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Vol. 26, No. 4 Dec., 2004

Descriptions of the Immature Stages of Three Species of the Tribe (Heteroptera: Lygaeidae: ) from China

XUE Huai-jun, BU Wen-jun (Institute of Entomology, College of Life Sciences, Nankai University, Tianjin 300071, China)

Abstract: Immature stages of 3 species of the tribe Ozophorini from China are described for the first time, they are Bryanellocoris orientalis Hidaka (3rd~5th instars), Primierus longispinus Zheng (4th~5th instars) and Vertomannus brevicollum Zheng (4th~5th instars). A brief study on fine structure of pale spots on head, pronotum and abdomen of 5th instar nymph of Bryanellocoris orientalis Hidaka was also given. Key words: Heteroptera; Ozophorini; immature stages; Lygaeidae; fine structure CLC number: Q969.35+4.4 Document code: A Article ID: 1000-7482(2004)04-0264-08

25 genera and 175 species in Ozophorini Sweet are currently recognized (Péricart, 1998). Hitherto, the descriptions of the nympal stages were restricted in the following few genera: Bergidea Breddin (Berg, 1884), Ethaltomarus Scudder (Slater & Woodward, 1974), Lygofuscanellus Scudder (Champion, 1913), Migdilybs Hesse (Hesse, 1925), Vertomannus Distant (Poppius & Bergroth, 1921), and the large new world genus Ozophora Uhler (Froeschner, 1944; Hussey, 1954; Sweet & Slater, 1961; Slater & Baranowski, 1978, 1979, 1983; Slater & O’Donnell, 1979; Slater & Hassey, 1981; Slater, 1987a, b). The nymphs we treated in present paper belong to three genera: Bryanellocoris Slater, Primierus Distant and Vertomannus Distant. The adult of them are mainly by Chen & Ashlock (1987), Slater & Zheng (1985) and Zheng & Zou (1981). So far, no nymphal stages of Bryanellocoris and Primierus species have been described and only one unidentified species of nymphal Vertomannus has been described by Poppius & Bergroth (1921). 1. On the diagnosis of nymphal Ozophorini The nymphs of Lygaeidae have proven to be very important to the taxonomic and phylog- enetic study of the family (Sweet & Slater, 1961; Sweet, 1967; Slater & Woodward, 1982;

Received date: 2004-02-16 Foundation item: The project was supported by "Education Grant" of National Natural Sciences Foundation of China (No. 108) Corresponding author, E-mail: [email protected] 264

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Schuh & Slater, 1995, etc.). Sweet (1967), Schuh & Slater (1995) and Péricart (1998) all gave a diagnosis of nymphal Ozophorini. Partly based on our own work, we integrated their contributions and gave a diagnostic description of nymphal Ozophorini as follows: Epicranial sulcus distinct, Y-shaped (epicranial stem very short sometimes); pronotum and wing pads with explanate lateral flange; distinct pronotal collar present; dorsal abdominal scent gland openings present between terga 3~4, 4~5 and 5~6, the sclerites surrounding the openings narrow; Y-suture strong developed; all spiracles ventral; suture between abdominal sterna 4 and 5 curving forward laterally and not attaining lateral margin of abdomen; abdominal trichobothria on sternum 5 closer to posterior margin of sternum 5 than to spiracle. 2. Description of nymphs All of the materials used in present study were collected from the field along with the nearly adult specimens in the same environment usually on the same plant. The specimens were preserved in 75% alcohol and deposited in the Collection of , Institute of Entomology, Nankai University. 2.1 Bryanellocoris orientalis Hidaka, 1962 Fifth instar nymph (Fig. 1) Body broadly elliptical, widest across 3rd abdominal segment. Background coloration brown with some black patches. Pale yellow spots present on dorsal side of body and ventral side of abdomen. Head shorter than wide across eyes, brown with irregular dark brown patches, covered with sparse erect and semi-erect small hairs, declivent obviously. Eyes reddish brown, not touching posterior margin of head. Epicranial sulcus Y-shaped with a short stem, yellowish brown. Antennal segments 1 reddish brown, comparatively stubbed; segments 2 and 3 yellow, slender; segment 4 reddish brown, narrowly fusiform. Labium dark brown with the distal part of segment 1 and segment 2 pale yellow, comparatively short, attaining base of midleg. Pronotum trapezoidal, declivent slightly. The anterior and posterior margin of pronotum almost straight. Pronotum brown with calli and area near posterior margin black. Explanate lateral pronotal flange yellow with black stripes. Anterior collar-like area of pronotum broad and distinct, with alternate longitudinal black and yellow short stripes. Scutellum mostly darker, irrorate with some pale yellow spots. Fore wing pads brown, with lateral margin explanate, attaining central area of tergum 3. Tergal suture pale, longitudinally running through the thorax. Legs pale yellow with terminal parts of femora, tibiae and 2nd tarsi brownish black. Two sharp and thin spines under terminal part of fore femora. Abdomen evenly elliptical, brown with pale yellow spots. Dorsal abdominal scent gland openings present between terga 3~4, 4~5 and 5~6 with dark brown narrow sclerites surrounding them. Sclerite between terga 3~4 over 1.5 times as wide as posterior two sclerites. Areas among three scent gland sclerites suffused with reddish brown. Y-suture distinct, tergal sutures between terga 3~4 broad and depressed, sutures and its neighboring region pale yellow; sutures parallel to lateral margins of terga 2 and 3 also broad and depressed. Ventral abdomen grayish brown, lateral part dotting with small pale round spots. Measurements (mm): Body length 3.40, width 1.70; head length 0.68; width across eyes 0.79; interocular space 0.45; pronotum length 0.69, width 1.28; length of antennal segments I 0.45, II 0.75, III 0.63, IV 1.02; length of labial segments I 0.37, II 0.35, III 0.30, IV 0.33; 中国科技论文在线 http://www.paper.edu.cn

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width of scent gland sclerites I 0.39, II 0.24, III 0.21. Fourth instar nymph (Fig. 2) Similar in shape and color pattern to 5th instar. Slight paler than 5th instar; epicranial sulcus almost V-shaped; eyes nearly touching posterior margin of head; wing pad attaining middle part of tergum 1; tergal sutures between terga 1~2 broad; labium relatively more elongate, reaching to base of posterior leg; spines under terminal part of fore femora thin and short. Measurements (mm): Body length 2.60, width 1.25; head length 0.45; width across eyes 0.63; interocular space 0.38; pronotum length 0.41, width 0.87; length of antennal segments I 0.30, II 0.51, III 0.45, IV 0.69; length of labial segments I 0.37, II 0.33, III 0.21, IV 0.27; width of scent gland sclerites I 0.30, II 0.18, III 0.15. 3rd instar nymph (Fig. 3) Similar in shape and color pattern to 4th instar. More paler; eyes touching posterior margin of head; spines under terminal part of fore femora hardly to seen; abdominal dorsum and metanotum yellow, with pale round spots; fore wing pads nearly quadrate in shape. Measurements (mm): Body length 1.75, width 0.82; head length 0.34; width across eyes 0.48; interocular space 0.33; pronotum length 0.27, width 0.66; length of antennal segments I 0.16, II 0.27, III 0.27, IV 0.45; length of labial segments I 0.24, II 0.21, III 0.18, IV 0.21; width of scent gland sclerites I 0.21, II 0.14, III 0.12. Material examined: Fifth instar 1, fourth instar 2, third instar 1 adults 1 1 , Dongzhong forestry centre (alt. 680m), Fangchenggang City, Guangxi Zhuangzu Autonomous Region, 08- -2002, leg by XUE Huai-jun.

Figs.1~3 Nymphs of Bryanellocoris orientalis Hidaka (dorsal view) 1. fifth instar; 2. fourth instar; 3. third instar. scale: 1.0 mm 2.2 Primierus longispinus Zheng, 1981 Fifth instar nymph (Fig. 4) Body elongate and narrow, background coloration yellowish brown. Head yellowish brown with erect or semi-erect soft hairs, relatively long, slightly declivent, lateral side of post-ocular portion straight and parallel to body axis. Eyes relatively 中国科技论文在线 http://www.paper.edu.cn

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small, far away from posterior margin of head, reddish brown. Epicranial sulcus Y-shaped (or V-shaped in some specimens), yellowish, distinct. Antennal segments 1 short, segments 1~3 yellow with segment 4 brownish black, all segments with semi-erect soft hairs. Labium comparatively narrow and long, yellow with terminal part of segment 4 brownish black, attaining base of posterior leg. Pronotum trapezoidal, yellowish brown with erect soft hairs. Anterior collar-like area of pronotum distinct. Anterior margin and posterior margin almost straight, explanate lateral pronotal flange slightly concave. Scutellum yellow with distal part comparatively darker. A thin median longitudiual pale yellow stripe running from anterior margin of pronotum to apex of scutellum. Fore wing pads with explanate lateral margin, attaining central area of tergum 3. Exposed part of hind wing pads dark brown. Legs thin and long, yellowish brown. Two spines under distal part of fore femora. Dorsal side of abdomen yellowish brown, lateral part of abdominal tergum 4 yellow. Dorsal abdominal scent gland openings present between terga 3~4, 4~5 and 5~6, areas surrounding openings narrowly and transversely sclerotized, dark brown. Y-suture distinct, tergal sutures between terga 3~4 and the sutures parallel to lateral margins of terga 2 and 3 broad and depressed. Ninth abdominal segment (undeveloped genital segment) dark brown. All abdominal spiracles on ventral side, small and pale. Abdominal sterna yellowish brown with sternum 4 and 5 pale yellow. Measurements (mm): Body length 5.10, width 1.53; head length 0.82; width across eyes 0.76; interocular space 0.48; pronotum length 0.72, width 1.25; length of antennal segments I 0.42, II 1.13, III 0.90, IV 1.10; length of labial segments I 0.64, II 0.78, III 0.75, IV 0.40; width of scent gland sclerites I 0.44, II 0.23, III 0.20.

Figs. 4~5 Nymphs of Primierus longispinus Zheng (dorsal view) 4. fifth instar; 5. fourth instar. scale: 1.0 mm

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268 昆 虫 分 类 学 报 第 26 卷第 4 期

Fourth instar nymph (Fig. 5) Similar in shape and color to 5th instar. Epicranial sulcus Y-shaped; labium relatively more elongate, reaching to posterior margin of sternum 3; abdomen more broader; tergal sutures between terga 1~2 broad; fore wing pads attaining middle part of tergum 1; pale spots much denser than that of 5th instar; spines under terminal part of fore femora small. Measurements (mm): Body length 3.65, width 1.35; head length 0.75; width across eyes 0.70; interocular space 0.46; pronotum length 0.48, width 0.94; length of antennal segments I 0.31, II 0.75, III 0.60, IV 0.75; length of labial segments I 0.54, II 0.60, III 0.58, IV 0.32; width of scent gland sclerites I 0.33, II 0.18, III 0.16. Material examined: Fifth instar 2, adults 1 1 ,Yiwanshui (alt. 1 920 m), Longling County, Yunnan Prov., 10- -2002, leg by XUE Huai-jun; Fifth instar 1, fourth instar 2, adults 18 9 ,Longxin (alt. 2 140 m), Longling County, Yunnan Prov., 14- -2002, leg by XUE Huai-jun. Both the nymphs and adults were collected in dehiscent follicles fruits of Spiraea sp. (Rosaceae). 2.3 Vertomannus brevicollum Zheng, 1981 Fifth instar nymph (Fig. 6) Body strongly ant mimetic, general coloration yellowish brown. Head yellowish brown with soft erect long hairs. The anterior part of head slightly declivent and the posterior part of head constricting to a thin “neck”. The “neck” 0.25 times as wide as head. Eyes relatively small, set far from posterior margin of head, reddish brown. Epicranial sulcus Y-shaped, distinct; stem very long, arms nearly straight. Antennal segments 1, 2 and 3 pale yellow; segment 4 yellowish brown, narrowly fusiform. Labium yellowish brown, attaining base of midleg. Pronotum trapezoidal, with explanate straight lateral margin. Anterior collar-like area of pronotum crescent-shaped, distinct. Tergal suture pale, longitudinally running through the thoracic dorsum. Fore wing pads yellowish brown, with explanate lateral margin, attaining central area of tergum 3. Legs yellowish brown with semi-erect hairs. A tooth-like spine present under terminal part of fore femora. Distal part of posterior femora dilated obviously. The abdomen largely yellowish brown with the middle part of terga 6~8 comparatively pale, suffused with reddish. Dorsal abdominal scent gland openings present between terga 3~4, 4~5, and 5~6. Brown sclerites surrounding scent gland openings comparatively broad. Y-suture distinct, tergal sutures between terga 3~4 broad and depressed, sutures and its neighboring region pale yellow; sutures of terga 2 and 3 parallel to lateral margins also broad and depressed. Abdominal sterna yellowish brown with sternum 4 pale yellow. Measurements (mm): Body length 4.30, width 1.32; head length 1.12; width across eyes 1.00; interocular space 0.70; pronotum length 0.63, width 1.05; length of antennal segments I 0.42, II 1.20, III 1.00, IV 1.13; length of labial segments I 0.52, II 0.48, III 0.42, IV 0.36; width of scent gland sclerites I 0.37, II 0.24, III 24, length of scent gland sclerites I 0.12, II 0.09, III 0.14. Fourth instar nymph (Fig. 7) Similar in shape and color to 5th instar. Neck shorter and broader, 0.43 times as wide as head, the length of head equal to width; the pronotum comparatively narrow, narrower than 中国科技论文在线 http://www.paper.edu.cn

2004 年 9 月 薛怀君等 中国直腹长蝽族三种若虫记述 269

width of head; lateral margin of pronotum arc-like slightly; wing pads extending to middle part of abdominal tergum 1; tergal sutures between terga 1-2 broad; tergal sutures between terga 3-4 and its neighboring region suffused with reddish.

Figs. 6~7 Nymphs of Vertomannus brevicollum Zheng (dorsal view) 6. fifth instar; 7. fourth instar. scale: 1.0 mm

Measurements (mm): Body length 3.42, width 1.13; head length 0.87; width across eyes 0.87; interocular space 0.66; pronotum length 0.46, width 0.81; length of antennal segments I 0.36, II 0.87, III 0.75, IV 0.86; length of labial segments I 0.39, II 0.38, III 0.30, IV 0.27; width of scent gland sclerites I 0.30, II 0.21, III 21, length of scent gland sclerites I 0.09, II 0.06, III 0.09. Material examined: Fifth instar 1, fourth instar 3, holotype and 14 paratypes, Mt. Emei, Sichuan Prov., 25- ~27- -1957, leg by ZHENG Le-yi and CHENG Han-hua. 3. Fine structure of “pale spots” Numerous small round pale spots can be found on dorsal side of body and ventral side of abdomen in nymphs of Bryanellocoris orientalis and dorsal side of abdomen of Primierus longispinus under optical microscope. The similar situation was found in some species of Ozophora (Slater & Baranowski, 1978, 1983; Slater, 1987a, b). The spots were not found in the adults of the two species we observed. We checked the fine structure of “spots” on 5th instar nymph of Bryanellocoris orientalis Hidaka by SEM (scanning electron microscope) in present study. The SEM figures show that: among the diversified minute body hairs, the round spot on head and pronotum is composed of some distally swollen tiny hairs surrounding a thick and long hair (Figs. 8~11). The distally swollen hair may be a kind of glandular hair (glandular hairs were never been reported in nymphal Rhyparochrominae hitherto). But the round “pale 中国科技论文在线 http://www.paper.edu.cn

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spot” on abdomen is composed of comparatively sparse (compare with the surrounding minute hairs, which are denser and shorter) needle-like tiny hairs, also with a thick and long hair in the center (Figs. 12~13). The contrast between minute hairs forming “pale spots” and the minute hairs forming the surrounding background areas makes the “pale spot” recognizable under optical microscope.

Figs. 8~13 The fine structure of round “pale spot” of Bryanellocoris orientalis Hidaka 8~10: head (dorsal view); 11: pronotum; 12~13: abdomen (dorsal view)

Acknowledgements: We are very grateful to Professor ZHENG Le-yi (Nankai University) for his helpful advice and critical revising of the manuscript. We express thanks to Ms. PAN Gui-ling (Nankai University) for her help in producing the SEM micrographs.

REFERENCES [1] 郑乐怡, 邹环光. 长蝽科, 中国蝽类昆虫鉴定手册(第二册)(萧采瑜等主编) [M]. 北京: 科学出版社, 1981, 1-250. [2] Berg C. Addenda et emendanda ad Argentina[M]. Bonariae: Pauli E. Coni, 1884, 213pp. [3] Champion G C. Coleoptera, etc. in Bromeliads[J]. Ent. mon. Mag., 1913, 49: 2-7. [4] Chen J K, Ashlock P D. A revision of the genus Bryanellocoris with thirty-five new species from the southwest Pacific (Hemiptera-Heteroptera: Lygaeidae)[J]. U. Kansas Sci. Bull., 1987, 53(8): 393-435. 中国科技论文在线 http://www.paper.edu.cn

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[5] Froeschner R C. Contribution to a synopsis of the Hemiptera of Missouri, Pt.III[J]. Amer. Midl. Nat., 1944, 31(3): 638-683. [6] Hesse A. List of the Heteropterous & Homopterous Himiptera of Southwest Africa[J]. Ann. S. Mus., 1925, 23: 1-178. [7] Hussey R F. Some records of Hemiptera new to Florida[J]. Quart. J. Acad. Sci., 1954, 18: 120-122. [8] Péricart J. Hémiptères Lygaeidae Euro-Méditerranéens. Faune de France 84 B[M]. FFSSN, 1998, 453pp. [9] Poppius B, Bergroth E. Beitrage zur Kenntnis der Myrmecoiden Heteropteren[J]. Ann. Hist.-nat. Mus. Hung., 1921, 18: 31-88. [10] Putshkov V G. Larvae of Hemiptera-Heteroptera. I. Lygaeidae[J]. Rev. Ent. URSS, 1958, 37(2): 392-413. [11] Schuh R T, Slater J A. True Bugs of the world (Hemiptera-Heteroptera)[M]. New York: Cornell Univ. Press, 1995, 336pp. [12] Slater J A. The systematic status of Ozophora quinquemaculata Barber and related taxa (Hemiptera: Lygaeidae)[J]. Florida Ent., 1987a, 70 (1): 134-162. [13] Slater J A. A revision of the Ozophora umbrosa complex in the West Indies (Hemiptera: Lygaeidae)[J]. J. New York Entomol. Soc., 1987b, 95(3): 414-427. [14] Slater J A, Baranowski R M. A new species of Bromeliad Lygaeid from Jamaica[J]. Florida Ent., 1978, 61 (2): 83-88. [15] Slater J A, Baranowski R M. New species of Ozophora from the Lesser Antilles with notes on the biology and immature stages (Hemiptera: Lygaeidae)[J]. Florida Ent., 1979, 62 (3): 244-259. [16] Slater J A, Baranowski R M. The genus Ozophora in Florida[J]. Florida Ent., 1983, 66 (4): 134-162. [17] Slater J A, Hassey M. The distribution and systematics of Ozophora atropicta Barber, with the description of a new species from the Neotropics[J]. Florida Ent., 1981, 64 (2): 246-259. [18] Slater J A, O’Donnell J E. An analysis of the Ozophora laticephala-complex with the description of eight new species (Hemiptera: Lygaeidae)[J]. J. Kansas Entomol. Soc., 1979, 52(2): 154-179. [19] Slater J A, Woodward T E. A new genus and four new species of Rhyparochrominae (Hemiptera: Lygaeidae) from Australia[J]. J. Aust. Entomol. Soc., 1974, 13: 305-316. [20] Slater J A, Woodward T E. Lilliputocorini, a new tribe with six new species of Lilliputocoris, and a cladistic analysis of the Rhyparochrominae (Hemiptera, Lygaeidae)[J]. Amer. Mus. Novitates, 1982, 2754: 1-23. [21] Slater J A, Zheng L Y. Revision of the lygaeid genera Porta and Primierus (Hemiptera: Heteroptera), with the description of a new genus of Ozophorini from Papua New Guinea (Hemiptera)[J]. Systematic Entomol., 1985, 10: 453-469. [22] Sweet M H. The tribal classification of the Rhyparochrominae (Heteroptera: Lygaeidae)[J]. Ann. Entomol. Soc. Amer., 1967, 60: 208-226. [23] Sweet M H, Slater J A. A genereic key to the nymphs of North American Lygaeidae (Hemiptera: Heteroptera)[J]. Ann.Entomol. Soc. Amer., 1961, 54, 333-340.

中国直腹长蝽族三种若虫记述 半翅目 长蝽科 地长蝽亚科

薛怀君 卜文俊 南开大学生命科学学院昆虫学研究所 天津 300071

本文对直腹长蝽族(半翅目 长蝽科 地长蝽亚科)的 3 个种的若虫进行了首次描述 即东方完缝长蝽 Bryanellocoris orientalis Hidaka 长刺棘胸长蝽 Primierus longispinus Zheng 和短头细颈长蝽 Vertomannus brevicollum Zheng 其中前二者为该属若虫的首次记 述 本文还通过扫描电镜观察对东方完缝长蝽 Bryanellocoris orientalis Hidaka 身体背面 分布的浅色圆点的细微结构进行了揭示

关键词 半翅目 直腹族 若虫 长蝽科 细微结构