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Publicly Available Published by De Gruyter July 16, 2015

Feeding stimulants for larvae of Graphium sarpedon nipponum (Lepidoptera: Papilionidae) from Cinnamomum camphora

  • Yong Zhang , Zhi-Hui Zhan , Shin-ichi Tebayashi , Chul-Sa Kim and Jing Li EMAIL logo

Abstract

The feeding response of larvae of the swallowtail butterfly, Graphium sarpedon nipponum (Lepidoptera: Papilionidae), is elicited by a methanolic extract from camphor tree (Cinnamomum camphora) leaves. Based on bioassay-guided fractionation, three compounds, isolated from the methanolic extract of fresh leaves of the camphor tree, were revealed to be involved in a multi-component system of feeding stimulants. Structures of these feeding stimulants were identified as sucrose, 5-O-caffeoylquinic acid and quercetin 3-O-β-glucopyranoside by NMR and LC-MS.

1 Introduction

Most butterfly species are phytophagous and usually utilize a limited range of host plants in nature. Although the host range of an insect is determined by a diversity of ecological, geographical, physiological and behavioral factors, the key elements underlying the host range determination are phytochemicals [1, 2]. As for larval insects, plant chemicals released from the leaf typically influence the decision as to whether or not the feeding will be continued [3, 4].

A number of swallowtail butterfly species in the genus Graphium commonly feed on species of the plant family Lauraceae, including the cinnamon tree. This insect belongs to the tribe Graphiini, which is placed between the Troidini and Papilionini in the evolutionary tree [5]. Thus, chemicals related to the host selection of species of the genus Graphium should be given attention to elucidate evolutionary processes in the Papilionidae family.

Graphium sarpedon nipponum, the common bluebottle, is one of the Lauraceae-feeding species, which usually utilizes Cinnamomum camphora as its major host. Adults of this butterfly are attracted by volatile components from C. camphora, which have been found to act as olfactory cues in determining the choice of food plants by G. sarpedon nipponum [6]. For a better understanding of the physiochemical background of present-day host utilization and host range evolution in Graphium butterflies, further attempts are needed to investigate the chemical basis for differential acceptance of a potential host plant.

Previously we reported the isolation and characterization of α-linolenic acid as a feeding stimulant from the hexane fraction of a C. camphora methanolic extract [5]. As part of our ongoing study on feeding stimulants from C. camphora, we have now investigated the polar fraction of C. camphora fresh leaves and isolated three additional feeding stimulants for G. sarpedon nipponum.

2 Materials and methods

2.1 Insect and plant

Eggs of G. sarpedon nipponum were collected from young branches of C. camphora trees growing on Monobe Campus of Kochi University, Japan. Larvae were kept at 25±3 °C and 70% relative humidity in Petri dishes with a 15:9 h, L:D photoperiod. The animate fifth instar larvae were used for bioassay. Fresh leaves of C. camphora were collected from the same source and used for extraction and bioassay.

2.2 Bioassay

The behavioral bioassay for the isolation of attractants and stimulants in the initiation of the feeding response were carried out as previously described [5]. Activities were expressed as gram leaf equivalents (g.l.e.) per semicircular Styrofoam test discs (45 mm in diameter, 0.7 mm in thickness). Samples of 0.5 g.l.e. were applied onto the discs. As the control, the same volume of a solvent blank was added to a disc. After drying, discs were placed in a Kimwipes box (13 cm×12 cm×9 cm) with the upper end open, and each disc was inserted into a slit of foam bottom, thereby kept in upright position. Usually one disc corresponded to one test sample, and the appropriate number of discs were introduced into the box for bioassay. Three fifth instar larvae, which had been starved for 6 h, were left in the box and their feeding behavior was observed for 24 h (25±3 °C, 15:9 h, D:L photoperiod). Styrofoam discs containing attractants or stimulants would be consumed by the larvae, and the feeding damage (consumed area in mm2) of discs was measured by a flat-bed scanner. Each test was repeated at least five times, and consumed areas of Styrofoam discs were averaged to serve as the index of the feeding stimulatory effect. Statistical analysis used one-way analysis of variance (ANOVA) followed by Tukey HSD test (p<0.05).

2.3 Extraction and fractionation

Fresh leaves (1.9 kg) of C. camphora were cut into pieces and extracted twice with 80% (v/v) aqueous methanol (Nacalai Tesque, Kyoto, Japan) at room temperature for three days under darkness. The combined extracts were filtered and the solvent was removed under reduced pressure. The residue (118.2 g) was redissolved in water (2.8 L) and partitioned with n-hexane (Nacalai Tesque, Kyoto, Japan) (2 L) for four times, yielding the n-hexane and aqueous layer, respectively. Each layer was dried under reduced pressure and subjected to the bioassay. The aqueous layer (63 g) was separated into four fractions by a reversed phase open column (ODS, 50 mm i.d.×500 mm, Wako Pure Chemical Industries, Osaka, Japan), eluting in sequence with an increasing concentration of methanol in water. Finally, the aqueous fraction A (28.86 g), the 20% MeOH/ H2O fraction B (8.67 g), the 40% MeOH/ H2O fraction C (7.60 g) and the MeOH fraction D (6.68 g) were obtained.

Fraction A was chromatographed on a reverse-phase HPLC column (Shiseido Capcell pak NH2 UG120Å 4.6 mm×250 mm, Shiseido, Japan) eluted with 75% CH3CN/H2O (Nacalai Tesque, Kyoto, Japan) at a flow rate of 1.0 mL/min, and four compounds were obtained. Compound 1 was isolated at Rt=5.92 min (0.71 mg/g.l.e.), compound 2 at Rt=7.21 min (2.08 mg/g.l.e.), compound 3 at Rt=8.12 min (0.76 mg/g.l.e.) and compound 4 at Rt=10.92 min (11.75 mg/g.l.e.).

Fraction B was purified on a reverse-phase HPLC column (Shiseido Capcell pak C18 UG120Å 10 mm×250 mm) and eluted with 20% MeOH/H2O (1% AcOH) at a flow rate of 3.0 mL/min to yield compound 5 (Rt=17.96 min, 0.48 mg/g.l.e.).

In the primary bioassay, fraction C did not stimulate feeding of the G. sarpedon nipponum larvae and was not subjected to further fractionation.

Fraction D was separated into three fractions: fraction D1, 0–10.6 min, fraction D2, 10.6–12.5 min, fraction D3, 12.5–20.0 min. This was done by reverse-phase HPLC (Shiseido Capcell pak C18 UG120Å 10 mm×250 mm), eluted with 20% CH3CN/H2O (1% AcOH). Compounds 6, 7 and 8 were isolated from fraction D3 by reverse-phase HPLC (Shiseido Capcell pak C18 UG120Å 10 mm×250 mm) at a flow rate of 3.0 mL/min, eluted with 20% CH3CN/H2O (1%AcOH), at Rt=13.01 min (13 μg/g.l.e.), Rt=13.72 min (18 μg/g.l.e.) and Rt=16.20 min (22 μg/g.l.e.), respectively.

2.4 Instruments

HPLC for the isolation and analysis of compounds was carried out with a Shimadzu LC-6AD pump equipped with a Shimadzu SPD-M10A detector (Shimadzu, Kyoto, Japan). NMR data were obtained on a JEOL JNM-L400 spectrometer (400 MHz, JEOL, Akishima, Japan) in CD3OD (Sceti, Tokyo, Japan) with TMS (Acros, NJ, USA) as an internal standard. Letters (br.) s, d, t, q and m represent (broad) singlet, doublet, triplet, quartet and multiplet, respectively, and coupling constants are given in Hz. LC-MS data were measured by a Shimadzu LC-MS 2010 liquid chromatography-mass spectrometer in APCI mode (Shimadzu, Kyoto, Japan).

3 Results and discussion

3.1 Chemical compounds in aqueous layer

A series of sugars (compounds 14) were isolated from fraction A. According to their diagnostic 1H-NMR and 13C-NMR spectra and by comparison of these with authentic samples [7], compounds 1, 2, 3 and 4 were identified as rhamnose, glucose, fructose and sucrose, respectively. Of these four sugars, sucrose (11.75 mg/g.l.e.) was the principal constituent with approximately 76.8%.

From fraction B, compound 5 was identified as 5-O-caffeoylquinic acid (5-CQA, 0.477 mg/g.l.e.) according to its diagnostic 1H-NMR and 13C-NMR spectra and by comparison with an authentic sample. The 13C-NMR spectrum indicated the presence of six carbons, including two carbonyl groups at δ175.1 (C-7) and δ168.8 (C-9′), respectively; two aromatic carbons bonded to hydroxyl groups at δ148.3 (C-3′) and δ145.5 (C-4′); two olefinic carbons at δ144.9 and δ121.3 corresponding to C-7′ and C-8′. Four aromatic carbons were assigned C-1′, C-2′, C-5′ and C-6′ at δ125.5, δ114.3, δ114.7 and δ115.7, respectively; three carbons, bonded to hydroxyl groups at δ73.7, δ68.4 and δ70.9, identified as C-1, C-3 and C-4; one carbon bonded to an ester group at δ70.6 attributed to C-5; and two methylene groups identified as C-2 and C-6 at δ37.2 and δ36.6, respectively. The 1H-NMR spectrum displayed two ortho-coupled doublets each for 1H, at δ6.70 and δ6.97, and a broad singlet for 1H at δ7.01, confirming the presence of a tri-substituted aromatic ring; and two doublets, each for 1H, at δ6.14 (H-7′) and δ7.41 (H-8′), indicating the presence of a trans-di-substituted ethylene moiety in the molecule [9].

5-CQA (5) was obtained as white amorphous powder. Further, LC-MS: m/z (%) 354 (80), 276 (57), 115 (20), 1H-NMR δH (CDCl3): 1.77 (1H, m, H-2a), 1.95 (1H, m, H-2b), 1.95 (1H, m, H-6a), 1.96 (2H, m, H-6b), 3.55 (1H, m, H-4), 3.91 (1H, m, H-5), 5.06 (1H, m, H-3), 6.14 (1H, d, J=15.8, H-7′), 6.70 (1H, d, H-5′), 6.97 (1H, d, H-6′), 7.01 (1H, br s, H-2′), 7.41 (1H, d, J=15.8, H-8′). 13C-NMR δc (CDCl3): 36.6 (C-6), 37.2 (C-2), 68.4 (C-3), 70.6 (C-5), 70.9 (C-4), 73.7 (C-1), 114.3 (C-2′), 114.7 (C-5′), 115.7 (C-6′), 121.3 (C-8′), 125.5 (C-1′), 144.9 (C-7′), 145.5 (C-4′), 148.3 (C-3′), 168.8 (C-9′), 175.1 (C-7).

Subsequent fractionation of fraction D by HPLC resulted in the isolation of a series of flavonoid glycosides (compounds 68) from fraction D3. Compounds 6, 7 and 8 were identified as quercetin 3-O-β-galactopyranoside, quercetin 3-O-β-glucopyranoside (0.42 mg/g.l.e.) and kaempferol 3-O-β-rutinoside, respectively, from their diagnostic 1H-NMR and 13C-NMR spectra and by comparison of these with authentic samples [8, 10]. Among these three compounds, only quercetin 3-O-β-glucopyranoside was active toward larvae of G. sarpedon nipponum. Its NMR data are given following. The inactive compounds quercetin 3-O-β-galactopyranoside and kaempferol 3-O-β-rutinoside have been described previously [8, 10].

Quercetin 3-O-β-glucopyranoside (7) was isolated as a yellow amorphous powder. LC-MS: m/z (%) 465 (38), 303 (82), 149 (29). 1H-NMR δH (CDCl3): 6.25 (1H, s, H-6), 6.46 (1H, s, H-8), 7.64 (1H, s, H-2′), 6.89 (1H, d, J=9.9, H-5′), 7.63 (1H, s, J=9.9, H-6′), 5.52 (1H, d, J=7.3, glc-1), 3.14–3.65 (glc). 13C-NMR δC (CDCl3): 156.5 (C-2), 133.5 (C-3), 177.6 (C-4), 161.5 (C-5), 98.9 (C-6), 164.5 (C-7), 93.6 (C-8), 156.3 (C-9), 104.0 (C-10), 121.7 (C-1′), 115.3 (C-2′), 144.9 (C-3′), 148.6 (C-4′), 116.3 (C-5′), 121.3 (C-6′), 101.9 (glc-1), 74.2 (glc-2), 76.6 (glc-3), 70.1 (glc-4), 77.6 (glc-5), 61.1 (glc-6).

3.2 Larval feeding stimulant activity of fractions

Our previous work had revealed that both the n-hexane and aqueous layer derived from a methanolic extract of C. camphora, strongly evoked a positive response (initiation of feeding) toward G. sarpedon nipponum respectively [5]. In the present study, the aqueous layer from the methanolic extract was further separated into the four fractions A, B, C and D. No individual fraction stimulated feeding of G. sarpedon nipponum larvae by itself, when assayed at the dose of 0.5 g.l.e. (Figure 1). However, the combination of (A+B+D) at a total of 0.5 g.l.e. stimulated feeding activity toward G. sarpedon nipponum as strongly as the original active aqueous layer (Figure 2). These results indicate that some compounds jointly involved in the feeding stimulant activity should reside in these three fractions.

Figure 1: Feeding response (mean±SE) of G. sarpedon nipponum toward the aqueous layer and individual fractions A–D from the aqueous layer. Control: Styrofoam discs treated with blank solvent. Significant difference between the control and the treated Styrofoam discs is presented by different letters. Each sample was tested at a total of 0.5 g.l.e. (p<0.05, n=5).
Figure 1:

Feeding response (mean±SE) of G. sarpedon nipponum toward the aqueous layer and individual fractions A–D from the aqueous layer. Control: Styrofoam discs treated with blank solvent. Significant difference between the control and the treated Styrofoam discs is presented by different letters. Each sample was tested at a total of 0.5 g.l.e. (p<0.05, n=5).

Figure 2: Feeding response (mean±SE) of G. sarpedon nipponum toward the aqueous layer and the fraction mixtures: A+B+C, A+B+D, A+C+D, B+C+D (each fraction equally represented 1/3). Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.
Figure 2:

Feeding response (mean±SE) of G. sarpedon nipponum toward the aqueous layer and the fraction mixtures: A+B+C, A+B+D, A+C+D, B+C+D (each fraction equally represented 1/3). Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.

3.3 Stimulation of larval feeding activity by isolated compounds

Continuous tracking of stimulants from the aqueous layer resulted in the isolation of three stimulants: sucrose (compound 4) from fraction A, 5-CQA (compound 5) from fraction B, and quercetin 3-O-β-glucopyranoside (compound 7) from fraction D. The bioassay result revealed that the combination (A+B+D) or (B+D+4) stimulated feeding, whereas the combination (B+D) did not, indicating that 4 was involved in feeding stimulation of G. sarpedon nipponum (Figure 3). But fraction A (with the principle constitute sucrose) alone did not stimulate feeding, thus, sucrose is just a co-stimulant. Similarly, the active combination (A+B+D) lacking 5 (from fraction B) or fraction B did not affect the feeding behavior of G. sarpedon nipponum. This suggests that 5-CQA is an essential component in the stimulation of the feeding response of G. sarpedon nipponum (Figure 4). A mixture of stimulants (4+5) was almost inactive, but their effect was strongly synergized by quercetin 3-O-β-glucopyranoside (compound 7 from fraction D, Figure 5). To examine the feeding-stimulant activities of the other two flavonoid glycosides in fraction D, feeding responses to the blends (4+5+6) and (4+5+8) were compared with those to the active fractions. Either of these mixtures did not exhibit feeding-stimulant activity (Figure 5). This suggested that quercetin 3-O-β-glucopyranoside (7) was the active feeding stimulating compound, whereas neither 6 nor 8 were involved in the multi-component system of feeding stimulants. Fraction D alone did not stimulate feeding, indicating that the feeding-stimulant activity of 7 in this fraction might be counteracted by some compounds, such as compound 6,8 or some unknown compounds exhibiting antifeedant activity. The present results demonstrate for the first time that sucrose, 5-CQA and quercetin 3-O-β-glucopyranoside are involved in the multi-component system of feeding stimulants of G. sarpedon nipponum.

Figure 3: Feeding response (mean±SE) of G. sarpedon nipponum toward combinations of fractions A, B, and D, or compound 4. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.
Figure 3:

Feeding response (mean±SE) of G. sarpedon nipponum toward combinations of fractions A, B, and D, or compound 4. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.

Figure 4: Feeding response (mean±SE) of G. sarpedon nipponum toward combination of fractions A, B, and D, or compound 5. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.
Figure 4:

Feeding response (mean±SE) of G. sarpedon nipponum toward combination of fractions A, B, and D, or compound 5. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.

Figure 5: Feeding response (mean±SE) of G. sarpedon nipponum toward compounds 4–8 in various combinations. 4: sucrose, 5: 5-O-caffeoylquinic acid, 6: quercetin 3-O-β-galactopyranoside, 7: quercetin 3-O-β-glucopyranoside, 8: kaempferol 3-O-β-rutinoside. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.
Figure 5:

Feeding response (mean±SE) of G. sarpedon nipponum toward compounds 48 in various combinations. 4: sucrose, 5: 5-O-caffeoylquinic acid, 6: quercetin 3-O-β-galactopyranoside, 7: quercetin 3-O-β-glucopyranoside, 8: kaempferol 3-O-β-rutinoside. Control: Styrofoam discs treated with blank solvent (p<0.05, n=5). For further details refer to Figure 1.

The strong feeding stimulation by essential nutrients can be universally observed throughout the animal kingdom; sugars in particular are known as general feeding stimulants in herbivorous insects, the larvae of which develop specific receptors tuned for these primary metabolites [11, 12]. Sugars 14 appear to provide a basic nutrient, and the principal constituent, sucrose (76.8% in fraction A), indeed plays an important role in the feeding-stimulant activity toward G. sarpedon nipponum (Figure 1).

5-CQA (from fraction B) is the most commonly found – and the only commercially available – isomer of chlorogenic acid [9]. The phenolic compound, chlorogenic acid, is widely distributed in the plant kingdom [13, 14]. It encompasses several isomers, such as 3-caffeolyl-muco-quinic acid (3-CmQA), 4-caffeoylquinic acid (4-CQA) and 5-caffeoylquinic acid (5-CQA), and these are known to play various roles in plant defense [15], or to have oviposition-stimulant activity for Papilio polyxenes and Papilio protenor [14, 16]. Zebra swallowtail females are stimulated strongly by a single of these compound, i.e. 3-CmQA [17]. In the present study, 5-CQA has been identified as a feeding stimulant for G. sarpedon nipponum for the first time.

Flavonoid glycosides are known as oviposition stimulants for some Rutaceae-feeding swallowtails. From methanolic extracts of one of its host plants, Citrus unshiu, four flavonoid oviposition stimulants for the swallowtail Papilio xuthus were identified [4]; from the epicarp of Citrus natsudaidai, two flavonoid glycosides, hesperidin and naringin, were isolated that stimulated oviposition of Papilio proteor [18]. Flavonoid glycosides from C. camphora have apparently not been reported previously as feeding-stimulants. In this study, quercetin 3-O-β-glucopyranoside was identified as a feeding stimulant.

Occurrence of some feeding stimulant compounds in appropriate concentrations in plants other than host plants might mislead female butterflies to oviposit on non-host plants. Oviposition “mistakes” by females would provide a chance to colonize novel host plants [19]. Sucrose, 5-CQA and quercetin 3-O-β-glucopyranoside are common compounds widespread in the plant kingdom. Therefore, it might be advantageous for G. sarpedon nipponum to utilize these compounds as food cues to exploit additional food resources with a similar phytochemical profile. The combination of sucrose, 5-CQA and quercetin 3-O-β-glucopyranoside includes both primary and secondary metabolites. Primary metabolites are generally important for larval growth and survival [20], whereas secondary metabolites are essential for stimulating the feeding response of G. sarpedon nipponum [5]. This may explain why this particular combination exhibits feeding-stimulant activity toward larvae of G. sarpedon nipponum. Moreover, it is interesting to note that the three compounds act synergistically, because any individual compound or the arbitrary combination of two compounds were inactive. Only three compounds in combination synergistically stimulate feeding activity. Similar synergistic effects among several compounds, such as sugars and flavonoids, have been confirmed in the feeding stimulation of Papilio xuthus [20].

Many Graphiini species are strongly associated with Lauraceae species, with either wide or narrow preferences within this plant family. Systematic studies on the chemistry controlling feeding behavior among these closely related species should provide important information on the evolutionary process of their host utilization and diversity.


Corresponding author: Jing Li, Ninth People’s Hospital of Chongqing, Beibei District, Chongqing 400715, China, Fax: +86-023-6825-0994, E-mail:

Acknowledgments

This work was supported in part by the Fundamental Research Foundation for the Central Universities (XDJK2013C156 and SWU113016 to Y.Z.).

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Received: 2014-9-2
Revised: 2015-1-20
Accepted: 2015-6-17
Published Online: 2015-7-16
Published in Print: 2015-5-1

©2015 by De Gruyter

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