Biological Control 47 (2008) 216–221 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Host specificity of Spathius agrili Yang (Hymenoptera: Braconidae), an important parasitoid of the emerald ash borer Zhong-Qi Yang a,*, Xiao-Yi Wang a, Juli R. Gould b, Hui Wu c a The Key Laboratory of Forest Protection, State Forestry Administration of China, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Dongxiaofu 2, Haidian District, Beijing 100091, China b United States Department of Agriculture, Animal and Plant Health Inspection Service, Center for Plant Health Science and Technology Laboratory, 1398 West Truck Road, Buzzards Bay, MA 02542, USA c North Greening Center, Changchun, Jilin 130117, China article info abstract Article history: To investigate the host range of Spathius agrili Yang (Hymenoptera: Braconidae), a total of 18 wood boring Received 11 April 2008 insects either in the genus Agrilus or associated with ash forests were collected, reared, and presented to Accepted 1 August 2008 S. agrili females in no-choice tests. Results showed that S. agrili can parasitize some other insect larvae in Available online 13 August 2008 genus of Agrilus, but attack rates were significantly lower than its natural host, emerald ash borer, Agrilus planipennisi Faimaire (Coleoptera: Buprestidae). In Y-tube olfactometer tests, female S. agrili were only Keywords: attracted to twigs and leaves of EAB infested Fraxinus velutina and F. pennsylvanica, and not to 12 other Spathius agrili potential host plants. Two other plants, Prunus persica (L.) and Ailanthus altissima (Mill.), significantly Emerald ash borer repelled the EAB. Field surveys of 17 wood boring insects, including six species of Agrilus, revealed that Agrilus planipennis Host range none of these species were parasitized by S. agrili. It was indicated that the EAB natural parasitoid S. agrili Specificity has high host specificity. Natural enemy importation Ó 2008 Elsevier Inc. All rights reserved. Biological control 1. Introduction range of the EAB for use in classical biological control (Liu et al., 2003; Yang et al., 2005, 2006; Zhang et al., 2005). The emerald ash borer (EAB), Agrilus planipennis Fairmaire Spathius agrili Yang (Hymenoptera: Braconidae) is an important (Coleoptera: Buprestidae) is native to several countries in north- gregarious idiobiont natural enemy ecto-parasitizing EAB larvae in eastern Asia. This pest feeds on the phloem and cambium of ash Tianjin, China and other locations (Yang et al., 2005). It typically trees (Fraxinus spp.) in its larva stage, constructs overwintering exhibited 3–4 generations per year, overwintering as a full-grown chambers in outer sap wood when it is full grown, then pupates larva in a cocoon inside its host gallery. It’s mean natural parasit- and emerges the following spring (Yu, 1992). EAB are mostly uni- ism rate can over 60% in field (Wang et al., 2006; Yang et al., voltine in Tianjin, northern China. They overwintered as prepupae 2008). This parasitoid is a potential natural enemy for importation in shallow chamber excavated in the outer sapwood by them- to North America for successful biological control of EAB. Studies selves. The average longevity of adults was about 21 days and on the parasitoid biology (Yang et al., 2008), relations of spatial the adulthood lasted through early July. Female adults oviposited pattern between wasp and host (Wang and Yang, 2005), and effects in mid May and eggs hatched on average in 15.74 days. The larval of host size on sex ratios and clutch sizes (Wang et al., 2008a,b) stage lasted about 300 days to complete an entire generation have been conducted in detail. The EAB had four larval instars (Wang, 2005). EAB was discovered in North America in 2002 and (Wang et al., 2005) and the larvae mine under bark of their host has been causing serious damage to American forests (Haack trees, and that the parasitoids locate them might by vibration cues et al., 2002). Because of its cryptic life behavior and the difficulty and drill through the bark to parasitize them (Wang et al., in trapping this insect, it has proven difficult to control and to pre- 2008a,b). The parasitoid is a new species published in 2005, and vent spread throughout the USA. In order to seek a long-term and the EAB larva is just known the only host in natural condition effective control strategy, researchers in China and the USA have (Yang et al., 2005). discovered and screened potential natural enemies from the native Potentially, the introduction of exotic natural enemies or mass release of biological control agents may lead to unwanted non-tar- get effects. Whether or not such effects occur will mainly depend upon the host range of the biological control agent and the pres- * Corresponding author. Fax: +86 10 6288 9502. E-mail address: [email protected] (Z.-Q. Yang). ence of non-target species in the area of release (Lenteren et al., 1049-9644/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2008.08.001 Z.-Q. Yang et al. / Biological Control 47 (2008) 216–221 217 2005). Although legal requirements for assessing the impact of nat- Thyestilla gebleri Faldermann (Coleoptera: Cerambycidae) from ural enemies on non-target plants have been in place for a long Chingma abulilon (A. theophrasti Medicus); Eucryptorrhynchus chin- time, such testing has recently been required in some countries ensis (Olivier) (Coleoptera: Curculionidae) from Heaven tree (Ailan- for the importation of entomophagous natural enemies (Van Dri- thus altissima (Mill.); and an unidentified Pyralidae from F. esch, 2004). The potential negative impact of released biological velutina). In the USA, Agrilus anxius was collected from European control agents is a key component of the environmental assess- white birch (Betula pendula Roth.) in Amherst, MA, A. bilineata ment. In addition, many scientists believe that host ranges of can- was from White oak (Quercus alba L.) from Freetown, MA, A. rufic- didate natural enemies should be tested prior to introduction olis was from Red raspberry (Rubus idaeus L.) from Morgantown, (Simberloff and Stiling, 1996; Strong and Pemberton, 2000). WV, and EAB larvae were collected from Green ash (Fraxinus penn- Physiological host range tests have to be conducted by deter- sylvanica Marsh.) and White ash (F. americana L.) near Brighton, MI. mining wasp’s acceptance of potential non-target hosts. But this is very difficult to fulfill and the results often overestimated than 2.2. Field investigation that in natural conditions (Rutledge and Wiedenmann, 1999). Usu- ally, parasitic wasps search their host habitats according to smell At present, the wasp S. agrili was known to distribute in Tianjin from host plants (Vinson, 1976). Parasitoids will consequentially and Jilin, China, naturally parasitizing EAB larvae inside ash bark. response to the volatiles emitted from host plants. Thus, examina- But other potential hosts from other places or other plants have tion of a wasp’s habitat preferences could be used as a predictor of not been investigated yet. Besides EAB, other wood boring insect ecological host range (Rutledge and Wiedenmann, 1999). In this species were collected during 2004–2007 in and near ash forests study we evaluate the host range of S. agrili through investigations in Tianjin China. The larvae were reared in the laboratory to deter- in the field and bioassays in laboratory. mine whether these insects had been parasitized by S. agrili. These insects included O. orientalis (Mutuura and Munroe) from X. sibiri- cum Patrin., C. luteellus (Motschulsky) from P. communis (L.), H. ins- 2. Materials and methods ularis Staudinger from F. velutina, T. gebleri (Falderman) from A. theophrasti Medic, Sylepta derogata F. from A. theophrasti Medicus, 2.1. Insects Carposina niponensis Walsingham from Z. jujuba Mill. and an unidentified Pyralidae larva from F. velutina. Some common bup- Spathius agrili was collected from the Guangang Forest Park in restids in the genus Agrilus were also collected in China such as Dagang District, Tianjin Municipality, China. EAB larvae parasitized A. mali from M. pumila in Shaanxi Province, A. lewisiellus from J. re- by S. agrili and parasitoid cocoons were collected from velvet ash, gia in Shaanxi Province, A. zanthoxylumi from Z. bungeanum in Sha- Fraxinus velutina Torr., and reared in the laboratory in both China anxi Province, A. sorocinus from A. julibris in Tianjin, A. auriventris (Insect Culture Laboratory, Guangang Forest Park, Tianjin) and from C. reticulata in Zhejiang Province, L. bellula from P. persica in the United States (USDA-APHIS-PPQ, Center for Plant Health Sci- Beijing, and C. affinis Fabricius from P. tabulaeformis Carr. in Shanxi ence and Technology Laboratory, Buzzards Bay, MA). After emer- Province. No fewer than 50 individuals of each species were col- gence, adult wasps were fed a 20% honey solution (China) or lected. The selection criteria for the host range investigation in- pure honey (USA). clude (1) concealed insect larvae, especially wood borers in the Larvae for use in host specificity testing were collected from the same habitat (ash forest) as EAB lived; (2) other jewel beetle larvae, following host plants in the following locations: Agrilus mali Mat- especially Agrilus species. Certainly, it is impossible to collect all in- sumura from apple (Malus pumila Mill.) in Yijun County of Shanxi sects meet these criteria, we only select some representative Province in August 2005, and from Sievers apple (Malus sieversii insects. (Ledeb.) Roem. in Yili of Xingjiang Uygur Autonomous Region in July and August 2006; Agrilus lewisiellus Kerremans from walnut 2.3. Host specificity testing tree (Juglans regia L.) in Yijun County of Shaanxi Province in August 2005; Agrilus auriventris Saunders from tangerine (Citrus reticulata Host specificity tests were conducted from 2004 to 2007 in Chi- Blanco) in Xiangshan County of Zhejiang Province in October 2005; na and in 2006 in the USA, respectively.