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Electrophysiological and Behavioral Responses of Helicoverpa Assulta (Lepidoptera: Noctuidae) to Tobacco Volatiles

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Electrophysiological and Behavioral Responses of Helicoverpa Assulta (Lepidoptera: Noctuidae) to Tobacco Volatiles Arthropod-Plant Interactions (2012) 6:375–384 DOI 10.1007/s11829-012-9190-7 ORIGINAL PAPER Electrophysiological and behavioral responses of Helicoverpa assulta (Lepidoptera: Noctuidae) to tobacco volatiles Jiu-Guang Sun • Ling-Qiao Huang • Chen-Zhu Wang Received: 30 March 2011 / Accepted: 29 February 2012 / Published online: 24 April 2012 Ó Springer Science+Business Media B.V. 2012 Abstract The Oriental tobacco budworm moth, Heli- Keywords Helicoverpa assulta Á GC–EAD Á GC–MS Á coverpa assulta (Guene´e) (Lepidoptera: Noctuidae), is a Tobacco Á Wind tunnel Á Olfactory receptor neuron Á Single serious pest on tobacco in China. The flowering stage of the sensillum recording host plant is one of the most attractive stages to H. assulta for feeding and oviposition. Nine electrophysiologically active compounds in tobacco headspace at flower stage were Introduction detected by gas chromatography–electroantennographic detection (GC–EAD). These compounds were subsequently The Oriental tobacco budworm moth, Helicoverpa assulta, identified by gas chromatography-mass spectrometry (Guene´e) (Lepidoptera: Noctuidae), is distributed in three (GC–MS) as (E)-b-ocimene, octanal, (Z)-3-hexenyl acetate, continents, Asia, Africa, and Australia. (Boo et al. 1995). (Z)-3-hexen-1-ol, nonanal, (Z)-3-hexenyl-2-methyl butyrate, Like the other oligophagous herbivores, H. assulta utilizes decanal, linalool, and (E)-b-caryophyllene. The synthetic a narrow range of host plants and mainly feeds on plant blend containing nine of the above compounds attracted species in Solanaceae such as tobacco, hot pepper, and mated H. assulta females from a distance by upwind oriented several Physalis species (Fitt 1989; Wang and Dong 2001). flight. Selected subtraction assays showed that the 4-com- The larvae of H. assulta preferentially feed upon the buds ponent mixture of (E)-b-ocimene, (Z)-3-hexenyl acetate, and the reproductive organs of tobacco and other host nonanal, and (E)-b-caryophyllene elicited equivalent levels plants, leading to severe economic loss. Because of their of attraction as the 9-component mixture. The removal of any habit of feeding inside the reproductive organs, the larvae of the four compounds from the 4-component blend resulted are difficult to control with conventional insecticides, and it in a significant decrease in female upwind flight behavior. is urgent to develop alternative control strategies (Boo et al. 1995). The sex pheromone of H. assulta has already been Handling Editor: Anna-Karin Borg-Karlson. identified by Sugie et al. (1991) and is highly attractive to male H. assulta (Cork et al. 1992). However, control J.-G. Sun Á L.-Q. Huang Á C.-Z. Wang strategies based on lures developed from female sex State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of pheromones have one important drawback, which is that Sciences, Beijing, People’s Republic of China only male behavior is affected, and not the behavior of gravid females. The pheromone-based approaches are not J.-G. Sun efficient at high population densities or when the mated Graduate School of the Chinese Academy of Sciences, Beijing, People’s Republic of China females immigrate in the control areas. Methods that could also manipulate the behavior of egg-laying females would C.-Z. Wang (&) enhance the efficacy of pheromonal techniques. Institute of Zoology, The Chinese Academy of Sciences, Chemical stimuli from plants play an important role in 1 Beichen West Road, Chaoyang District, Beijing 100101, People’s Republic of China insect–plant interactions. Many phytophagous insects use e-mail: [email protected] odors as cues for orientation to host, for mate-finding, their 123 376 J.-G. Sun et al. own nutrition, or oviposition (Schoonhoven et al. 2005). mating status, tested females were dissected and checked Up to now, in the case of lepidopteran moths, attractant for the presence of a spermatophore in the bursa copulatrix. plant volatiles mediating female long-range responses to Moths were provided with a 10 % honey solution. host plants have been identified, including Argyresthia conjugella (Bengtsson et al. 2006), Cydia molesta (Natale Chemicals et al. 2004), Cydia pomonella L. (Hern and Dorn 1999, 2004; Light et al. 2001), Mamestra brassicae (Rojas 1999), Plant odorants (Z)-3-hexen-1-ol (98 %) and (Z)-3-hexenyl Paralobesia viteana (Cha et al. 2008a, b), Lobesia botrana acetate (97 %) were purchased from Roth KG Company (Tasin et al. 2005, 2006a, b, 2007), Helicoverpa armigera (Karlsruhe, Germany). Octanal (98 %), nonanal (97 %), (Hartlieb and Rembold 1996; Jallow et al. 1999), Manduca decanal (97 %), racemic linalool (97 %), (E)-b-caryo- sexta (Fraser et al. 2003). More recently, in H. assulta and phyllene (99 %), and (R)-(?)-limonene (96 %) were other closely related heliothine moths, some selective obtained from Fluka Chemie Company (Buchs, Switzer- olfactory receptor neurons for particular volatile com- land). (Z)-3-hexenyl-2-methyl butyrate (97 %) and (Z)-3- pounds have been found by using gas chromatography hexenyl butyrate (98 %) were from Kosher (Houston, (GC) linked to single sensillum recording techniques USA). (E)-b-ocimene, obtained as a gift from Dr. J. J. A. (Stranden et al. 2003a, b; Røstelien et al. 2005). van Loon. (Wageningen University, the Netherlands), was Despite the importance of role played by olfactory cues analyzed by gas chromatography and mass spectrometry in host-plant location by H. assulta, little is known about (GC–MS), and its purity was 60 %, and the other fraction long-range perceptible host-plant signals of this moth is mainly limonene (more than 30 %). Hexane was from species. Tobacco is the primary host plant of H. assulta, Beijing Chemical Company, Beijing, China. and the flowering period of host plant is the most attractive stage for ovipositing or feeding (Wu 1990). In the present Collection of volatiles study, electrophysiologically active compounds from headspace samples of tobacco flowers were identified by Headspace sampling was used to collect volatiles from gas chromatography–electroantennographic detection clusters at full bloom of intact tobacco. This method is (GC–EAD), and their behavioral activity with female H. similar to that described by Wei et al. (2006), but with minor assulta was investigated in a wind-tunnel bioassay. modifications. Whole flowers were enclosed in a plastic oven bag (50 cm 9 60 cm) that was sealed with self-sealing strips around the stem. The compressed air was led through a water Methods and materials bubbler (500 ml) for humidification and a freshly activated charcoal filter for purification. The moisturized and filtered Plants air was pushed into the bag at a rate of 500 ml/min. Volatiles were trapped in a glass tube (10 cm long, 6 mm in diameter) Tobacco plants, Nicotiana tabacum L. (Solanaceae) var. containing at 80 mg of 80/100 mesh Super Q adsorbent NC89, obtained from Institute of Tobacco, the China (Alltech Assoc., Deerfield, IL, USA) with polypropylene Academy of Agricultural Sciences (CAAS), were kept in a wool in both ends. The glass tube was connected with Teflon climatized greenhouse at 26 ± 2 °C, 60 ± 10 % R.H. tubing to a small pump (Beijing Institute of Labor Instru- Potted plants that had fully expanded 4–5 true leaves were ments, China). Each collection lasted for 8 h and replicated transferred from the greenhouse to the outdoor in early for 5 times. Volatiles were desorbed by eluting the cartridge June in Beijing. Tobacco plants at full blossom were used with 200 ll redistilled hexane and stored at a freezer at for collection of volatiles in the field. -20 °C for subsequent use. Insects Gas chromatography and electroantennographic detection (GC–EAD) Helicoverpa assulta were originally collected as larvae from the tobacco field in Zhengzhou, Henan Province of The antenna of H. assulta was prepared as described by Zhao China, and maintained for over ten generations in controlled et al. (2006) with some modifications. The antenna of the conditions under a 16L: 8D photoperiod cycle at 26 ± 1 °C 3-6-day-old mated females was cut at the base of the fla- and 55–65 % relative humidity. Larvae were fed on artifi- gellum and the tip of terminal segment was removed. The cial diet described by Wu and Gong (1997). Pupae were excised antenna was mounted between two microelectrodes sexed and placed in cages separately. After emergence, with some electrode gel. The electrodes were connected with male and female adults mated in nylon cages. 3-day-old a micromanipulator (Syntech MP-15, Germany). The signals mated females were used in wind-tunnel tests. To verify the from the antenna were amplified with a high impedance 123 Tobacco volatiles attracting Helicoverpa assulta 377 amplifier (IDAC-4, Syntech, Germany) and were sent to a electrode was inserted into the base of a sensillum and computer. Data storage and processing was conducted by the made sure it was in contact with a single receptor neuron. Autospike software package (Syntech, Germany). Linked First, we stimulated with the various volatiles under the GC–EAD analyses were conducted using an Agilent 7890A dose of 500 lg, and when the responding signal was suf- GC equipped with a polar HP-INNOWAX column ficiently strong for one compound, we stimulated with (30 m 9 0.25 mm 9 0.25 lm). Nitrogen was used as car- different concentrations of the compound. All the tests rier and makeup gas (30 ml/min). A 2 ll sample was intro- were performed by blowing air (10 ml/s) through a Pasteur duced into the GC column in a splitless mode using a split/ pipette (15 cm long) containing test compounds on filter splitless injector at 220 °C with the Flame Ionization paper strip (0.5 cm 9 3.0 cm). Action potentials of the Detector (FID) at 250 °C. The oven temperature was pro- receptor neurons were amplified through a USB-IDAC grammed as follows: 40 °C for 2 min; 5 °C/min to 230 °C interface amplifier (IDAC-4, Syntech, Germany).
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