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Chemical Factors Influencing the Feeding Preference of Three Appl. Entomol. Zool. 40 (1): 161–168 (2005) http://odokon.ac.affrc.go.jp/ Chemical factors influencing the feeding preference of three Aulacophora leaf beetle species (Coleoptera: Chrysomelidae) Makoto ABE*,† and Kazuhiro MATSUDA Insect Science and Bioregulation Laboratory, Faculty of Agriculture, Tohoku University; Sendai, Miyagi 985–8555, Japan (Received 23 July 2004; Accepted 2 November 2004) Abstract Three cucurbitaceous feeding leaf beetle species, Aulacophora indica, A. lewisii, and A. nigripennis, were investigated with regard to the relationship between feeding preference by the beetles and cucurbitacins B, E, I, and E-glucoside contents in the leaves of 18 cucurbitaceous plant species. HPLC analysis and TLC analysis of A. lewisii revealed that the cucurbitacin B and E-glucoside, which are strong feeding stimulants for A. indica and A. lewisii, were abundant in Lagenaria siceralia, Sicyos angulatus, and Cucumis melo leaves. In a feeding preference test using fresh leaves, A. in- dica preferred various cucurbitaceous plant species and methanol extracts regardless of the contents of the four cucur- bitacins. A. lewisii mostly fed on Luffa cylindrica leaves in which the four cucurbitacins were not detected. A. lewisii was also stimulated to feed by the methanol extracts of Lagenaria siceraria and L. cylindrical, while A. nigripennis, which is only slightly stimulated to feed by the four cucurbitacins, fed primarily on Trichosanthes kirilowii var. japon- ica leaves. Among 18 cucurbitaceous plants, only Diplocyclos palmatus leaves were completely rejected by the three beetle species, and these beetle species did not even feed on D. palmatus leaves treated with the cucurbitacins. These results indicate that some leaf constituents as well as the four cucurbitacins play an important role in host plant selec- tion by the three cucurbitaceous feeding beetle species. Key words: Cucurbitaceae; cucurbitacin; Aulacophora; feeding stimulant; feeding deterrent lewisii Baly (Abe et al., 2000). On the contrary, A. INTRODUCTION lewisii was strongly stimulated to feed by the cu- Cucurbitacins are known as feeding stimulants curbitacins, but the beetle feeds almost solely on for cucurbitaceous feeding leaf beetles such those leaves from the genus Luffa (Lewis and Metcalf, in the genera Acalymma, Aulacophora, Ceratoma, 1996; Abe et al., 2000). For these reasons, we have and Diabrotica, and are regarded as an essential come to believe that some other constituents in ad- factors for these beetle species to recognize the cu- dition to the cucurbitacins in leaves of cucurbita- curbitaceous host plants (Chambliss and Jones, ceous plants play important roles in the host plant 1966; Shinha and Krishna, 1969, 1970; Metcalf et selection by the Aulacophora beetles. Although cu- al., 1980; Ferguson et al., 1983; Nishida et al., curbitacins have been analyzed on cotyledons, 1986; Metcalf and Metcalf, 1992; Eben et al., fruits, and roots of many cucurbitaceous plants 1997). On the other hand, we have reported an ex- (Rehm et al., 1957; Rehm and Wessels, 1957; ample for which the host plant selection by two Lavie and Glotter, 1971; Metcalf et al., 1982; Fer- Aulacophora beetle species is explained by the guson et al., 1983; Nishida et al., 1986; Kitajima presence of cucurbitacins in the cucurbitaceous and Tanaka, 1989), investigations of the content of host plant leaves: A. nigripennis Motschulsky uses the cucurbitacins in leaves are limited. As for Aula- genus Trichosanthes plants (Cucurbitaceae) as cophora beetle species, the relationship between hosts, however, their feeding responses to cucur- host plant preference and the cucurbitacins is not bitacins B, E, I, and E-glucoside were much clear. Elucidation of host plant selection mecha- weaker than those of A. indica (Gmelin) and A. nisms will contribute to agricultural applications *To whom correspondence should be addressed at: E-mail: [email protected] † Present address: Final Disposal Engineering Section, Research Center for Material Cycles and Waste Management, National Institute for Environ- mental Studies; Tsukuba, Ibaraki 305–8506, Japan DOI: 10.1303/aez.2005.161 161 162 M. ABE and K. MATSUDA such as the breeding of insect resistant plants as of Faculty of Agriculture, Tohoku University. well as increasing our understanding of insect- Chemicals. Cucurbitacins B, E, and E-gluco- plant relationships. To clarify the relationship be- side were isolated from the fruits of Ecuballium tween cucurbitaceous plants and Aulacophora bee- elaterium (L.) A. Rich. and identified by NMR and tles, we evaluated the four cucurbitacins in leaves MS spectrometer (Abe et al., 2000). Cucurbitacin I of cucurbitaceous plants and investigated leaf con- was purchased from Funakoshi Co. Ltd. stituents that play an important role in host plant Feeding preference for leaves. To evaluate the selection by three Aulacophora beetle species, A. feeding preference of the three beetle species for indica, A. lewisii, and A. nigripennis. cucurbitaceous plants, a feeding test was conducted with the 18 cucurbitaceous plants described above. A filter paper (7 cm diameter, No. 1, Toyo) was MATERIALS AND METHODS placed at the bottom of a petri dish (6 cm diameter) Insects. A. nigripennis was collected in a field at and distilled water was added to maintain humidity. the Faculty of Agriculture, Tohoku University. A. Two centimeter disks of fresh test plant leaves were indica and A. lewisii were collected at Ishigaki Is- punched out with a cork borer. Two such leaflet land, Okinawa Prefecture. Adults were kept in a pieces were weighed and then placed on the filter cylindrical plastic case (9ϫ14 cm diameter) lined paper at the bottom of the petri dish. Three insects on the bottom with moistened paper towel, and lar- (mixed sex and starved for 24 h) were released into vae were in cylindrical plastic cases (5ϫ9 cm di- the petri dish. The test was continued for 2 h and ameter) filled halfway with moistened sand. These replicated five times. After completion of the test, insects were successively reared at 24Ϯ1°C, the leaflets were removed and weighed again. The 16L–8D photoregime and provided cucurbitaceous amount fed on was defined as the weight con- plant leaves (A. indica: Cucurbita maxima Duch- sumed. esne, Sicyos angulatus L., and Trichosanthes kir- Feeding response to D. palmatus leaf treated ilowii Maxim var. japonica Kitam. leaves; A. with cucurbitacins. On D. palmatus, neither the lewisii: Luffa cylindrical (L.) Roemer leaf; A. ni- fresh leaf nor the methanol extract was preferred gripennis: T. kirilowii var. japonica and S. angula- by the beetles. Therefore, it was considered that D. tus leaves) as food. palmatus leaf either contains strong feeding deter- Plants. Eighteen cucurbitaceous plants (nine rents or lacks a feeding stimulant. To clarify the wild species, nine cultivated species) were used for presence of feeding deterrent or lack of feeding tests. The wild species were: Diplocyclos palmatus stimulant, a feeding test using D. palmatus leaf (L.) C. Jeffrey, Gynostemma pentaphyllum Makino, treated with cucurbitacins was conducted. As a Melothria japonica Maxim. ex Cogn., M. liukiuen- feeding stimulant, cucurbitacin B was used for A. sis Nakai, Schizopepon bryoniaefolius Maxim., S. indica, and cucurbitacin I for A. lewisii. These cu- angulatus, Trichosanthes bracteata (Lam.) Voigt, curbitacins are known to exhibit strong feeding T. kirilowii var. japonica, and T. rostrata Kitam. stimulant activity to the respective two species Cultivated species (cultivar name and the seed (Abe et al., 2000). Because A. nigripennis was only company) were as follows: Benincasa hispida minimally stimulated to feed by cucurbitacins, (Thunb.) Cogn. (Maokuwa, Fukutane Co. Ltd.), methanol extract of T. kirilowii var. japonica leaf Citrulus lanatus (Thunb.) Matsum. and Nakai was used as a feeding stimulant. A fresh 2 cm leaf (Shimabeni, Tohoku Co. Ltd.), Cucumis melo L. disk of D. palmatus was punched out. An ethanol (Ougon, Sakata Seed Co. Ltd.), Cucumis sativus L. solution (0.03 ml) of feeding stimulants was ap- (Suyo, Sakata Seed Co. Ltd.), Cucurbita maxima plied uniformly to the upper surface of the leaf (Miyako, Sakata Seed Co. Ltd.), Lagenaria sicer- disk. The solvent was removed quickly by air-dry- aria (Molina) Standl. (Sennari, Sakata Seed Co. ing. The concentration of the cucurbitacins was ad- Ltd.), Luffa cylindrical (L.) Roemer (Futonaga, justed to 0.1 mg/ml, and the concentration of Sakata Seed Co. Ltd.), Momordica charantia L. methanol extract of T. kirilowii var. japonica leaf (Futoreishi, Takii Seed Co. Ltd.), and Sechium was 1 g leaf equivalent/ml. One leaflet was edule (Jacq.) Sw. (Hayatouri, Fukutane Co. Ltd.). weighed and then placed on the filter paper at the All plants were cultivated at the experimental field bottom of the petri dish. Three insects (mixed sex Feeding Preference of Three Aulacophora Leaf Beetle Species 163 and starved for 24 h) were released into the petri ture of the water bath was less than 40°C). Chloro- dish. Each test was continued for 4 h and replicated form extract was then dissolved in chloroform ® five times. After completion of the test, the leaflet (0.2 ml) and placed on a Sep-pak C18 cartridge. was removed and weighed again. The amount fed After the solvent was removed by airflow, the ex- on was defined as the weight consumed. tract was eluated with 70% methanol in water Feeding preference to methanol extracts from (3 ml). The eluate was dried in vacuo and then dis- leaves. To confirm whether feeding stimulants were solved in methanol (0.2 ml) for test sample. The present in 18 cucurbitaceous plant leaves, feeding sample was subjected to HPLC and TLC analysis. responses by three beetle species to leaf extracts HPLC systems were JASCO GULLIVER SERIES were investigated. Fresh leaves were extracted with with DP-L 910 multi scan detector (Japan Spectro- methanol (20 ml/g fresh leaves, repeated three scopic Co. Ltd.) and TOSO CCPM pump with UV- times). The solvent was removed by a rotary evap- 8000 detector (TOSO Co. Ltd.). Wavelength was orator.
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