Protaphelinus, a newly recorded genus of Aphelinidae (Hymenoptera: Chalcidoidea) from China

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1 Entomotaxonomia (2014) 36(3): ISSN Protaphelinus, a newly recorded genus of Aphelinidae (Hymenoptera: Chalcidoidea) from China WANG Zhuhong 1, 2, HUANG Jian 1, 21, LI Chengde 3 1. Key Laboratory of Integrated Pest Management for Fujian-Taiwan Crops, Ministry of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, Fujian , China 2. Fujian Provincial Key Laboratory of Insect Ecology; Fujian Agriculture and Forestry University, Fuzhou, Fujian , China 3. School of Forestry, Northeast Forestry University, Harbin, Heilongjiang , China Abstract: The genus Protaphelinus Mackauer (Hymenoptera: Aphelinidae) is recorded for the first time from China and Protaphelinus nikolskajae (Yasnosh) is redescribed in detail and illustrated by macrophotography. This is the parasitoid specifically associated with the gall-making aphid, Pemphigus borealis Tullgren (Aphidoidea: Pemphyidae) found on the poplar tree (Populus sp.) in Wudalianchi, Heilongjiang Province. Key words: Parasitica; parasitoid; taxonomy CLC number: Q Document code: A Article ID: (2014) 蚜小蜂科一中国新纪录属 原蚜小蜂属记述 ( 膜翅目 : 小蜂总科 ) 1, 王竹红 2 1,, 黄建 21, 李成德 3 1. 福建农林大学农业部闽台作物有害生物综合治理重点实验室, 福建福州 ;2. 福建农林大学福建省昆虫生态重点 实验室, 福建福州 ;3. 东北林业大学林学院, 黑龙江哈尔滨 摘要 : 记述蚜小蜂科 1 中国新纪录属 原蚜小蜂属 Protaphelinus Mackauer, 对该属模式种尼氏原蚜 小蜂 Protaphelinus nikolskajae (Yasnosh) 作了重新描述, 附有雌 雄形态特征及其蚜虫寄主照片 本研 究的尼氏原蚜小蜂采自黑龙江五大连池, 寄生火山杨 Populus sp. 上的远东枝瘿绵蚜 Pemphigus borealis Tullgren 目前该属世界仅记载 1 种, 是造瘿蚜虫瘿绵蚜科 Pemphyidae 瘿绵蚜属 Pemphigus 的专性寄生蜂 关键词 : 寄生部 ; 寄生蜂 ; 分类 Introduction The genus Protaphelinus Mackauer (Hymenoptera: Aphelinidae) was erected by Mackauer in 1972 with the type-species Protaphelinus nikolskajae (Yasnosh), which was treated as a new combination for Aphelinus nikolskajae Yasnosh originally in the genus Aphelinus Dalman (Mackauer 1972). Within the aphis-attacking parasitoids in the family Received 3 March Published 25 September Corresponding author, jhuang1234@126.com

2 WANG et al. Protaphelinus from China 217 Aphelinidae, species of Protaphelinus are the specific parasitoids of gall-making aphids of the genus Pemphigus (Aphidoidea: Pemphyidae) on poplar trees (Mackauer 1972), and the other aphis-attacking aphelinids mainly include all species of Aphelinus and a few Encarsia (Huang 1994; Huang & Polaszek 1998; Hayat 1998). The second species in the genus, Protaphelinus dargahae, was described by Rishi & Lone (1984). It is parasitic on the gall-making aphid, Pemphigus bursarius Linn. infesting Populus nigra var. italica Muench. in Kashmir of India. But Hayat (1998) synonymized this species with Protaphelinus nikolskajae and pointed out the description of Pr. dargahae does not agree with the figures given by these authors. The characters differentiating Pr. dargahae from Pr. nikolskajae given by Rishi & Lone appear to be either observational errors or are not supported by correct illustrations, and the figure of the whole insect given is apparently that of a male, not female (Hayat 1998). To date, the genus Protaphelinus contains only one species worldwide (Noyes 2014). In this work the genus Protaphelinus is recorded for the first time from China and Protaphelinus nikolskajae is redescribed and illustrated in detail. It was reared from the gall-making aphid, Pemphigus borealis Tullgren, on the poplar tree Populus sp. in Heilongjiang Province. Material and methods The specimens studied here were obtained during a survey for parasitoids of aphids at Wudalianchi, Heilongjiang Province. Field-collected galls caused by the gall-making aphid Pemphigus borealis from poplar trees were kept in glass tubes until emergence of the adult parasitoids. These were preserved in 75% ethanol. The body colour was described and photographed from ethanol-preserved specimens before clearing and slide-mounting. The specimens were slide-mounted for species identification following the method outlined by Noyes (1982). The specimens in ethanol were photographed with a MicroPublisher 5.0 RTV camera attached to a Zeiss Stemi 2000-C stereo zoom trinocular microscope with Auto-Montage software and Sony DSC-T900 camera. Slide-mounted specimens were photographed using the same camera and software but attached to a Zeiss Axioskop 40 phase contrast trinocular microscope. Body length was measured from ethanol-preserved specimens before being slide-mounted, and all other measurements were taken from slide-mounted specimens. The specimens examined in this study are deposited in the College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China (FAFU). Terminology follows Hayat (1998), and the following abbreviations are used: C1, C2, etc. antennal clava segments 1, 2, etc.; F1, F2, etc. antennal funicle segments 1, 2, etc.; T1, T2, etc. metasomal tergites 1, 2, etc; OAL distance between a posterior ocellus and the anterior ocellus; OOL distance between a posterior ocellus and eye margin; POL distance between the two posterior ocelli. Taxonomy Genus Protaphelinus Mackauer, 1972, new record to China Protaphelinus Mackauer, 1972: Type-species: Aphelinus nikolskajae Yasnosh, by original

3 218 Entomotaxonomia (2014) 36(3): designation. Female. Antenna 6-segmented, antennal formula Frontovertex broader than dorsal eye length; temples well-developed. Mid-lobe of mesoscutum with reduced number of setae; anterior pair of mesoscutellar setae in line with posterior angles of axillae. Fore wing with costal cell about as long as marginal vein; stigmal vein short, linea calva distinct. Tarsal formula 5-5-5, tarsal claws unequal in lengths. Metasoma with hypopygium reaching apex of metasoma and apically with long setae; ovipositor with the third valvula short, shorter than mid basitarsus. Male. Body smaller and colour darker than female, the morphological characters similar to female, except male genitalia. Remarks. Protaphelinus is close to Aphelinus Dalman 1820, but differs from the latter by the following characters: frontovertex broader than eye length; pronotum with a single long bristle at each posterolateral corner; mid-lobe of mesoscutum with reduced number (at most 16) of setae; legs with tarsal claws strongly unequal in lengths, the shorter about 0.5 of the longer one. Aphelinus species are characterized by a relatively less broad frontovertex; pronotum with two long bristles at each posterolateral corner; mid-lobe of mesoscutum usually densely setose (more than 26 setae); legs with tarsal claws at most subequal, if unequal then the smaller one at least 0.66 of the longer one. Distribution. Oriental; Nearctic; Palaearctic. Host. Specific parasitoids of gall-making aphids of the genus Pemphigus Hartig (Aphidoidea: Pemphyidae) on poplar trees, Populus spp. Protaphelinus nikolskajae (Yasnosh, 1963) (Figs. 1 18) Aphelinus nikolskajae Yasnosh, 1963: 181. Female, male. Georgia, Tbilisi (ZIASP). Protaphelinus nikolskajae (Yasnosh): Mackauer, 1972: New combination for Aphelinus nikolskajae Yasnosh. Protaphelinus dargahae Rishi & Zutshi, 1979: 4. [abstract], Synonymy by Hayat, 1998: 50. Protaphelinus dargahae Rishi & Lone, 1985: 132. Female, male. India, Srinagar (authors' coll.?), Synonymy by Hayat, 1998: 50. Female (Figs. 1 13). Body length about mm. Colour. Head brownish yellow, frontovertex with pale brown patches, occiput with a transverse brown band on each side of foramen, eyes pale grey and ocelli brownish red, tips of mandibles dark brown. Mesosoma brown to dark brown, except side-lobe of mesoscutum yellow to dark yellow, anterior area of mid-lobe of mesoscutum slightly pale. Metasoma pale brown, with dark brown bands on each tergite, apex of last tergite white; ovipositor brownish yellow, third valvula pale brown. Antenna brownish yellow, except scape and clava apically pale brown. Wings hyaline. Legs brownish yellow, apex of tarsi dark. Head. Frontovertex broad, about 0.5 of head width; eyes finely setose; ocellar triangle with the obtuse apical angle, posterior ocelli slightly more than one ocellus diameter to eye margin, and about two diameters to occipital margin, POL about 2.9 as long as OOL and 2.2 of OAL; mandible with two teeth and a truncation. Antenna with scape about 5.0 as long as wide; pedicel large, about 2.0 as long as wide, distinctly longer than combined length of F1 plus F1, 0.48 as long as clava; F1 and F2 small, 0.62 and 0.57 as long as wide respectively; F3 slightly longer and wider than F1 and F2 respectively, 0.89 as long as wide; a singe segment clava about 3.0 as long as wide, with 7 9 longitudinal sensilla.

4 WANG et al. Protaphelinus from China 219 Figures 1 8. Protaphelinus nikolskajae,. 1. Body, dorsal view; 2. Body, ventral view; 3. Antenna; 4. Fore wing; 5. Head, frontal view; 6. Mesosoma; 7. Ovipositor before slide-mounting; 8. Ovipositor. Mesosoma. Pronotum divided centrally; mid-lobe of mesoscutum with setae; each side-lobe of mesoscutum with 4 setae; each axilla with 1 setae; mesoscutellum large, 0.83 as long as mid-lobe of mesoscutum, with 2 pairs of setae, placoid sensilla closer to fore pair of setae than to hind pair; mesopostphragma, measured from apex of mesoscutellum, 2.08 as long as mesoscutellum. Fore wing broad, 2.18 as long as maximum width of wing disc, marginal fringe short; wing disc densely setose, linea calva proximally bordered by about 20

5 220 Entomotaxonomia (2014) 36(3): setae in 1 2 lines which are longer than discal setae; submarginal vein with 8 10 setae; marginal vein with setae along anterior margin; postmarginal vein absent; stigmal vein short, with a small neck. Figures Male and aphid host of Protaphelinus nikolskajae P. nikolskajae, : 9. body, dorsal view; 10. body, ventral view; 11. male genitalia before slide-mounting; 12. male genitalia; 13. antenna; 14. fore wing; Aphid host: 15. galls made by Pemphigus borealis on the poplar tree Populus sp.; 16. aphid host mummies in the gall; 17. aphid host mummies with emergence hole of Protaphelinus nikolskajae; 18. adult Pemphigus borealis.

6 WANG et al. Protaphelinus from China 221 Metasoma. Metasoma broad and long, about 1.76 as long as mesosoma; hypopygium densely setose in apical half; ovipositor distinctly short, basally located at T5, not projecting beyond apex of metasoma, about 0.75 as long as mid tibia, third valvula 0.40 as long as second valvifer. Male (Figs. 9 14). Body length about mm. Head pale yellow, eyes pale grey and ocelli brownish red, tips of mandibles dark brown. Mesosoma with pronotum, mid-lobe of mesoscutum and axillae pale yellow to pale brown, side-lobe of mesoscutum pale yellow; mesoscutellum, metanotum and propodeum dark brown; sterna of mesosoma pale yellow; metasoma black brown, or with dark brown bands on each brown tergite; male genitalia with aedeagus white, digiti brown with apex dark brown. Antenna pale yellow, except pedicel mostly and clava apically pale brown. Wings hyaline. Legs pale yellow, last tarsi pale brown. Antennal scape with a groove in distal 0.66 bearing sensilla. Mid-lobe of mesoscutum with about 11 setae. Male genitalia about 1.56 as long as mid tibia, parameres short, and each digitus with two denticles. Host (Figs ). Pemphigus borealis Tullgren (Aphidoidea: Pemphyidae) on the poplar tree, Populus sp. The other aphid host ranges are recorded as follows: Pemphigus bursarius Linnaeus, Georgia (Achvlediani, 1963); Pemphigus lichtensteini Tullgren, on Populus sp., France (Ferrière, 1965), Georgia (Yasnosh, 1963); Pemphigus spirothecae Passerini, on Populus nigra L. var. italica Muench., Georgia (Yasnosh, 1963); Pemphigus sp. (spirothecae group), on Populus nigra L., West Pakistan (Mackauer, 1972); Pemphigus sp., India (Hayat, 1972). Distribution. China (Heilongjiang); Pakistan; India; Georgia; France; Canada. Specimens examined. 30 8, China, Heilongjiang, Wudalianchi, 13-VII-2013, coll. Zhuhong WANG, Jian HUANG & Yaling ZHANG, ex. Pemphigus borealis Tullgren on poplar trees. Discussion Aphelinus nikolskajae was originally described as new species by Yasnosh (1963) and later became a new combination as the type-species Protaphelinus nikolskajae (Yasnosh) of the genus Protaphelinus by Mackauer (1972). They are specialized parasitoids of the gall-making aphid Pemphigus spirothecae Passerini on the pyramidal poplar tree in Georgia. Aphelinus nikolskajae was recorded from China by Liao et al. (1987) and is parasitic on the aphid Myzus sp. (Aphidoidea: Aphididea). However, Liao et al. (1987) made a misidentification for the species and the brief description with an incorrect figure and the aphid host association given by Liao et al. do not completely agree with Aphelinus nikolskajae. Discrepancies include the advanced axillae being yellow and the mesoscutum being densely setose in female, the mesoscutum with yellow patches and the metasoma dark brown medially and yellow basally and apically in male, and not having the gall-making aphid host, Myzus sp. (Liao et al. 1987). In Aphelinus nikolskajae, the axillae are dark brown and not elongated; the mid-lobe of mesoscutum has a reduced number (12 16) of setae in the female; the mesoscutum with pronotum, mid-lobe of mesoscutum and axillae are mostly pale brown; mesoscutellum, metanotum and propodeum are dark brown; the metasoma is dark brown, or with dark brown bands on each brown tergite in male. Both the morphological characters and

7 222 Entomotaxonomia (2014) 36(3): the host association are essential in identification of aphid-attaching aphelinid parasitoids. Acknowledgements We are grateful to Ms. Yaling ZHANG (Tibet Academy of Agriculture and Animal Husbandry Sciences, Lhasa, China) for help with specimen collection, and to Prof. Gexia QIAO (Institute of Zoology, Chinese Academy of Sciences, Beijing, China) for identification of the gall-making aphid. This project was funded by the National Natural Science Foundation of China ( ), the Natural Science Foundation of Fujian Province (2012J01084) and the Commonwealth Industry Scientific Research Fund, China ( ). References Achvlediani MN Material zum studium der blattlausparasiten des ostlichen gruziniens. Soobshcheniga Akademii Nauk Gruz SSR, 30: Ferrière C Faune de l Europe et du Bassin Méditerranéen. 1. Hymenoptera Aphelinidae d Europe et du Bassin Méditerranéen. Masson et Cie, Paris, 209 pp. Hayat M The species of Aphelinus Dalman, 1820 (Hymenoptera: Aphelinidae) from India. Entomophaga, 17: Hayat M Aphelinidae of India (Hymenoptera: Chalcidoidea): a taxonomic revision. Memoirs on Entomology, International. Associated Publishers, Gainesville, Florida, 416 pp. Huang J Systematic studies on Aphelinidae of China (Hymenoptera: Chalcidoidea). Contributions of the Biological Control Research Institute, Fujian Agricultural University Special Publication No. 5. Chongqing Publishing House, Chongqing, China, 348 pp. Huang J & Polaszek A A revision of the Chinese species of Encarsia Förster (Hymenoptera: Aphelinidae): parasitoids of whiteflies, scale insects and aphids (Hemiptera: Aleyrodidae, Diaspididae, Aphidoidea). Journal of Natural History, 32: Liao DX, Li XL, Pang XF & Chen TL Hymenoptera: Chalcidoidea (1). Economic Insect Fauna of China, No. 34. Science Press, Beijing, China, 241 pp. Mackauer M The aphid-attacking genera of Aphelinidae (Hymenoptera), including the description of a new genus. Canadian Entomologist, 104(11): Noyes J Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). Journal of Natural History, 16: Noyes J Universal Chalcidoidea Database. World Wide Web electronic publication. Available from: (Accessed February 2014). Rishi ND & Zutshi V Record of a new species of the genus Protaphelinus (Aphelinidae Chalcidoidea). Proceeding of Indian Science Congress 66th, part III. p. 4 (Abstract only). Rishi ND & Lone MA Description of a new species of Protaphelinus Mackauer (Hymenoptera: Aphelinidae) parasitic on gall forming aphid, Pemphigus bursarius Linn. infesting Populus nigra var. italica Muench. in Kashmir (India). Journal of Entomological Research (New Delhi), 8(2): Yasnosh VA New species of the genus Aphelinus Dalm. (Hymenoptera, Chalcidoidea) in the fauna of the USSR. Entomologicheskoe Obozrenie, 42(1): 181.