearctic regions (eight genera), the generic com- lands. The galls have never been collected in Honshu, ponents of Asphondyliina are much different between Shikoku, and Kyushu, Japan, which are included in the the two regions. In the Neotropical region, all genera, Palaearctic Region (Yukawa and Masuda 1996), even except for Bruggmanniella, are considered to be phy- though the host plant is naturally distributed in these logenetically rather close to Asphondylia, which is the areas (Horikawa 1972). largest, cosmopolitan, and radiating genus of Asphon- Remarks. This species differs from the other con- dyliina (Gagne´ 2004, Yukawa et al. 2005), because geners by the unique pupal apical horn (Fig. 3C) and these genera share all or some synapomorphies, such shape of the larval sternal spatula (Fig. 2D). On the as, e.g., pigmented pupal skin, presence of upper and southwest islands of Japan, similar stem galls have lower frontal horns, absence of parameres on gono- been found on Cinnamomum doederleinii Engeler coxites (Mo¨hn 1961, Gagne´ 1994). In contrast to the and Machilus thunbergii Sieb. and Zucc. (Lauraceae) Neotropical genera, all Palaearctic genera, except for (Yamauchi et al. 1982; Yukawa and Masuda 1996). Asphondylia and Houardiella Kieffer, 1912, do not pos- However, the taxonomic position of the gall midges sess these synapomorphies. Indeed, Palaearctic genera that are responsible for these stem galls was not de- have some morphological features that are common to termined because we had no adult and pupal speci- those of Schizomyiina and not found in Nearctic As- mens of the gall midges to examine. phondyliina other than Bruggmanniella, such as stubby ovipositors in Daphnephila Kieffer, 1905, shal- low construction of male ßagellomeres and absence of Discussion apical spur on the Þrst tarsomeres in Illiciomyia, and In the tribe Asphondyliini, two subtribes, Asphon- absence of setae on larval cervical papillae and on dyliina and Schizomyiina, have been clearly divided some papillae on the ventral surface in Pseudasphon- based on the Neotropical and western Palaearctic taxa dylia (Yukawa 1971, 1974; Tokuda and Yukawa 2002, by many synapomorphies (Mo¨hn 1961, Gagne´ 1994). 2005; Tokuda 2004). Therefore, these Palaearctic gen- However, recent taxonomic studies of the tribe in the era probably diverged earlier than the Nearctic genera eastern Palaearctic Region have demonstrated that from a common ancestor of Asphondylia and its related some genera could not be clearly classiÞed into either genera. Such differences in generic components of Asphondyliina or Schizomyiina in the light of the Asphondyliina possibly imply that the common an- previous subtribal concept (Tokuda 2004, Tokuda et cestor of the subtribe Asphondyliina originated in the al. 2004a). At present, only two characteristics, the Old World and that of the genus Asphondylia in the solid tooth or teeth of the gonostylus and the dorsally Neotropical Region. situated larval anus, are regarded as synapomorphies In the Neotropical and Nearctic regions, Bruggman- of the subtribe Asphondyliina (Tokuda 2004), niella is associated with various plant families such as whereas Schizomyiina seems to be a paraphyletic Anacardiaceae, Celastraceae, Malpighiaceae, Mora- group of Asphondyliina, because no synapomorphies ceae, and Sapotaceae (Gagne´ 2004). In these regions, 636 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 99, no. 4

Bruggmanniella perseae Gagne´, 2004 is the only species in the present radiation of the genus Asphondylia that is associated with Lauraceae, inducing fruit galls (Gagne´ 2004, Yukawa et al. 2005). on avocado, Persea americana Mill. (Gagne´ et al. 2004). Morphologically, B. perseae seems closer to the other Neotropical congeners than to the Palaearctic and Acknowledgments Oriental species that induce stem galls on Lauraceae. We express our thanks to R. J. Gagne´ and K. M. Harris for For example, the larval sternal spatula has four ante- critical reading of a draft. We are grateful to H. Kuratomi, rior lobes in B. perseae and some congeners in the A. Mori, S. Yamauchi, and M. Yukinari for offering gall midge Neotropical Region (Gagne´ et al. 2004), but only two specimens. M.T. thanks O. Tadauchi, S. Kamitani, and lobes in the Palaearctic species. In addition, the male D. Yamaguchi for support. This study was partly supported by cerci are fused basally in B. perseae and Neotropical the Research Fellowships of the Japanese Society for the congeners but usually discrete two lobes in the Palae- Promotion of Sciences for Young Scientists (to M.T.). arctic species. These differences indicate that Brugg- manniella species possibly have become gallers on Downloaded from https://academic.oup.com/aesa/article/99/4/629/62315 by guest on 01 October 2021 Lauraceae independently in the Palaearctic and Neo- References Cited tropical regions. However, there are still many unde- Bissett, J., and A. Borkent. 1988. Ambrosia galls: the signif- scribed species associated with Machilus, which is an icance of fungal nutrition in the evolution of the Ce- allied genus of Persea, in the Palaearctic and Oriental cidomyiidae (Diptera), pp. 203Ð225. In K. A. Pirozynski regions (Yukawa et al. 2005). Further morphological and D. L. 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