echo, a specialist on cycads, sequester the azoxyglycoside, cycasin (Teas, 1967;. Teas et al., 1966); larvae of the milkweed specialist, Cycnia tenera, sequester.
Journal of Chemical Ecology, Vol. 23, No. 12, 1997
FATE OF HOST-PLANT IRIDOID GLYCOSIDES IN LEPIDOPTERAN LARVAE OF NYMPHALIDAE AND ARCTHDAE
M. DEANE BOWERS1,* and NANCY E. STAMP2 1 University
of Colorado Museum and E.P.O. Biology, Campus Box 334 University of Colorado, Boulder, Colorado 80309 2Department of Biological Sciences Binghamton University, State University of New York Binghamton, New York 13902-6000
(Received February 17, 1997; accepted August 14, 1997) Abstract—We compared the ability of larvae of six lepidopteran species to sequester iridoid glycosides. All larvae were fed on a common host plant, Plantago lanceolata, which contains two iridoid glycosides, aucubin and catalpol. Four species of arctiids were examined: Pyrrharctia Isabella, Spilosoma congrua, Spilosoma latipennis, and Spilosoma virginica. For comparison, we also examined two nymphalid species, one of which, Junonia coenia (a specialist on plants containing iridoid glycosides), was known to sequester iridoid glycosides, and the other, Vanessa cardui, was a general 1st that also feeds on P. lanceolata. We found that, as expected, J. coenia larvae did contain iridoid glycosides, whereas V. cardui did not. To our surprise, Spilosoma congrua contained substantial amounts of iridoid glycosides (mean = 7.14% dry weight), whereas none of the other arctiids (S. lalipennis, S. virginica, or P. Isabella) contained detectable levels of iridoid glycosides. We found small amounts of iridoid glycosides in the frass of S. virginica but none in the frass of 5. congrua or P. Isabella. Key Words—Arctiidae, Nymphalidae, iridoid glycosides, sequestration.
INTRODUCTION
Sequestration of plant secondary compounds for use as a defense against potential predators is found in many groups of herbivorous insects, most notably the Lepidoptera, Coleoptera, tenthredinid Hymenoptera, and Hemiptera (Duffey, *To whom correspondence should be addressed. 2955 0098-033l/97/I200-2955$l2.50/0 © 1997 Plenum Publishing Corporation
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1980; Blum, 1981; Brower, 1984; Rothschild, 1985; Bowers, 1992). Most such insects are specialists, feeding on one or a few species of plants from which they acquire their defensive compounds (Bowers, 1988). In contrast, one group of moths, the Arctiidae, are often quite general in their feeding habits (Rothschild, 1985), and yet some species are able to sequester host-plant secondary compounds (Rothschild et al., 1979). The iridoid glycosides are one group of plant secondary compounds that are sequestered by several insect species, most of which are specialists (Bowers, 1991; Rimpler, 1991). In some of these species, such as members of the genus Euphydryas (Bowers, 1991; Rimpler, 1991; Stermitz et al., 1994; Bowers and Williams, 1995), the iridoids are retained through to the adult stage, but in other species, such as the buckeye (Junonia coenia, Nymphalidae), compounds are sequestered and retained only in the larval stage (Bowers and Collinge, 1992). Only one generalist species, the gypsy moth Lymantria dispar (Lymantriidae), has been examined for iridoid glycoside sequestration, and it does not sequester iridoid glycosides, but eliminates them in the frass (Bowers and Puttick, 1986). Because arctiid caterpillars may feed on plants that contain iridoid glycosides (Tietz, 1975; Dethier, 1988, 1989; Covell, 1984), and some species can sequester secondary compounds from their larval host plants (Teas et al., 1966; Teas, 1967; Rothschild et al., 1979; Ehmke et al., 1990; Hesbacher et al., 1995), we tested several species of arctiids for their ability (or lack thereof) to sequester iridoid glycosides. We used four different arctiid species, all of which are generalist feeders that include plant taxa containing iridoid glycosides in their diet (Tietz, 1972; Covell, 1984): Pyrrharctia isabella (J. Smith), Spilosoma virginica (Fab.), Spilosoma latipennis Stretch, and Spilosoma congrua (Wlk.). For comparison with another generalist, we used larvae of the painted lady, Vanessa cardui (L.) (Nymphalidae). For comparison with a specialist, we used Junonia coenia (Hubner), also a nymphalid, which sequesters iridoid glycosides in the larval instars (Bowers and Collinge, 1992). Larvae were fed on a host plant that all of these lepidopteran species had in common, narrow-leafed plantain, Plantago lanceolata (L.) (Plantaginaceae). This plant contains two iridoid glycosides, aucubin and catalpol (Duff et al., 1965; Bowers and Stamp, 1992; Fajer et al., 1992).
METHODS AND MATERIALS
Study Organisms. The buckeye (J. coenia) feeds on plants in four families, Verbenaceae, Scrophulariaceae, Acanthaceae, and Plantaginaceae, all of which contain iridoid glycosides (Bowers, 1984). Two iridoid glycosides, aucubin and catalpol, serve as feeding and oviposition stimulants for buckeyes (Bowers,
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1984; Pereyra and Bowers, 1988). Buckeye larvae sequester aucubin and catalpol (Bowers and Collinge, 1992). The amount of iridoid glycosides that a caterpillar contains depends primarily on the iridoid glycoside content of the host plant (Camara, 1996). Larvae used in these experiments were from a laboratory colony at the University of Colorado that was maintained on leaves of P. lanceolata (Plantaginaceae). The painted lady (V. cardui) is a cosmopolitan butterfly. Painted ladies are generalist feeders that use plants in over 20 families, and P. lanceolata is a common host plant (Scott, 1986; Garrigan, 1994). The caterpillars used in this experiment originated from a colony maintained at Carolina Biological Supply (Burlington, North Carolina). Pyrrharctia Isabella is the common woolly bear, found throughout North America. This species is quite polyphagous in its feeding habits: Shapiro (1968) tested P. Isabella on 95 plant species in 57 different plant families and found that only one of these species did not elicit a feeding response. Plantago lanceolata is a commonly used host plant (Shapiro, 1968). Pyrrharctia Isabella larvae were reared from eggs deposited from female P. Isabella collected at Makonikey, Massachusetts. The three species of Spilosoma are all polyphagous feeders. The feeding behavior of 5. virginica (= Diacrisia virginica) has been studied in some detail (Dethier, 1988), but that of the other two species (S. congrua and 5. latipennis) has not. All three of these species are considered to be quite polyphagous (Tietz, 1972; Covell, 1984). Spilosoma virginica were obtained from a single female collected in Storrs, Connecticut; S. latipennis larvae were reared from eggs deposited by females collected in Storrs, Connecticut; S. congrua were reared from eggs obtained from a females collected on Martha's Vineyard, Massachusetts. All of these species will feed on P. lanceolata (Tietz, 1972; Covell, 1984; Bowers, personal observation). The iridoid glycoside content of P. lanceolata varies between individual plants and between leaves on an individual plant (Bowers and Stamp, 1992, 1993). The content varies from undetectable in the oldest leaves to as much as 12% in the youngest leaves (Bowers and Stamp, 1992; Bowers et al. 1992; Klockars, et al., 1993). We did not quantify the concentration of iridoid glycosides in the plant material that we fed to the caterpillars in this study. Feeding Experiments. Because the rearing conditions differed somewhat for each species, depending on when the eggs were obtained, the specifics are described for each species. All larvae were reared in the laboratory in Boulder, Colorado, on Plantago lanceolata obtained from plants growing in Boulder; except for P. Isabella larvae, which were reared in Binghamton, New York, on P. lanceolata collected there. Junonia coenia were reared in the laboratory at 25 °C day: 20°C night, with
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a photoperiod of 14 hr light. Larvae were reared in plastic Petri dishes (2.5 X 14.5 cm) from hatching until they had just molted to the fifth instar, but had not fed. Larvae were frozen and freeze-dried for chemical analysis. Vanessa cardui larvae were reared on leaves of P. lanceolata from the second instar until they molted to the fifth instar. For the first instar, these larvae were reared on artificial diet obtained from Carolina Biological Supply. This diet contains ground leaf material of another host plant, mallow (Malva sp., Malvaceae). Although V. cardui larvae will feed and oviposit on P. lanceolata in nature (Scott, 1986; Garrigan, 1994), mortality of first instars was very high when larvae were reared on P. lanceolata. Frass was collected from each larva during the fourth instar, frozen, and freeze-dried. Spilosma congrua and 5. virginica larvae were reared in monospecific groups on leaves of P. lanceolata until the third instar, when 15 third instars were placed individually into large Petri dishes (2.5 X 14.5 cm). Larvae were allowed to feed until they had just molted to the fifth instar; at which time each larva was frozen and freeze-dried. Frass was collected from each 5. virginica larva during the fourth instar, frozen, and freeze-dried. Frass from S. congrua was collected from a separate set of larvae during the fifth instar. This allowed us to examine both larval tissue and frass for the presence or absence of iridoid glycosides. Spilosoma latipennis larvae were reared individually in Petri dishes under the same conditions as the other larvae. As larvae got ready to molt to the fifth instar, they were isolated without food, and after the molt they were frozen and freeze-dried. We used two different sets of P. isabella larvae. The first set of larvae was reared under the conditions described above for the Spilosoma species. These larvae were isolated from food as they were about to molt to the fifth instar and were frozen after they had molted. A second set of larvae was collected from a laboratory experiment in which actively feeding fifth instars were killed, their gut dissected out, and the remainder freeze-dried for chemical analysis. Chemical Analyses, Larvae and frass samples were analyzed for aucubin and catalpol content by gas chromatography (Gardner and Stermitz, 1988; Bowers and Collinge, 1992). Briefly, freeze-dried samples were ground to a fine powder, the powder weighed, extracted overnight in 5 ml methanol, filtered, and the filtrate evaporated to dryness. The residue was taken up in water and partitioned with ether to remove lipophilic substances. The water fraction, containing sugars and iridoid glycosides, was evaporated, the residue taken up in 1 ml methanol, an aliquot of 0.10 ml transfered to a small tube, and the methanol evaporated. Tri-sil Z (Pierce Chemical Company, Rockford, Illinois) was used to derivatize the iridoid glycosides prior to injection on the gas chromatograph.
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RESULTS
Newly molted, fifth instar J. coenia contained relatively large amounts of iridoid glycosides, over 20% dry weight (Table 1). The ratio of aucubin to catalpol was approximately 4:1. Vanessa cardui, a generalise nymphalid, did not contain detectable amounts of iridoid glycosides, nor did the frass (Table 1); suggesting that the ingested iridoid glycosides were metabolized by the larvae. To our surprise, we found that Spilosoma congrua larvae sequestered iridoid glycosides, although in amounts less than half those of J. coenia (Table 1). The ratio of aucubin to catalpol (1:2) was quite different in 5. congrua compared to J. coenia. We did not detect any iridoid glycosides in the frass from the S. congrua larvae. Neither S. latipennis, S. virginica, nor P. Isabella contained detectable amounts of iridoid glycosides. Whether P. Isabella were feeding or not, no iridoid glycoides were detected. We did find low levels of iridoid glycosides in the frass from S. virginica, but were unable to sample the frass from S. latipennis or P. isabella.
DISCUSSION In contrast to the other four generalist species tested, S. congrua was able to sequester substantial amounts of iridoid glycosides from P. lanceolata. Indeed, the two congeners of Spilosoma congrua, S. virginica and 5. latipennis, did not contain any detectable iridoid glycosides. These data suggest that, although these arctiids are all relatively polyphagous (Tietz, 1972; Covell, 1984), there are some biochemical features of the gut of 5. congrua that are different from these other taxa. In addition, although S. congrua contained a mean of 8% dry weight iridoid glycosides, this was less than half the amount contained in the specialist, Junonia coenia. This indicates that J. coenia is more efficient than 5. congrua at sequestering iridoid glycosides from its host plant. The ratio of aucubin to catalpol was quite different in J. coenia (4:1) than in S. congrua (1:2). Although we did not measure the aucubin and catalpol content of the plant material we fed to the larvae, in all studies in which we have measured aucubin and catalpol content of P. lanceolata, there is typically two to five times more aucubin than catalpol in the plants (Fajer et al, 1992; Bowers and Stamp, 1993; Adleret ah, 1995; Stamp and Bowers, 1996). If that were the case with the leaves fed to S. congrua, then those larvae are able to selectively sequester catalpol over aucubin. Thus, there may be variation among different sequestering species in the total as well as relative amounts of iridoid glycosides that they are able to store [as has been shown for the monarch, Danaus plexippus, and the queen, Danaus gillippus, and sequestration of cardenolides (Cohen, 1985)].
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Other arctiids have been recorded as sequestering chemical compounds from the plants on which the larvae feed. For example, larvae of Seirarctia echo, a specialist on cycads, sequester the azoxyglycoside, cycasin (Teas, 1967; Teas et al., 1966); larvae of the milkweed specialist, Cycnia tenera, sequester cardenolides from their host plants in the Asclepiadaceae (Cohen and Brower, 1983), and larvae of a third specialist, Tyriajacobaeae, sequester alkaloids from Senecio (Asteraceae) (Aplin et al., 1968; Nickisch-Rosenegk and Wink, 1993). Several other, more polyphagous European species of arctiids reportedly sequester host-plant alkaloids, including Arctia caja and, interestingly, Spilosoma lubricipeda and S. lutea (European species of Spilosoma), Phragmatobia fuliginosa, Diacrisia sannio, and Callimorpha dominula (Rothschild et al., 1979; Nickisch-Rosenegk and Wink, 1993). In Spilosoma lubricipeda, alkaloids were found in pupae reared on Senecio vulgaris at levels of about 120 ^ig per pupa, and in Spilosoma lutea, pupae contained 170-340 /g alkaloid, depending on the host-plant species (Senecio vulgaris or S. jacobaea) (Rothschild et al., 1979). Smaller amounts were found in the adult moths, 17-27 ug per individual. For these European Spilosoma species, however, alkaloids were determined from bulk samples of many individuals, rather than by analyzing each individual separately, thus there is no information available about variation in individual levels of alkaloids (Rothschild et al., 1979). In a more recent and more detailed study, last instar Spilosoma lubricipeda were fed a 2-mg dose of the pyrrolizidine alkaloid heliotrine, offered on leaf discs of several different host-plant species (Nickisch-Rosenegk and Wink, 1993). These larvae sequestered 8.2-20.9% of the alkaloid, eliminated 12.0-27.5%, and the remainder (64.3-74.3%) was apparently degraded. Some species of the genus Spilosoma may be especially good at sequestering particular groups of plant allelochemicals, as our data with S. congrua also suggest. Another recent paper reported that the adults of 11 species of lichen-feeding arctiids in five genera (out of a total of 20 species in eight genera that were tested) sequestered lichen allelochemicals (Hesbacher et al., 1995). Interestingly, the data indicated that not all individuals of a particular species contained the compounds in amounts that were detectable by HPLC. In addition, in those arctiid taxa that did contain lichen-derived compounds, the amounts were quite low, on the order of micrograms. In another study (Strohmeyer et al., 1997), buckeyes, painted ladies, and a third species, the tobacco hornworm, Manduca sexta (Sphingidae), were fed artificial diets containing dried, powdered leaves of P. lanceolata. The iridoid glycoside concentration of these diets ranged from 5.63 to 9.21% dry weight (Strohmeyer et al., 1997). In this study, hemolymph was collected from 6-12 individual larvae and pooled for analysis. When analyzed for iridoid glycosides, the pooled hemolymph of painted ladies and tobacco hornworms contained very
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small amounts of iridoid glycosides: painted ladies: 0.43-0.97 ug/*l hemolymph; tomato hornworms: 1.07-1.44 Mg/Ml (Strohmeyer et al., 1997). In contrast, buckeye larvae contained 63.60-69.96 / g / * l hemolymph. These data, combined with our data from the present experiment, suggest that although very small amounts of iridoid glycosides may pass from the gut to the hemolymph in nonsequestering caterpillar species, only certain species, such as J. coenia and 5. congrua, are able to accumulate large amounts of these compounds. In the four studies described above (Rothschild et al., 1979; NickischRosenegk and Wink, 1993; Hesbacher et al., 1995; Strohmeyer et al., 1997), the taxa other than j. coenia that contained detectable amounts of host-plant allelochemicals had relatively very low amounts of those compounds (see also Krasnoff et al., 1987). There may have been such low levels of iridoid glycosides in some of the species that we studied, but they may not have been detectable under the conditions that we were using for chromatographic analysis. In such cases, although very small amounts of host-plant compounds may pass through the gut wall, and thus considered to be sequestered (Duffey 1980), it is unlikely such low levels of these compounds will have strong antipredator effects. The differences in the amount of iridoid glycosides sequestered by larvae of J. coenia and S. congrua could affect their interaction with potential predators. Although the concentrations of iridoid glycosides in these larvae may be enough to deter certain predators, such as ants (Dyer and Bowers, 1996), other predators, such as wasps and stinkbugs may not be deterred initially (Stamp, 1992). Furthermore, the effect of iridoid glycosides may depend on the amount that an individual caterpillar contains (Dyer and Bowers, 1996), and we did detect variation among individual caterpillars within a species (Table 1). In addition, the amount of chemical defense may be only one part of what determines whether a prey item is discovered and eaten. For example, in a field experiment, J. coenia were four times more likely to be killed by predatory wasps than 5. congrua, apparently because the J. coenia were much more apparent on their host plants (Stamp, 1992). However, over time, the wasps learned to avoid J. coenia, thus predation rates declined on these caterpillars; while predation rates on S. congrua were low but did not decline over time (Stamp, 1992). Spilosoma congrua larvae were much more cryptic in their behavior, and this behavior, combined with some degree of chemical defense, afforded them as much protection as the more apparent, yet better chemically defended J. coenia larvae. Thus, it is the entire defensive repertoire of a caterpillar and its effectiveness in protecting that individual (including behavioral as well as chemical defenses) that determines the ultimate fate of a potential caterpillar prey. Acknowledgments—We thank T. Alexander, S. Denton, L. Dyer, and L. Van Stelten for help with rearing and preparation of samples for chemical analysis. This work was supported by National Science Foundation grants DEB-9306644 to M.D.B. and DEB-9306795 to N.E.S.
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REFERENCES ADLER, L. S., SCHMITT, J. A., and BOWERS, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolate (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75-85. APLIN, R. T., BENN, H. M., and ROTHSCHILD, M. 1968. Poisonous alkaloids in the body tissues of the cinnabar moth (Callimorpha jacobaeae L.). Nature 219:747. BLUM, M. 1981. Chemical Defenses of Arthropods. Academic Press, New York. BOWERS, M. D. 1984. Iridoid glycosides and hostplant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567-1577. BOWERS, M. D. 1988. Chemistry and coevolution: Iridoid glycosides, plants and herbivorous insects, pp. 133-165, in K. Spencer (ed.). Chemical Mediation of Coevolution. Academic Press, New York. BOWERS, M. D. 1991. Iridoid glycosides, pp. 297-325, in G. Rosenthal and M. Berenbaum (eds.). Herbivores: Their Interactions with Plant Secondary Metabolites, Vol. 1, 2nd ed. Academic Press, Orlando, Florida. BOWERS, M. D. 1992. Evolution of unpalatability and the cost of chemical defense in insects, pp. 216-244, in B. D. Roitberg and M. B. Isman (eds.). Insect Chemical Ecology: An Evolutionary Approach. Chapman and Hall, New York. BOWERS, M. D., and COLLINGE, S. K. 1992. Fate of iridoid glycosides in different stages of the buckeye, Junonia coenia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 18:817-831. BOWERS, M. D., and PUTTICK, G. P. 1986. The fate of ingested iridoid glycosides in lepidopteran herbivores. J. Chem. Ecol. 12:169-178. BOWERS, M. D., and STAMP, N. E. 1992. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J. Chem. Ecol. 18:989-995. BOWERS, M. D., and STAMP, N. E. 1993. Effects of plant age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778-1791. BOWERS, M. D. and WILLIAMS, E. 1995. Variable chemical defence in the checkerspot butterfly Euphydryas gillettii (Lepidoptera: Nymphalidae). Ecol. Entomol. 20:208-212. BOWERS, M. D., COLLINOE, S. K., GAMBLE, S., and SCHMITT, J. 1992. Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91:201-207. BROWER, L. P. 1984. Chemical defense in butterflies, pp. 109-134, in R. I. Vane-Wright and P. R. Ackery (eds.). The Biology of Butterflies. Symposium of the Royal Entomology Society, Number 11. Academic Press, New York. CAMARA, M. D. 1996. Diet breadth in Junonia coenia: The costs and benefits of sequesting plant secondary metabolites for chemical defense. PhD dissertation. University of Colorado, Boulder. COHEN, J. A. 1985. Differences and similarities in cardenolide contents of queen and monarch butterflies in Florida and their ecological and evolutionary implications. J. Chem. Ecol. 11:85-103. COHEN, J. A., and BROWER, L. P. 1983. Cardenolide sequestration by the dogbane tiger moth (Cycnia tenera; Arctiidae). J. Chem. Ecol. 9:521-532. COVELL, C. 1984. A Field Guide to the Moths of Eastern North America. Houghton Miffin, Boston. DETHIER, V. G. 1988. The feeding behavior of a polyphagous caterpillar (Diacrisia virginica) in its natural habitat. Can. J. Zool. 66:1280-1288. DETHIER, V. G. 1989. Patterns of locomotion of polyphagous arctiid caterpillars. Ecol, Entomol. 14:375-386. DUFF, R. B., BACON, J. S. D., MUNDIE, C. M., FAMER, V. C., RUSSELL, J. D., and FORRESTER, A. R. 1965. Catalpol and methyl catalpol: Naturally occurring glycosides in Plantago and Buddleia species. Biochem. J. 96:1-5.
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DUFFEY, S. S. 1980. Sequestration of plant natural products by insects. Annu. Rev. Entomol. 25:447-477. DYER, L. A., and BOWERS, M. D. 1996. The importance of sequestered iridoid glycosides as a defense against an ant predator. J. Chem. Ecol. 22:1527-1539. EHMKE, A., WITTE, L., BILLER, A., and HARTMANN, T. 1990. Sequestration, W-oxidation and transformation of plant pyrrolizidine alkaloids by the arctiid moth Tyria jacobaeae L. Z. Naturforsch. 45c: 1185-1192. FAJER, E. D., BOWERS, M. D., and BAZZAZ, F. A. 1992. The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: A test of the carbon/ nutrient balance hypothesis. Am. Nat. 140:707-723. GARDNER, D. R., and STERMITZ, F. R. 1988. Hostplant utilization and iridoid glycoside sequestration by Euphydryas anicia individuals and populations. J. Chem. Ecol. 15:2147-2168. GARRIGAN, D. 1994. Host selection by Vanessa cardul butterflies: The ecology and evolution of diet breadth. PhD dissertation. University of Utah, Logan. HESBACHER, S., GIEZ, I., EMBACHER, G., FIEDLER, K., MAX, W., TRAWOOER, A., TURK, R., LANCE, O. L., and PROKSCH, P. 1995. Sequestration of lichen compounds by lichen-feeding members of the Arctiidae (Lepidoptera). J. Chem. Ecol. 21:2079-2089. KLOCKARS, G., BOWERS, M. D., and COONEY, B. 1993. Leaf variation in iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and oviposition of the buckeye, Junonia coenia (Nymphalidae). Chemoecology 4:72-78. KRASNOFF, S. B., BJOSTAD, L. B., and ROELOFS, W. L. 1987. Quantitative and qualitative variation in male pheromones of Phragmatobia fuliginosa and Pyrrharctia isabella (Lepidoptera: Arctiidae). J. Chem. Ecol. 13:807-822. NICKISCH-ROSENEGK, E. V., and WINK, M. 1993. Sequestration of pyrrolizidine alkaloids in several arctiid moths (Lepidoptera: Arctiidae). J. Chem. Ecol. 19:1889-1903. PEREYRA, P. C., and BOWERS, M. D. 1988. Iridoid glycosides as oviposition stimulants for the budkeye, Junonia coenia (Nymphalidae). J. Chem. Ecol. 14:917-928. RIMPLER, H. 1991. Sequestration of iridoids by insects, pp. 314-330, in J. B. Harborne and F. A. Thomas Barberan (eds.). Ecological Chemistry and Biochemistry of Plant Terpenoids. Clarendon Press, Oxford, England. ROTHSCHILD, M. 1985. British aposematic Lepidoptera, pp. 9-62, in J. Heath and A. M. Emmet (eds.). The Moths and Butterflies of Great Britain and Ireland. Harley Books, Essex, England. ROTHSCHILD, M., APLIN, R. T., COCKRUM, P. A., EDGAR, J. A., FAIRWEATHER, P., and LEES, R. 1979. Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of the secondary plant substances in the Arctiidae. Biol. J. Linn. Soc. 12:305-326. SCOTT, J. 1986. The Butterflies of North America. Stanford University Press, Stanford, California. SHAPIRO, A. 1968. Laboratory feeding preferences of the banded wollybear, Isia Isabella. Ann. Entomol. Soc. Am. 61:1221-1224. STAMP, N. E. 1992. Relative susceptibility to predation of two species of caterpillar on plantain. Oecologia 92:124-129. STAMP, N. E., and BOWERS, M. D. 1996. Consequences for hostplant chemistry and growth of plantain (Plantago lanceolata) when herbivores are attacked by predatory wasps and stinkbugs. Ecology 77:535-549. STERMITZ, F. R., ABDEL-KADER, M. S., and POMEROY, M. 1994. Iridoid glycosides from some butterflies and their larval foodplants. Phytochemistry 37:997-1001. STROHMEYER, H. H., STAMP, N. E., JARZOMSKI, C. M., and BOWERS, M. D. 1997. Effects of prey species and prey diet on two invertebrate predators, stinkbugs and jumping spiders. Ecol. Entomol. In press.
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TEAS, H. J. 1967. Cycasin synthesis in Seirarctia echo (Lepidoptera) larvae fed methylazoxymethanol. Biochem. Biophys. Res. Commun. 26:686-690. TEAS, H. J., DYSON, J. G., and WHISENANT, B. R. 1966. Cycasin metabolism in Seirarctia echo Abbot and Smith (Lepidoptera: Arctiidae). J. Ga. Entomol. Soc. 1:21-22. TIETZ, H. M. 1972. An Index to the Described Life Histories, Early Stages and Hosts of the Macrolepidoptera of the Continental United States and Canada. Allyn Museum, Sarasota, Florida.
