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(Hymenoptera: Braconidae), a Parasitoid of the Emerald Ash Borer

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(Hymenoptera: Braconidae), a Parasitoid of the Emerald Ash Borer Biological Control 52 (2010) 24–29 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer Xiao-Yi Wang a, Zhong-Qi Yang a,*, Juli R. Gould b, Hui Wu c, Jian-Hai Ma d a The Key Laboratory of Forest Protection, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China b Animal and Plant Health Inspection Service, Department of Agriculture, Otis ANGB, MA 02542 5008, USA c Forestry Bureau of Sanming City in Fujian Province, Sanming, Fujian 365000, China d Forest Pest Control Station of Qinghai Province, Xining, Qinghai 810000, China article info abstract Article history: Spathius agrili Yang (Hymenoptera: Braconidae) is a newly described and important idiobiont ectoparasi- Received 6 November 2008 toid of the emerald ash borer (EAB) that has excellent potential as a biological control agent against EAB Accepted 15 September 2009 populations in the USA. In order to understand the ecological factors involved in the search and discovery Available online 23 September 2009 of concealed hosts by S. agrili, we investigated the behavioral responses of adult female wasps to potential semiochemicals from host plants, hosts, and host frass as well as to vibration signals from host feeding Keywords: and movement. Using a bioassay, we showed that S. agrili first finds the host’s habitats by detecting Spathius agrili the volatile compounds emitted by ash. In the second phase of host location and acceptance, the parasit- Agrilus planipennis oids detect the mechanical vibrations produced by host feeding and movement under the surface of the Host location Concealed insect pest bark and then probe to find the EAB larvae. Contact chemicals seem to play little or no role in short-range Biological control host finding. Female wasps avoided laying eggs on EAB larvae already parasitized and thus paralyzed. We hypothesized that female wasps were not attracted to these larvae due to their lack of feeding or move- ment. While an induced paralysis in the host is instrumental in avoiding superparasitism, we cannot rule out that S. agrili females also use an oviposition pheromone to deter conspecific females. Together, these results suggest that vibration and olfactory cues play significant roles in distinct phases of S. agrili host habitat and host location behaviors. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction is packed inside gallery, which makes detection and control of the insect challenging (Wang et al., in press). EAB was accidentally The emerald ash borer (EAB), Agrilus planipennis Fairmaire (=A. introduced into North America in the late 1990s and subsequently marcopoli Obenberger) (Coleoptera: Buprestidae), is an important killed large numbers of ash trees in the United States and Canada insect pest attacking trees in the genus Fraxinus (Oleaceae). It is na- (Haack et al., 2002). Eradication of the pest appears increasingly tive to Japan, Korea, China, and far eastern Russia. The susceptible unlikely as its distribution continues to expand. host trees include Fraxinus mandshurica Rupr., Fraxinus velutina Spathius agrili Yang (Hymenoptera: Braconidae) is an ectopar- Torr., Fraxinus americana L., Fraxinus pennsylvanica Marshall var. asitoid initially discovered in Tianjin, China that can cause a high subintegerrima (Vahl), and Fraxinus nigra Marshall (Yu, 1992; Pan percentage of parasitism in EAB populations. Parasitism rates are and You, 1994; Zhang et al., 1995; Haack et al., 2002; Zhao et al., typically 40–50%, but can be as high as 85–90% in some areas (Yang 2005). The EAB lays eggs inside bark crevices and the newly et al., 2005). Spathius agrili has also been found in Changchun, Jilin hatched larvae chew through the outer bark layer, later feeding Province. The adult female detects EAB larvae hidden under the on the cambium layer. There are four larval instars (Wang et al., bark, and using its ovipositor, penetrates through the bark to inject 2005). The fully grown fourth-instar larvae excavate galleries in venoms for paralyzing the host. The female then lays a clutch of the outer sapwood, where they pupate the following spring. EAB eggs on the surface of host (Yang et al., in press). Parasitized EAB adults emerge in early summer, leaving a D-shaped exit hole in larvae cease feeding and parasitoid progeny develop on the para- the bark. During immature development, larval frass is not ejected lyzed EAB larvae. The braconid larvae pupate at the end of host gal- outside of the tree as is the case for many wood-boring beetles, but leries after completely consuming the host. Parasitoid females have the ability to evaluate host larval sizes under the bark to opti- mally allocate the size and sex ratio of each clutch of eggs (Wang * Corresponding author. Fax: +86 10 6288 9502. et al., 2008). Female adults usually select late larval instars, which E-mail address: [email protected] (Z.-Q. Yang). 1049-9644/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2009.09.008 X.-Y. Wang et al. / Biological Control 52 (2010) 24–29 25 are larger, to ensure an adequate food supply for their offspring ima leaves, 10 mg of fresh EAB frass or 64 fourth-instar EAB larvae. (Wang et al., 2006). Each material was tested against clean air flowing in the other arm Spathius agrili has good potential as a biological control agent of the tube. Newly eclosed (within 1 week), mated female wasps and was released in the United States to control EAB populations were released individually into the base of the Y-tube and ob- in 2007 (Gould, personal comm.). The use of this parasitoid will re- served for up to 5 min. Choice was recorded when the wasp quire an adequate knowledge of its interactions with EAB, and we crossed a line half-way up the length of a given arm. No response provide here a preliminary investigation of the ecological mecha- was recorded if the wasp failed to make a selection within 5 min of nisms of S. agrili host location. More specifically, we have investi- its release into the tube. Each treatment included at least 30 repli- gated (i) S. agrili host-habitat location behavior (role played by cates (different female wasps), and wasps that failed to make a chemical cues from ash plants), (ii) host location behavior (re- choice were eliminated from the statistical analysis. Each wasp sponses to host vibration or semiochemicals from host larvae and was tested only once and all tests were performed between 0800 frass), and (iii) host-acceptance behaviors (with EAB, non-habitual and 1700 h at a temperature range of 25–29 °C and a relative hosts, and artificial hosts) and occurrence of superparasitism (two humidity of 55–70%. The Y-tube was washed with 95% ethanol egg clutches on one host larva) in a laboratory setting. This knowl- once every 10 runs, and for the testing of treatments (plant, EAB edge should prove useful in several applications related to the use larvae, and frass materials), the positions of the sample bottle of this natural EAB control agent, notably in artificial rearing tech- and the clean air bottle were switched once every five runs. In or- niques and field efficacy tests. der to expose wasps to uniform lighting, the entire Y-tube device was positioned vertically inside a wood box covered with a white cloth. 2. Materials and methods 2.2. Host location Both the parasitoids, S. agrili, and hosts, EAB larvae, tested in this study were collected from the Guangang Forest Park of Dagang 2.2.1. Field and laboratory observations of host-seeking behavior District in Tianjin, China (38°560N, 117°290E). The experimental Adult S. agrili were observed at a study site located in the Guan- forest contained a stand of 12-year-old velvet ash, F. velutina, gang Forest Park of Dagang District in Tianjin, China in 2005–2006. approximately 80% of which were infested with EAB. EAB larvae A stand of 12-year-old velvet ash, F. velutina, infested with EAB was were collected from the ash trees by peeling the bark. Wasp co- selected for the observations. From July to September, the mating coons were obtained from the host galleries and taken to the lab- behavior of adults and the host-seeking behaviors of female para- oratory for adult emergence. Newly emerging adult wasps were sitic wasps were observed on trees selected randomly in the field gregariously maintained within glass vials (2.8 cm dia. Â 11.5 cm and on twigs in the laboratory. Host-seeking behaviors of 10 fe- length) for group mating and developmental maturation of the fe- males were observed on ash trunks in field, while under laboratory male reproductive systems, which took approximately one week. conditions, 30 observations of mating and host-seeking behaviors All adult wasps were reared in glass vials (2.8 cm dia. Â 11.5 cm were recorded. length) sealed with cotton plugs and were fed a 20% honey solution applied to a small cotton ball on a piece of filter paper attached to 2.2.2. Response to dead hosts and artificial hosts the inside of the vial. One possible mechanism of S. agrili host location is the detec- Two methods were used to present EAB larvae to S. agrili fe- tion of mechanical vibrations produced by live hosts (feeding or males for parasitization. The ‘‘twig” method involved using small movement). We tested whether female wasps will oviposit on lar- F. velutina twigs (1.0–1.5 cm in diameter) that were cut into 5– vae that are not moving by presenting them with dead or artificial 10 cm long sections and then split in half along their length.
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