Pyrrolizidine Alkaloids Mediate Host-Plant Recognition by Ovipositing ...

Journal of Chemical Ecology, Vol. 23, No. 7, 1997

PYRROLIZIDINE ALKALOIDS MEDIATE HOST-PLANT RECOGNITION BY OVIPOSITING FEMALES OF AN OLD WORLD DANAID BUTTERFLY, Idea leuconoe

KEIICHI HONDA, 1 '* NANAO HAYASHI,' FUMIKO ABE,2 and TATSUO YAMAUCHI 2 'Study of Environmental Sciences Faculty of Integrated Arts and Sciences Hiroshima University, Higashihiroshima 739, Japan ^Faculty of Pharmaceutical Sciences Fukuoka University, Jonan-ku, Fukuoka 814-80, Japan (Received March 28, 1996; accepted February 28, 1997) Abstract—A giant danaid butterfly. Idea leuconoe, specializes on apocynaceous plants such as Parsonsia laevigata, which has been reported to contain pyrrolizidine alkaloids. Females of I. leuconoe deposited eggs in response to methanolic extract of P. laevigata, and subsequent bioassay-guided fractionation of the extract revealed that phytochemicals crucial for host recognition by ovipositing females are Parsonsia-specific macrocyclic pyrrolizidine alkaloids including parsonsianine, parsonsianidine, and 17-methylparsonsianidine. Parsonine, another P. laevigata pyrrolizidine component with a keto-dihydropyrrolizine moiety that is closely related in structure to male pheromones of the butterfly, and several nonhost pyrrolizidine alkaloids were entirely inactive. We interpret these data as strong evidence for an ancestral association through herbivory between danaid butterflies and pyrrolizidine alkaloids. Key Words—Oviposition stimulants. Idea leuconoe, Lepidoptera, Danaidae, Parsonsia laevigata, Apocynaceae, pyrrolizidine alkaloids, parsonsianine, parsonsianidine, 17-methylparsonsianidine.

INTRODUCTION

Close associations of some lepidopterous insects with pyrrolizidine alkaloids (PAs) have long been known and have been studied extensively in regard to pharmacophagy (Boppre, 1984a, 1986, 1990). Adults of many danaid and ithomiid butterflies utilize plant-derived PAs as defensive substances or as precur*To whom correspondence should be addressed.

1703 0098-0331/97/0700-1703$l2.50/0 €> 1997 Plenum Publishing Corporation

1704

HONDA, HAYASHI, ABE, AND YAMAUCHI

sors of male pheromones (Schneider et al., 1975; Eisner and Meinwald, 1987; Kelley et al., 1987; Stelljes and Seiber, 1990). Danaid butterflies use various plants including Asclepiadaceae, Apocynaceae, and Moraceae as their main host plants (Ackery and Vane-Wright, 1984). However, since host plants of the majority of danaid butterflies do not contain PAs, the adult butterflies utilizing those plants ingest PAs from nectar, withered foliage, or roots of PA-containing plants, including plants in the families Boraginaceae, Compositae, and Leguminosae (Edgar, 1975; Pliske, 1975; Boppre, 1981, 1983). Two controversial hypotheses have been put forward on the origin of Danaidae-PA interactions. One is that the PA requirement of danaid or ithomiid butterflies for sex pheromone and chemical defense stems from an ancestral association involving host plants that contained PAs as defensive chemicals. Intense herbivory by these adapted insects may have led to an evolution of cardenolides or steroidal alkaloids in some of the ancestral plants, with some danaids or ithomiids coevolving to colonize Asclepiadaceae (plants with cardenolides) or Solanaceae (plants with steroidal alkaloids, but no PAs). According to this scenario, the intake of PAs by danaids as adults from nonhost plants is a remnant of their ancestral association with host plants containing PAs (Edgar et al., 1974; Edgar, 1982, 1984). An alternative hypothesis has been propounded by Boppre (1978, 1984b), who argued that an association may have arisen from accidental uptake of PAs by danaids from PA-containing nectar. Those danaids that could tolerate the toxicity of PAs gained a selective advantage by storing them and subsequently developed a preference for them and a pheromonal system based on them. In time, some species shifted their larval food from PA-lacking plants to PAcontaining ones, which also would ensure protection for the larvae. Sufficient knowledge to choose between these two hypotheses is not available. An investigation of host recognition chemicals in a danaid species that relies on PA-containing plants (e.g., Apocynaceae) for larval growth and for PA acquisition may provide some new insight into the evolution of PA dependence among some Danaidae. Chemical and biological investigations of phytochemicals involved in egglaying by butterflies of several families have revealed an array of oviposition stimulants and deterrents (Renwick and Chew, 1994; Honda, 1995a,b; Nishida, 1995a). Relatively little, however, is known about chemical constituents reponsible for host selection by danaid females. To date, two publications have dealt with oviposition stimulants for danaid butterflies feeding on asclepiad plants that do not contain PAs. Ideopsis similis, a specialist on Tylophora tanakae, was induced to oviposit by phenanthroindolizidine alkaloids (Honda et al., 1995a,b), while certain quercetin glycosides (flavonoid) stimulated oviposition by the monarch butterfly, Danaus plexippus, which feeds on plants in Asclepias and related genera (Haribal and Renwick, 1996).

HOST RECOGNITION BY A BUTTERFLY

1705

Idea leuconoe is one of the Old World butterflies inhabiting Southeast Asia and the Ryukyu Islands of Japan. It specializes on an apocynaceous plant, Parsonsia laevigata, in Japan. The present paper reports oviposition stimulants for this butterfly and discusses the origin and the evolutionary process of the PA-danaid association.

METHODS AND MATERIALS

Insects. Females wild-caught in the Yaeyama Islands and their offspring (30- to 50-day-old gravid females) were used for behavioral bioassays. Larvae were raised on P. laevigata in a greenhouse at 22-29°C under a natural photoperiod from July to October. After emergence, both sexes were kept together for a month under quasinatural conditions in a greenhouse equipped with flowers as a nectar source. Individual females were examined to determine whether the female laid fertilized eggs. Females fed with 15% aqueous sucrose daily during the experiments were pretested to determine if they responded positively to the foliage of P. laevigata and negatively to an artificial leaf (see below) sprayed with water (control). Those that showed a positive response to the control leaf were discarded. Bioassay for Ovipositional Response. Mature females of I. leuconoe (usually more than 30 days after eclosion) search for and select oviposition sites by landing on potential plants and drumming the leaf surface with clubbed forelegs, which contain sensory hairs. Apparently, plant chemicals are perceived by chemoreceptors. If the plant is acceptable, a female immediately curls the abdomen and lays an egg on the underside of the leaf. A similar sequence of oviposition behavior also was observed under experimental conditions. A heart-shaped green plastic plate (29 cm2) coated with a test sample was presented to a gravid female as a foliage surrogate. Females were permitted free flight in a transparent plastic chamber (30 cm X 40 cm X 26 cm high) that was externally illuminated with an incandescent lamp (3500 lux). The ovipositionstimulatory activity of test materials at a dose of 100 /xg/cm2 for crude fractions or 10 /ig/cm2 for pure chemicals was estimated by a method similar to that given in a previous paper (Honda and Hayashi, 1995). The response was expressed as shown by equations 1 and 2,

1706


where N is the total number of females tested, and /?, denotes the response rate of an Individual. /?,• was calculated by equation 2, where 5, is the score for a single trial of a given female, and n is the number of trials. Trials were replicated four to seven times. Sj was scored as 1.0 for actual egg-laying or an equivalent behavior, 0.5 for half-curling the abdomen after drumming, and 0.0 for drumming only with no positive response. Unresponsiveness to the control leaf was confirmed every three trials of sample presentation. For all trials, merely alighting on ovipositional substrates without drumming was not included. Extraction, Fractionation, and Identification of Plant Chemicals. Fresh leaves of P. laevigata collected in Iriomote Island were extracted with methanol (about 5 ml/g) at room temperature for a week. The methanolic extract was evaporated to dryness in vacuo below 50°C and partitioned between chloroform and water to yield a chloroform fraction (fraction A) and a water-soluble fraction. The water-soluble fraction was further separated into five subfractions (fractions B-F) by column chromatography on a porous polymer gel (MCI Gel CHP20P, 75-150 /im, Mitsubishi Kasei). Fractions were eluted stepwise with water (fraction B), 25% aqueous methanol (fraction C), 50% aqueous methanol (fraction D), 75% aqueous methanol (fraction E), and methanol (fraction F). Identification of constituents was based on direct comparisons of TLC profiles on silicic acid, with chloroform-methanol-water (7:3:1) as the developer. NMR spectral data of compounds isolated by means of preparative TLC (Merck PLC plate Silica gel 60) were compared with those of authentic compounds that had been isolated and identified previously from P. laevigata by Abe and Yamauchi (1989) and Abe et al. (1990, 1991a,b). Test Chemicals. Pure chemical compounds of host-plant origin used for bioassays were those isolated previously or in this study by reported methods. Monocrotaline, retrorsine, and isatidine (retrorsine N-oxide) were purchased commercially (Aldrich). RESULTS When an artificial leaf painted with the methanol extract of P. laevigata was presented to a flying female, she alighted on the leaf and readily responded positively to the extract, with deposition of an egg after a sequence of drumming. This explicitly implies that a bioactive principle(s) that cues the female to recognize its host is present in the methanol extract of the host plant. The six fractions (A-F) obtained from the methanol extract were bioassayed for their oviposition-stimulatory activity (Table 1). The active substances were localized in fractions A and D, with weak activity in fraction C, which seemed due to contamination. Chemical analyses of constituents in fractions A and D revealed that three PAs, parsonsianine (1), parsonsianidine (2), and 17-methylparsonsianidine (3),

1707


TABLE 1 . OVIPOSITIONAL RESPONSES OF Idea leuconoe TO FRACTIONS DERIVED FROM HOST PLANT, Parsonsia laevigata Fraction"

Response (%, mean ± SE)

Females (N)

A B C D E F

78.1 ± 6.8

9 12 11 10 10 10

0 19.9 83.8 6.7 2.5

± ± ± ±

7.2 6.8 4.4 2.5

"The amount of each sample applied on the ovipositional substrate was 100 jig/cm 2 .

were present in fraction A. Fraction D contained in addition to 1 and 2, two lignan glycosides, lariciresinol-4,4'-bis-0-a-L-rhamnoside and secoisolariciresinol-4,4'-bis-0-a-L-rhamnoside, and a flavonol glycoside, kaempferol 3-0glucosyI-(l-*2)-glucoside, as the major components. The ability of each compound to elicit oviposition was assayed along with three other PAs, monocrotaline, retrorsine, and isatidine, that are common in PA-containing plants but not found in P. laevigata. Another PA, parsonine (4), that had been isolated from stems of P. laevigata (Abe and Yamauchi, 1987) was also tested. Only three PAs (1-3) evoked potent positive responses, and the other compounds were appraised as inactive (Table 2). The active compounds (Figure 1) are 14-membered macrocyclic PAs and are specific, as far as is known, to the genus Parsonsia (Edgar et al., 1980; Abe et al., 1990, 1991a,b). DISCUSSION

Components 1-3 are predominant PAs in the host plant and individually exerted significant stimulatory activities; ovipositing females are highly likely to rely on these PAs as principal cues in recognizing their host plant. Implication for Host Shift. It is possible that the present-day specialization of /. leuconoe on P. laevigata is an outcome of host shift. At present, many danaids feed on asclepiad plants that do not contain PAs, which undoubtedly indicates that their host selection is mediated by plant chemicals other than PAs. A recent report has documented that oviposition by an Asclepias-fetder, Danaus plexippus, is elicited by flavonoids (Haribal and Renwick, 1996). Generally speaking, host shift from one plant species to another seems unlikely to occur if there are no similarities in composition or physiological action of secondary metabolites present in the two. P. laevigata may contain some chemicals other

1708


TABLE 2. OVIPOSITIONAL RESPONSES OF Idea leuconoe TO HOST-PLANT CONSTITUENTS AND NONHOST PYRROLIZ1DINE ALKALOIDS

Compound"

Response (%, mean ± SE)

Females (N)

1 2 3 4 5 6 7 8 9 10

97.1 ± 1.7 98.2 ± 1.0 98.0 ± 1.3 0 0.6 ± 0.6 1.5 ± 1.5 0 2.4 ± 1.6 0.9 ± 0.9 2.9 ± 1.7

17 17 17 14 14 13 10 13 13 13

"1: parsonsianine, 2: parsonsianidine, 3: 17-methylparsonsianidine, 4: parsonine, 5: lariciresinol4,4'-bis-O-a-L-rhamnoside, 6: secoisolariciresinol-4,4'-bis-O-a-L-rhamnoside, 7: kaempferol 3-Oglucosyl-(l-»2)-glucoside, 8: monocrotaline, 9: retrorsine, 10: isatidine. The amount of each compound applied on the ovipositional substrate was 10 ^g/cm 2 . Compounds 1-7 are present in the host plant (P. laevigata) of the butterfly. Compound 7 was dissolved in methanol, the others in acetone. Compounds 1-3, when dissolved in a protic solvent such as methanol, tended to rapidly lose their biological activities during storage, although there was no sign of appreciable reduction of their titer. Therefore, it seems likely that some uncharacterized degradation products probably formed via solvolysis or decomposition, perhaps only in trace amounts, exerted a notable deterrent effect.

than PAs by which Asclepiadaceae-feeding danaids are stimulated to oviposit, and such plant constituents would be likewise stimulative to I. leuconoe. However, females of I. leuconoe responded to none of the other coexisting compounds that included a flavonoid (7). Flavonoids, among other phytochemicals, are extremely widespread in the plant kingdom. Our finding, therefore, appears somewhat unexpected, assuming that the females remain responsive to ancestral stimulants. It has been demonstrated that certain cyclitols and their derivatives constitute a common subset of oviposition stimulants, although distinct compounds are involved for several papilionid butterflies feeding on Rutaceae, Apiaceae, or Aristolochiaceae, the last of which is a suspected ancestral host-plant family of the Papilionidae (Papaj et al., 1992; Honda, 1995a; Nishida, 1995a). Although PAs are distributed in many plant families, host plants with PAs presently used by danaid and ithomiid butterflies are confined to apocynaceous plants in the tribe Parsonsieae (Edgar, 1984). Females of 7. leuconoe may be anticipated to show a broader response spectrum to PAs in oviposition, since most danaid butterflies, irrespective of sex, are considered to have affinity for


1709

FIG. 1. Major pyrrolizidine alkaloids present in Parsonsia laevigata, the host plant of Idea leuconoe. Each of compounds 1-3 singly stimulates oviposition by the butterfly, whereas compound 4 does not.

a variety of PAs due to their indiscriminate uptake of unspecified PAs from diverse plants (females of most danaids also visit PA sources, and this behavior is often observed in the field). However, I. leuconoe females proved to be narrowly adapted only for host-specific PAs. Therefore, the use of specific PAs in host recognition by the females seems to be a plesiomorphic feature in evolutionary time. PAs consist of two structurally distinct parts designated necine base and necic acid. Since all PAs tested here (including those not present in Parsonsia) except parsonine (4) share the same necine base, our results suggest that specific structures of the necic acid moiety are crucial for conferring oviposition-stimulatory activity. It is not clear, however, whether these three PAs are distinguished from one another by the females. Implication for Pheromone System. Very recently, adult males of I. leuconoe were found to secrete danaidone, viridifloric /3-lactone, and others from the abdominal hair-pencils. Behavioral and electrophysiological experiments have substantiated that the first two compounds elicit receptive responses from the females (Nishida et al., 1996). By virtue of their structural similarities to the subunits of PAs, i.e., necine base and necic acid, they are believed to be derived

1710


from host-plant PAs sequestered during the larval period. The adults of both sexes have also been shown to store large quantities of characteristic PAs that are suspected to be of host-plant origin (Nishida et al., 1991; Kim et al., 1994), since field observations showed that they almost never visit PA-containing nonhost plants. Although the stored PAs are somewhat different in structure from compounds 1-3, it has been briefly mentioned that they also stimulate oviposition by the females (Nishida, 1995b). Danaidone, a keto-dihydropyrrolizine compound frequently encountered in male androconial secretions of danaids, has been thought to play an important role in mating systems of most danaids (Eisner and Meinwald, 1987; Boppre, 1990; Honda et al., 1995a). Males of /. leuconoe also make use of this compound in courtship, but the per capita quantity of danaidone is extremely small; some hundredths to some thousandths as compared with those of other PA-seeking danaids. It seems, therefore, untenable to speculate that a PA-seeking insect that is dependent on them for pheromone biosynthesis (Schneider et al., 1975) came to produce a much smaller amount of pheromone (danaidone) after having switched its host to a PA-containing plant in order to gain easier access to PAs. It also appears curious that, despite that, it ceased to gather more PAs from other plants in the adult. Furthermore, if pharmacophagous acquisition of PAs as adults has evolutionarily resulted in a development of capacity for producing pheromones, and again if host shift occurred after the establishment of their pheromone system, then parsonine (4) present in the host plant would probably be very important to the males, because this unique compound consists simply of two skeletal parts of keto-dihydropyrrolizine and viridifloric acid, which would be readily and efficiently converted to their pheromones, danaidone and viridifloric /3-lactone, respectively. From the sole viewpoint of chemical reaction, parsonine appears to be the best precursor of the known PAs (Logie et al., 1994) available for pheromone biosynthesis. The physiological significance of parsonine does not seem limited only to the males. Since males of I. leuconoe are considered to rely exclusively on host-plant PAs for pheromone production, the quality and the quantity of PAs including parsonine in the host plant would also be a matter of primary concern to the females that have to achieve successful mating and fertilization. Then ovipositing females of I, leuconoe would be expected to show a more or less positive response to parsonine. However, parsonine had no stimulatory activity at all. In view of the well-known male-biased attraction of danaids to PA-containing plants, presumably to get pheromone precursors (Edgar, 1975; Pliske, 1975; Boppre, 1981, 1983), the unresponsiveness of I. leuconoe females to parsonine strongly suggests that any later colonization of PA-containing plants by this butterfly as a result of host shift from PA-free plants, if it ever occurred, was independent of their reproductive strategy. In this butterfly, necic acid-derived viridifloric j8-lactone disseminated by males as a sex pheromone is one of the major hair-pencil components (Nishida

1711


et al., 1996). At present, there is no evidence for the use of necic acid-derived pheromones by other danaids feeding on PA-free plants, although males of several ithomiid butterflies have been reported to secrete a 7-lactone structurally related to the necic acid moiety from costal fringes of the hindwings (Edgar et al., 1976; Schulz et al., 1988). The lactone is thought to serve as a territorial marker. Accordingly, it appears unreasonable to assume that such a pheromone system as that represented by I. leuconoe has evolved from those of the major lineage of danaid butterflies that sequester PAs as adults and secrete necine basederived dihydropyrrolizines as principal components (Eisner and Meinwald, 1987). It may be concluded that the establishment of an association of this primitive butterfly with PA-containing plants would have preceded the development of its pheromone system. This is also suggestive of an additional and as yet unknown function of PAs of physiological importance. It may also be hypothesized that ancestors of danaids and ithomiids that had originally utilized two categories of compounds as pheromones might have possibly diverged into two or more groups: one using chiefly necine base derivatives (danaids) and another using chiefly necic acid derivatives (ithomiids). A number of danaid and ithomiid larvae still maintain the capacity for assimilating and storing PAs (Rothschild and Edgar, 1978; Trigo and Motta, 1990). The present work and other facts discussed above strongly support the hypothesis that the ancestors of danaid butterflies used PA-containing host plants and that the present-day dependence of danaids on PAs originates from their ancestral association with PA-containing host plants. Host shifts from PA-containing plants (e.g., Apocynaceae) eventually to PA-free plants (e.g., Asclepiadaceae) in danaid butterflies that evolved a strategy to acquire PAs as adults from nonhost plants could occur if some phytochemical mediators other than PAs are involved in the exploitation of novel hosts. Acknowledgments—We thank Dr. M. Nakai of UBE Scientific Analysis Laboratory, Inc., M. Sakamoto of Hiroshima City Forest Park for help in collecting and rearing butterflies, and Dr. R. Nishida of Kyto University for helpful discussion. We are greatly indebted to Dr. James L. Nation, University of Florida, who kindly improved our manuscript linguistically.

REFERENCES ABE, F., and YAMAUCHI, T. 1987. Parsonine, a pyrrolizidine alkaloid from Parsonsia laevigata. Chem. Pharm. Bull. 35:4661-4663. ABE, F., and YAMAUCHI, T. 1989. Lignan glycosides from Parsonsia laevigata. Phylochemistry 28:1737-1741. ABE, F., NAGAO, T., OKABE, H., YAMAUCHI, T., MARUBAYASHI, N., and UEDA, I. 1990. Parsonsianine, a macrocyclic pyrrolizidine alkaloid from the leaves of Parsonsia laevigata (Studies on Parsonsia. III). Chem. Pharm. Bull. 38:2127-2129. ABE, F., NAOAO, T., OKABE, H., and YAMAUCHI, T. 199la. Macrocyclic pyrrolizidine alkaloids from Parsonsia laevigata. Phytochemistry 30:1737-1739.

1712


ABE, F., YAMAUCHI, T., YAOA, S., and MINATO, K. 1991b. Pyrrolizidine alkaloids from Parsonsia laevigata in Okinawa Island (Studies on Parsonsia. V). Chem. Pharm. Bull. 39:1576-1577. ACKERY, P. R., and VANE-WRIGHT, R. I. 1984. Milkweed Butterflies: Their Cladistics and Biology. Cornell University Press, New York, 425 pp. BOPPRE, M. 1978. Chemical communication, plant relationships, and mimicry in the evolution of danaid butterflies. Enlomol. Exp. Eppt. 24:264-277. BOPPRE, M. 1981. Adult Lepidoptera "feeding" at withered Heliotropium plants (Boraginaceae) in East Africa. Ecol. Entomol. 6:449-452. BOPPRE, M. 1983. Leaf-scratching—a specialized behaviour of danaine butterflies (Lepidoptera) for gathering secondary plant substances. Oecologia 59:414-416. BOPPRE, M. I984a. Redefining "pharmacophagy." J. Chem. Ecol. 10:1151-1154. BOPPRE, M. 1984b. Chemically mediated interaction of butterflies, pp. 259-275, in R. 1. VaneWright and P. R. Ackery (ed.). The Biology of Butterflies. Academic Press, London. BOPPRE, M. 1986. Insects pharmacophagously utilizing defensive plant chemicals (pyrrolizidine alkaloids). Naturwissenschaften 73:17-26. BOPPRE, M. 1990. Lepidoptera and pyrrolizidine alkaloids. Exemplification of complexity in chemical ecology. J. Chem. Ecol. 16:165-185. EDGAR, J. A. 1975. Danainae and 1,2-dehydropyrrolizidine alkaloid-containing plants-with reference to observations made in the New Hebrides. Phil. Trans. R. Soc. B 272:467-476. EDGAR, J. A. 1982. Pyrrolizidine alkaloids sequestered by Solomon Island Danaine butterflies. The feeding preferences of the Danainae and Ithomiinae. 7. Zoo/. London 196:385-399. EDGAR, J. A. 1984. Parsonsieae: Ancestral larval foodplants of the Danainae and Ithomiinae, pp. 91-93, in R. I. Vane-Wright and P. R. Ackery (ed.). The Biology of Butterflies. AcademicPress, London. EDGAR, J. A., CULVENOR, C. C. J., and PLISKE, T. E. 1974. Coevolution of danaid butterflies with host plants. Nature 250:646-648. EDGAR, J. A., CULVENOR, C. C. J., and PLISKE, T. E. 1976. Isolation of a lactone, structurally related to the esterifying acids of pyrrolizidine alkaloids, from the costal fringes of male Ithomiinae. J. Chem. Ecol. 2:263-270. EDGAR, J. A., EGGERS, N. J., JONES, A. J., and RUSSELL, G. B. 1980. Unusual macroeyclic pyrrolizidine alkaloids from Parsonsia heterophylla A. Cunn and Parsonsia spiralis Wall. (Apocynaceae). Tetrahedron Lett. 21:2657-2660. EISNER, T., and MEINWALD, J. 1987. Alkaloid-derived pheromones and sexual selection in Lepidoptera, pp. 251-269, in G. D. Prestwich and G. J. Blomquist (ed.). Pheromone Biochemistry. Academic Press, London. HARIBAL, M., and RENWICK, J. A. A. 1996. Oviposition stimulants for the monarch butterfly: Flavonol glycosides from Asclepias curassavica. Phytochemistry 41:139-144. HONDA, K. 1995a. Chemical basis of differential oviposition by lepidopterous insects. Arch. Insect Biochem. Physiol. 30:1-23. HONDA, K. 1995b. Plant secondary metabolites implicated for host selection and host specificity in butterflies. Comp. Physiol. Biochem. 12:145-165. HONDA, K., and HAYASHI, N. 1995. A flavonoid glucoside, phellamurin, regulates differential oviposition on a rutaceous plant, Phellodendron amurense, by two sympatric swallowtail butterflies, Papilio protenor and P. xuthus: The front line of a revolutionary arms race? /. Chem. Ecol. 21:1531-1539. HONDA, K., TADA, A., and HAYASHI, N. 1995a. Dihydropyrrolizines from the male scent-producing organs of a danaid butterfly, Ideopsis similis (Lepidoptera: Danaidae) and the morphology of alar scent organs. Appl. Entomol. Zool. 30:471-477. HONDA, K., TADA, A., HAYASHI, N., ABE, F., and YAMAUCHI, T. 1995b. Alkaloidal oviposition stimulants for a danaid butterfly, Ideopsis similis L., from a host plant, Tylophora tanakae (Asclepiadaceae). Experientia 51:753-756.


1713

KELLEY, R. B., SEIBER, J. N., JONES, A. D., SEGALL, H. J., and BROWER, L. P. 1987. Pyrralizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico. Experientia 43:943-946. KIM, C. S., NISHIDA, R., ABE, F., YAMAUCHI, T., and FUKAMI, H. 1994. 14-Deoxyparsonsianidine Ak>xide: A pyrrolizidine alkaloid sequestered by the giant danaine butterfly, Idea leuconone. Biosci. Biotech. Biochem. 58:980-981. LOOIE, C. G., GRUE, M. R., and LIDDELL, J. R. 1994. Proton NMR spectroscopy of pyrrolizidine alkaloids. Phytochemistry 37:43-109. NISHIDA, R. 1995a. Oviposition stimulants of swallowtail butterflies, pp. 13-26, in J. M. Scriber, Y. Tsubaki and R. C. Lederhouse (ed.). Swallowtail Butterflies: Their Ecology and Evolutionary Biology. Scientific Publishers, Gainesville. NISHIDA, R. 1995b. Sequestration of plant secondary compounds by butterflies and moths. Chemoecology 6:127-138. NISHIDA, R., KIM, C. S., FUKAMI, H.,andlRiE, R. 1991. Ideamine /V-oxides: Pyrrolizidine alkaloids sequestered by the danaine butterfly, Idea leuconoe. Agric. Biol. Chem. 55:1787-1792. NISHIDA, R., SCHUL/, S., KIM, C. H., FUKAMI, H., KUWAHARA, Y., HONDA, K., and HAYASHI, N. 1996. Male sex pheromone of a giant danaine butterfly, Idea leuconoe. J. Chem. Ecol. 22:949-972. PAPAJ, D. R., FEENy, P., SACHDEV-GUPTA, K., and ROSENBERRY, L. 1992. D-( + )-Pinitol, an oviposition stimulant for the pipevine swallowtail butterfly, Baltux philenor. J. Chem. Ecol. 18:799-815. PLISKE, T. E. 1975. Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids. Environ. Entomol. 4:455-473. RENWICK, J. A. A., and CHEW, F. S. 1994. Oviposition behavior in Lepidoptera. Annu. Rev. Entomol. 39:377-400. ROTHSCHILD, M., and EDGAR, J. A. 1978. Pyrrolizidine alkaloids from Senecio vulgaris sequestered and stored by Danaus plexippus. J. Zool. London 186:347-349. SCHNEIDER, D., BOPPRE, M., SCHNEIDER, H., THOMNPSON, W. R., BORIACK, C. J., PETTY, R. L., and MEINWALD, J. 1975. A pheromone precursor and its uptake in male Danaus butterflies. J. Comp. Physiol. 97:245-256. SCHULZ, S., FRANCKE, W., EDGAR, J., and SCHNEIDER, D. 1988. Volatile compounds from androconial organs of danaine and ithomiine butterflies. Z. Nalurforsch. 43c:99-104. STELUES, M. E., and SEIBER, J. N. 1990. Pyrrolizidine alkaloids in an overwintering population of monarch butterflies (Danaus plexippus) in California. J. Chem. Ecol. 16:1459-1470. TRIGO, J. R., and MOTTA, P. C. 1990. Evolutionary implications of pyrrolizidine alkaloid assimilation by danaine and ithomiine larvae (Lepidoptera: Nymphalidae) Experientia 46:332-334.