First Recorded Parasitoid from China of <I>Agrilus planipennis</I>: A New Species of <I>Spathius</I> (Hymenoptera: Braconidae: Doryctinae)

Agrilus planipennis Fairmaire (=A. marcopoli Obenberger) (Coleoptera: Buprestidae) attacks ash trees (Fraxinus spp.) (Oleaceae) in its native range of northern China (including Shandong, Tianjin, Inner Mongolia; Liaoning, Jilin, and Heilongjiang provinces) as well as in Mongolia, the Korean Peninsula, Japan, and the Russian far east. In northern China, it has been a serious pest of imported North American ash [i.e., Fraxinus americana L., Fraxinus velutina Torr., and Fraxinus pennsylvanica varieties pennsylvanica Marsh and lanceolata (Borkh.) Sarg.-Budd and Best] used in plantations and as ornamentals. It also has been reported attacking native ash [i.e., Fraxinus mandshurica Rupr., and Fraxinus chinensis varieties chinensis Roxb. and rhynchophylla (Hance) Hemsl.], most often when associated with the exotic ash species also being attacked. The first major A. planipennis outbreaks in China during the early 1960s were on F. americana, and they produced great losses for landscaping and timber industries (Yu 1992). A. planipennis was first collected in southeastern Michigan in May 2002 from ash trees (Haack et al. 2002). It was soon discovered in Windsor, Ontario, Canada, and then Ohio, Maryland (nursery stock from Michigan), and Indiana (Marchant 2004, Rauscher and Mastro 2004). Within southeastern Michigan, it has been reared from all species of native ash and is thought to have been present for at least 5 yr before discovery (McCullough and Roberts 2002). It was predicted that A. planipennis could spread throughout the range of ash in North America, causing substantial economic and environmental damage (Haack et al. 2002, Mastro and Reardon 2004). In its native range, A. planipennis larvae were reported from species of Juglans, Ulmus, and Pterocarya. However, representatives of these genera in North America have not been reported to serve as hosts. The concealed A. planipennis larvae are difficult to detect until the foliage wilts, dead twigs become noticeable, or adult emergence holes are noted. This delay in detection challenges control efforts with conventional pesticides. The clear threat to ash in North America and China spurred the formation of a Sino-American program to study the potential for biocontrol of A. planipennis. During exploration for natural enemies, an undescribed species of Spathius Nees (Hymenoptera: Braconidae) was discovered attacking A. planipennis larvae in China and preliminary laboratory and field studies of its biology were conducted there. The description of this new Spathius species, biological observations, and a discussion of its biocontrol potential are presented. Typical of most Doryctinae, Spathius species attack wood-boring beetle larvae. Worldwide in distribution with >300 species described, Spathius is particularly species rich in the Old World tropics (Shenefelt and Marsh 1976) and is distinguished from other winged Doryctinae by 1) forewings with three submarginal cells; 2) first subdiscal cell of forewing closed; and 3) first metasomal segment petiolate, widening apically, lacking basal wing-like projections, and inserted on propodeum near coxal bases (Marsh 1997). Nixon (1943) studied the Old World Spathius species; Shenefelt and Marsh (1976) published a catalog of the world species of Spathius.Marsh (1997) produced a key for identification of the genera of New World Doryctinae, including Spathius.Matthews (1970) revised the species in America North of Mexico. The Japanese species of the genus were studied by Watanabe (1937). Tobias (1986) reviewed the genus in the European part of Russia and Belokobylskij (1998) described Spathius species from Russian Siberia. The Chinese Spathius species were studied by the late Prof. Dr. Hsiu-Fu Chao, Fujian Agricultural University, Fuzhou. He listed 40 species for China, of which 34 new species (and one new subspecies) were described by him (Chao 1957, 1977, 1978,,; Chao and Chen 1965). Surveys during 2003 and 2004 for stressed ash trees were conducted in Tianjin Province, mainly of F. velutina, and in Liaoning, Jilin, and Heilongjiang provinces, mainly of F. mandchurica. Surveys were performed every other day in 2003 from mid-August to early November and in 2004 from early April to the end of August. Surveys during other months were performed monthly. Trunk bark of stressed trees (in Tianjin, mainly F. velutina; and in Liaoning, Jilin, and Heilongjiang, mainly F. mandchurica) was peeled back to search for A. planipennis larvae and their associated parasitoids. A. planipennis larvae were collected and possible parasitoid eggs, larvae, or pupae in cocoons were placed in vials (12 mm in diameter by 75 mm in height). Each vial sample contained a single brood of parasitoids and their A. planipennis host larva. These vials were brought into the laboratory, and their contents were transferred into new vials containing a piece of filter paper dipped in distilled water for moisture. The vials were then tightly plugged with sterilized cotton and maintained at 20–23°C in a rearing room. Distilled water was added every 3 d to the filter paper. Parasitoid eggs, larvae, and pupae were successfully reared to adults. After the parasitoids emerged, they were killed and point mounted. Specimens were examined with an Olympus SZH 10 stereomicroscope. Scanning electron microscopy (SEM) photographs were taken with a ZOEL 550LV scanning electron microscope. Terminology follows van Achterberg (1993). Abbreviations applied to ocelli are OD, longest diameter of ocellus; OOL, shortest distance between a posterior ocellus and compound eye; and POL, shortest distance between hind ocelli. The types are deposited in the Insect Museum, Chinese Academy of Forestry, Beijing, the Nationaal Natuurhistorisch Museum, Leiden, The Netherlands; the U.S. National Museum of Natural History, Washington, DC; and West Virginia University, Morgantown, WV. Authorship of the new species is attributed solely to Zhong-Qi Yang. As a check on the conspecificity of Spathius specimens, we sequenced portions of three genes (16S rRNA, cytochrome oxidase I [COI] and 28S rRNA) from seven specimens arising from three regions: China (Dagang, Tianjin – samples Spathius-017 and Spathius-020), Japan (Yasu-cho, Shiga – samples Spathius-003, Spathius-007, and Spathius-008), and Russia (two specimens identified as S. generosus by Belokobylskij – Spathius-050 and Spathius-051). Specimens were first photographed using color digital photography (JVC GC-QX5HD mounted on a Leica MZ12.5 stereomicroscope) and environmental SEM (Philips XL30 ESEM-FEG); these photographs are available (along with those of other Spathius specimens) on a Web site (Whitfield 2004). Molecular methodology was as described in Whitfield et al. (2002). Aligned sequences for 16S resulted in a 481-bp data set, for COI 709 bp, and for 28S 691 bp (two of the specimens, Spathius-003 and Spathius-050, failed to amplify for 28S, so data for this gene are missing), resulting in a total of 1881 bp. Sequences are deposited in GenBank under accession numbers AY920284–AY920302. Data were analyzed in two ways: 1) maximum parsimony by using PAUP* 4.0 (Swofford 2001), by using a branch-and-bound search and 2) Bayesian analysis by using MrBayes3 (Ronquist and Huelsenbeck 2003), with models selected by MrModeltest 2.0 (Nylander 2002)—F81 for 16S, HKY for 28S, GTR + G for COI—and allowing four chains to sample for 2 million generations (100,000 as burnin). Fig. 1–7. S. agrili n. sp. (♀). (1) Antennal segments 1–5. (2) Head dorsal view. (3) Head anterior view. (4) Mesosoma lateral view. (5) Mesosoma dorsal view. (6) Scutellum, metanotum, and propodeum. (7) a, Forewing. b, Hind wing Body length 3.5–4.3 mm (holotype 4.0 mm). (Figs. 1–3). Antenna (Fig. 1) 35-segmented, covered with short setae; third segment (first flagellar segment) slightly curved, length 1.6 times the fourth; third, fourth, and penultimate segments with length 6.8, 4.0, and 2.0 times their width, respectively; antenna 1.2 times length of body (without ovipositor). Maxillary palp length 1.5 times height of head. Length of eye in dorsal view 1.4 times temple (Fig. 2). Temple bulging laterally. Occiput slightly concave medially, occipital carina complete; vertex smooth, evenly convex, with few conspicuous short setae. OOL:OD:POL, 9:3:4. Frons medially transversely striate with a longitudinal smooth stripe anterior to median ocellus (Fig. 3). Face evenly convex, with delicate transverse striations on whole surface interrupted medially on upper one-third by a smooth stripe, lower one-third near clypeus superficially rugulose; conspicuous long setae distributed over face and glabrous only below antennal sockets and near malar space. Clypeus convex, finely rugose with anterior margin flanged; width of hypoclypeal depression 0.3 times width of face. Gena smooth; length of malar space 0.8 times basal width of mandible and 0.4 times height of eye in lateral view. Mandible basally with distinctly curved long setae. (Figs. 4–7). Mesosoma twice as long as high (Fig. 4). Pronotum with lateral upper one-half having about seven transverse rugae and some short longitudinal carinae in a pronotal trough; lower one-half superficially striate. Propleural flange distinct and crescentic. Epicnemial carina distinct but upper one-third near anterior margin absent. Precoxal sulcus (sternaulus) extending posteriorly for 0.55 length of mesopleuron, deep, narrow, and weakly crenulate. Epicnemial area concave as a wide, oblique trough with about eight weak transverse carinae; the carina reach the deep episternal scrobe. Mesopleuron medio-posteriorly convex, smooth with a few setae; a deep fovea present between the apices of pleural sulcus and of epicnemial area. Postpectal carina above middle coxa present and extending for some distance. Metapleuron coarsely reticulate, rugose, metapleural furrow deep, complete. Mesoscutum somewhat wider than long (58:54) in dorsal view (Fig. 5), anterior curving strongly downwards to pronotum (Fig. 4). Notauli well defined, converging posteriorly and meeting medially, anterior part (before meeting) crenulate and posterior part (after meeting) irregularly carinate; some setae lateral. Median lobe finely and densely reticulate and lateral lobes with fine reticulation. Scutellum narrows and curves downwards posteriorly (Fig. 5) with length 0.44 times mesoscutum; reticulate, rugose posteriorly; three or four setae along lateral margins. Scutellar sulcus deep with three longitudinal carinae dividing it into four large virtually smooth foveae (Fig. 6). Metanotum with its metascutellum horn-like, protruding medio-posteriorly. Propodeum 0.5 times as long as mesonotum, its median carina short, 0.25 times as long as its branches, transverse, lateral and pleural carinae distinct, transverse carinae arising from the branches of median carina at about half length of propodeum (28:50). Areola large, extending backward to reach area petiolaris at 0.8 length of propodeum, with scattered coarse rugae, dorsal area distinctly (more or less vermiculate) rugose at posterior half, and somewhat finely rugose at anterior half, other areas coarsely and irregularly rugose. (Fig. 7). Forewing length 2.8–3.3 mm (holotype 3.2 mm). r:3-SR:SR1, 6:18:33; 2-SR:3-SR:r-m, 18:18:11; 1-CU1:2-CU1, 2:27; m-cu:2-SR+M, 8:3; M+CU1 rather strongly sinuate, length of vein r 0.9 times width of pterostigma. Hind wing: 2-SC+R thickened and curved to SC+R1; marginal cell parallel sided from base to apex. (Figs. 8–10). Hind coxa smooth with a weak dentiform projection baso-ventrally. Length of femur, tibia, and basitarsus of hind leg 3.3, 12.3, and 7.5 times their width, respectively. Fore tibia with irregular row of ≈15 pegs and middle tibia (Fig. 8) with 14 pegs along length of anterior surface. Apex of fore tibia with dentiform projection (Fig. 9). Hind tibia with outer apical lobe having a row of four conspicuous peg-like spines (Fig. 10); hind tarsus as long as hind tibia; length of hind tibial spurs 0.1 and 0.2 times length of hind basitarsus; relative lengths of hind tarsal segments, proximal to distal, 58:29:19:11:17. Fig. 8–14. S. agrili n. sp. (♀). (8) Middle tibia showing the pegs on anterior edge. (9) Apex of fore tibia showing the dental projection. (10) Apex of hind tibia showing four peg-like spines on apex. (11) Mesosoma and metasoma lateral view. (12) First tergite lateral view. (13) Metasoma dorsal view. (14) Metasoma with ovipositor (Figs. 11–14). Petiolate, as long as head plus mesosoma (Fig. 11), somewhat wider than mesoscutum (34:30). First tergite arched at base in lateral view (Fig. 12), abruptly widening at apex in dorsal view (Fig. 13), its length 2.2 times its apical width, 1.8 times as long as propodeum, 1.3 times middle femur, and 0.8 times the combined length of other tergites, and 1.15 times tergites 2 + 3 (which is as long as tergites 4–7 combined); dorsal carinae extending to hind margin along each side; the dorsum at basal three-quarters coarsely rugulose and apical quarter with fine and longitudinal striae. Tergites 2 + 3 with basal four-fifths distinctly finely granulate to reticulate, the apical fifth and following tergites smooth and shiny. All tergites (except the first) having one transverse row of short setae. Ovipositor bent slightly upwards posteriorly; sheath shorter than metasoma (84:90) (Fig. 14) and 0.6 times as long as forewing. Reddish brown. Antenna with pedicel and flagellar segments 1–15, trochanters, tarsi, and first tergite yellowish or orange-brown. Palpi and ovipositor sheath brown. Metasoma dark brown except for first tergite. Basal 1/10 of middle and hind tibiae white. Wing veins brown. Forewing infuscate with transverse hyaline bands at base, middle, and apical areas (Fig. 7); vein r-m of forewing and hind wing hyaline. The body length among paratypes range from 3.5 to 4.3 mm and forewing length from 2.8 to 3.3 mm. The medial area of the vertex of some individuals has superficial or delicate transverse striae behind posterior ocelli. The hind wing 2-SC+R is thickened and curved to SC+R1 and the marginal cell parallel sided. The anterior third of tergite 4 may be delicately reticulate to granulate. The granulation to reticulation of the anterior two thirds of tergites 2 + 3 may be finely striate. Body length 3.4–3.8 mm. Forewing length 2.2–2.6 mm. Similar to female except, for the following: antenna 33–37-segmented. Hind wing with 2-SC+R thickened, length 2.7 times its width; length of vein r 0.6–0.9 times width of pterostigma. HOLOTYPE ♀, Dagang, Tianjin City, 5 December 2001, reared from a cocoon collected from galleries of A. planipennis in F. velutina Torr., Zhong-Qi Yang and Jian-Jun Pang, deposited in Insect Museum, Chinese Academy of Forestry. PARATYPES: 7♀, 3♂, same data as holotype; 23♀, 12♂, 20 June 2002, Zhong-Qi Yang; 35♀, 15♂, 12 August 2002, Xiao-Yi Wang and Zhong-Qi Yang; 26♀, 8♂, 30 May 2004, Xiao-Yi Wang, the other data as holotype; 6♂, Jingyuetan Forest Park, Changchun, Jilin Province, 18 September 2004, Zhong-Qi Yang and Xiao-Yi Wang, reared from the cocoons collected in A. planipennis gallery on ash tree F. mandshurica. Above-mentioned type specimens are deposited in the Insect Museum, Chinese Academy of Forestry; 10♀, 5♂ (4♀, 1♂, 20 June 2002; 1♀, 4♂, 25 June 2003; 5♀, 15 August 2003), deposited in the Nationaal Natuurhistorisch Museum, Leiden, The Netherlands; 15♀, 5♂, 30 May 2004 in the U.S. National Natural History Museum, Washington, DC; and 4♀, 3♂, 15 June 2004 in the West Virginia University Arthropod Collection, Morgantown, WV. Northern China: Tianjin and Jilin provinces. Specific name derived from genus name of its host, A. planipennis. The new species can be placed in the S. dissors-species group (Nixon and is to Spathius from the by It can be distinguished from the as vertex smooth behind with weak vein of forewing as long as vein basal cell of forewing with a at proximal one-third of wing at the and vein of forewing slightly curved as in the with the European species the new species is to S. on the by van Achterberg and deposited in the Collection, The new species by having distinct transverse carina on the the propodeum the third and antennal segments somewhat first tergite with the dark brown length of eye times temple in dorsal view in S. the tergite coarsely and the first cell of forewing distinctly medially than laterally. S. A. Belokobylskij the new species to S. generosus a species reared from major (Coleoptera: northern The type (in The Natural History Museum, has been examined by two of and and from S. agrili by having the first tergite for most of its the ovipositor sheath distinctly times as long as metasoma and 0.8 times as long as basal 0.4 of the hind tibia vein of hind wing strongly strongly so in S. vein r of forewing somewhat shorter times as long as vein and the basal areas of the propodeum granulate or superficially rugulose rugose in S. S. agrili is also to the of two Chinese S. and S. These two species with S. agrili have about as long as and are parallel S. agrili times as long as and metasoma as long as ovipositor or S. agrili metasoma length of propodeum between carinae weakly S. agrili propodeum coarsely forewings slightly S. agrili infuscate with three transverse hyaline the data we three most trees from the maximum parsimony tree of three maximum parsimony trees and a tree produced by Bayesian analysis were with the in Fig. resulting from the maximum parsimony and Bayesian of 16S, and 28S above branches are from the parsimony and those below are posterior from the Bayesian that tree is was used The two Chinese specimens for 16S and COI and only by bp for as the three Japanese specimens sequences for all three but the two Russian specimens are Spathius-050 near the Chinese samples by bp for each of 16S and is from the Japanese or Chinese samples by a of 25 bp, from other These strongly the of at least four species in seven one from Japan, two from and one from China that be somewhat to one of the Russian between the four species well the range of at least for COI et al. 2004). S. agrili is an the host during and its In the were to search ash tree to A. planipennis larvae in their galleries by with their on twigs and a host was the female ovipositor the bark into the A. planipennis gallery and from one to on the host, which was at some point during this After larvae they to the body surface of the host to The larvae an A. planipennis in larvae cocoons in the end of their host The parasitoids as and near the end of A. planipennis also as larvae in in the outer and the first S. agrili early A. planipennis larvae were in beetle a single host, one to 18 successfully on the host was killed in all The female to was S. agrili to have to four generations a with one for A. planipennis. in and in a biocontrol be to a pest and in its to we the of S. in China it to be an parasitoid of A. planipennis. S. A. Russian Academy of for the of the new species and specimens for the and Reardon and Forest Morgantown, for of the we University of for and and Forest Japan, for we Wang, University, West are also to the following in China: and of Chinese Academy of for the types of Spathius described by late Hsiu-Fu Chao in the Insect Museum of the Fujian Agricultural University, for in the new species with a and on species; and Forest Park, Dagang, Tianjin, for in the Jian-Jun Pang, Tianjin for field in Tianjin Jilin and Jingyuetan Forest Park, Changchun, Jilin and Xiao-Yi Wang and of Forest for in field and SEM

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