Arthropod-Plant Interactions

, Volume 13, Issue 6, pp 835–852 | Cite as

Does chemistry make a difference? Milkweed butterfly sequestered cardenolides as a defense against parasitoid wasps

  • Carl M. StenoienEmail author
  • Rebecca A. Meyer
  • Kelly R. Nail
  • Myron P. Zalucki
  • Karen S. Oberhauser
Original Paper


Plant allelochemicals have important roles in plant defense as well as ecological and co-evolutionary dynamics within tri-trophic systems of plants, herbivores, and natural enemies. Milkweed butterflies represent a model system for chemical ecology because they sequester cardenolides semi-proportionally to the concentration in their host plants, yet little is known about the role of sequestered cardenolides in interactions with invertebrate natural enemies. We experimentally tested the preference and performance of two species of parasitic wasps (Pteromalus cassotis Walker and Pteromalus puparum Linnaeus) on milkweed butterfly pupae (monarchs, Danaus plexippus Linnaeus, and Euploea core Cramer) reared on plants to contain variable concentrations of sequestered cardenolides. We measured host survival and parasitoid reproductive success to determine whether greater concentrations of herbivore-sequestered plant toxins provide a defensive benefit or influence parasitoid success. We found that P. puparum was unable to develop from monarchs, regardless of toxicity. Monarchs containing more cardenolides (those fed Asclepias curassavica) were more likely to survive encounters with P. cassotis than those containing fewer cardenolides (fed Asclepias incarnata), but only because this parasitoid was less likely to attack more toxic monarchs. Once attacked, host toxicity had no effect on the likelihood of monarch survival nor the emergence of parasitoids. Host toxicity affected parasitoid performance in more subtle ways, however, decreasing P. cassotis brood size and survival to adulthood. When attacking cardenolide-free E. core pupae, P. cassotis reproduced successfully, but P. puparum did not, suggesting that milkweed butterflies may employ other defenses against parasitoids, perhaps in addition to cardenolides.


Danainae Pteromalidae Apocynaceae Tri-trophic interaction Pupal parasitoid Monarch butterfly 



We would like to thank Stephen Malcolm for assistance in analyzing cardenolide contents of monarch pupae, as well as Ross Kendall, who reared and shipped butterflies from Australia. Several undergraduate research assistants contributed to this research, including Laura Lukens, Dane Elmquist, Lauren Henrich, Sophia Crosby, Andrea Gruver, Joseph Miller, Jonathan Lundquist, Peter Xiong, Giulia DeLuca, Rachel Quaday, Bradley Kelley, and Sylvia Durkin. We would also like to thank Emilie Snell-Rood, George Heimpel, Marlene Zuk, Saskya van Nouhuys, and multiple anonymous reviewers for constructive comments on earlier versions of this manuscript. This research was financially supported by University of Minnesota Richard and Judi Huempfner Fellowship and the Dayton Fund of the Bell Museum of Natural History. C.S. and K.R.N. were supported by National Science Foundation Fellowships (BCS-0003920) and University of Minnesota Doctoral Dissertation Fellowships.

Supplementary material

11829_2019_9719_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)


  1. Abram PK, Brodeur J, Burte V, Boivin G (2016) Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biol Control 98:52–60Google Scholar
  2. Abram PK, Brodeur J, Urbaneja A, Tena A (2018) Nonreproductive effects of insect parasitoids on their hosts. Annu Rev Entomol 64:259–276PubMedGoogle Scholar
  3. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant–herbivore interactions. New Phytol 194:28–45PubMedGoogle Scholar
  4. Asplen MK, Bruns E, David AS, Denison RF, Epstein B, Kaiser MC, Kaser JM, Lacroix C, Mohl EK, Quiram G, Prescott K, Stanton-Geddes J, Vincent JB, Wragg PD, May G (2012) Do trade-offs have explanatory power for the evolution of organismal interactions? Evolution 66:1297–1307PubMedGoogle Scholar
  5. Barbosa P, Saunders JA, Kemper J, Trumbule R, Olechno J, Martinat P (1986) Plant allelochemicals and insect parasitoids effects of nicotine on Cotesia congregata (say) (Hymenoptera: Braconidae) and Hyposoter annulipes (Cresson) (Hymenoptera: Ichneumonidae). J Chem Ecol 12:1319–1328PubMedGoogle Scholar
  6. Barbosa P, Gross P, Kemper J (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72:1567–1575Google Scholar
  7. Barron MC, Barlow ND, Wratten SD (2003) Non-target parasitism of the endemic New Zealand red admiral butterfly (Bassaris gonerilla) by the introduced biological control agent Pteromalus puparum. Biol Control 27:329–335Google Scholar
  8. Batalden RV, Oberhauser KS (2015) Potential changes in eastern North American monarch migration in response to an introduced milkweed, Asclepias curassavica. In: Oberhause KS, Nail KR, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell University Press, Ithaca, pp 215–224Google Scholar
  9. Benson J, van Driesche R, Pasquale A, Elkinton J (2003) Introduced braconid parasitoids and range reduction of a native butterfly in New England. Biol Control 28:197–213Google Scholar
  10. Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892Google Scholar
  11. Berryman AA, Hawkins BA (2006) The refuge as an integrating concept in ecology and evolution. Oikos 115:192–196Google Scholar
  12. Blum MS (1981) Chemical defenses of arthropods. Academic Press, New YorkGoogle Scholar
  13. Brower LP (1984) Chemical defence in butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic Press, London, pp 109–134Google Scholar
  14. Brower LP, Fink LS (1985) A natural toxic defense system: cardenolides in butterflies versus birds. Ann N Y Acad Sci 443:171–188PubMedGoogle Scholar
  15. Brower LP, Brower JV, Corvino JM (1967) Plant poisons in a terrestrial food chain. Proc Natl Acad Sci USA 57:893–898PubMedGoogle Scholar
  16. Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 161:1349–1350PubMedGoogle Scholar
  17. Burks BD (1975) The species of Chalcidoidea described from North America north of Mexico by Francis Walker (Hymenoptera). Bulletin of the British Museum (Natural History). Entomology 32:139–170Google Scholar
  18. Burks BD (1979) Pteromalidae. In: Krombein KV, Hurd PD, Smith DR, Burks BD (eds) Catalog of hymenoptera in America north of Mexico, vol 1. Smithsonian Institute Press, Washington, D.C, pp 768–835Google Scholar
  19. California Academy of Sciences Entomology General Collection Database (2015) Accessed 24 April 2015
  20. Campbell B, Duffey S (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205:700–702PubMedGoogle Scholar
  21. Campbell B, Duffey S (1981) Alleviation of a-tomatine-induced toxicity to the parasitoid, Hyposoter exiguae, by phytosterols in the diet of the host, Heliothis zea. J Chem Ecol 7:927–946PubMedGoogle Scholar
  22. Couture JJ, Servi JS, Lindroth RL (2010) Increased nitrogen availability influences predator-prey interactions by altering host-plant quality. Chemoecology 20:277–284Google Scholar
  23. de Roode JC, Pedersen AB, Hunter MD, Altizer S (2008) Host plant species affects virulence in monarch butterfly parasites. J Anim Ecol 77:120–126PubMedGoogle Scholar
  24. Decker LE, de Roode JC, Hunter MD (2018) Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds. Ecol Lett 21:1353–1363PubMedGoogle Scholar
  25. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307PubMedGoogle Scholar
  26. Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution 1:33–54Google Scholar
  27. Dixon CA, Erickson JM, Kellett DN, Rothschild M (1978) Some adaptations between Danaus plexippus and its food plant, with notes on Danaus chrysippus and Euploea core (Insecta: Lepidoptera). J Zool 185:437–467Google Scholar
  28. Dobler S, Petschenka G, Pankoke H (2011) Coping with toxic plant compounds—the insect’s perspective on iridoid glycosides and cardenolides. Phytochemistry 72:1593–1604PubMedGoogle Scholar
  29. Dobler S, Dalla S, Wagschal V, Agrawal AA (2012) Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. Proc Natl Acad Sci USA 109:13040–13045PubMedGoogle Scholar
  30. Dobler S, Petschenka G, Wagschal V, Flacht L (2015) Convergent adaptive evolution—how insects master the challenge of cardiac glycoside-containing host plants. Entomol Exp Appl 157:30–39Google Scholar
  31. Duffey SS (1980) Sequestration of plant natural products by insects. Annu Rev Entomol 25:447–477Google Scholar
  32. Duffey S, Bloem K, Campbell B (1986) Consequences of sequestration of plant natural products in plant-insect-parasitoid interactions. In: Boetel DJ, Eikenbary RD (eds) Interactions of plant resistance and parasitoids and predators of insects. Wiley, Chichester, pp 31–60Google Scholar
  33. Ehrlich P, Raven P (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608Google Scholar
  34. El-Heneidy AH, Barbosa P, Gross P (1988) Influence of dietary nicotine on fall armyworm, Spodoptera frugiperda and its parasitoids, the ichneumonid wasp Hyposoter annulipes. Entomol Exp Appl 46:227–232Google Scholar
  35. Feng Y, Wratten S, Sandhu H, Keller M (2015) Host plants affect the foraging success of two parasitoids that attack light brown apple moth Epiphyas postvittana (Walker)(Lepidoptera: Tortricidae). PLoS ONE 10:e0124773PubMedPubMedCentralGoogle Scholar
  36. Fink LS, Brower LP (1981) Birds can overcome the cardenolide defence of monarch butterflies in Mexico. Nature 291:67–70Google Scholar
  37. Gauld ID, Gaston KJ (1994) The taste of enemy-free space: parasitoids and nasty hosts. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 279–299Google Scholar
  38. Gauld ID, Gaston KJ, Janzen D (1992) Plant allelochemicals, tritrophic interactions and the anomalous diversity of tropical parasitoids: the “nasty” host hypothesis. Oikos 65:353–357Google Scholar
  39. Gillette CP (1888) Parasites on Danais archippus and Anthomyia raphani. Can Entomol 20:133–134Google Scholar
  40. Glendinning JI (1993) Comparative feeding responses of the mice Peromyscus melanotis, P. aztecus, Reithrodontomys sumichrasti, and Microtus mexicanus to overwintering monarch butterflies in Mexico. In: Malcolm SB, Zalucki MP (eds) Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County, Los Angeles, pp 323–333Google Scholar
  41. Gols R, Harvey JA (2009) Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids. Phytochem Rev 8:187–206Google Scholar
  42. Gowler CD, Leon KE, Hunter MD, de Roode JC (2015) Secondary defense chemicals in milkweed reduce parasite infection in monarch butterflies, Danaus plexippus. J Chem Ecol 41:520–523PubMedGoogle Scholar
  43. Halstead JA (1988) First records of Platychalcis in North America and new host records of Ceratosmicra spp. and Brachymeria ovata (Hymenoptera: Chalcididae). Entomol News 99:193–198Google Scholar
  44. Harvey JA, van Nouhuys S, Biere A (2005) Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J Chem Ecol 31:287–302PubMedGoogle Scholar
  45. Harvey JA, Gols R, Wagenaar R, Bezemer MT (2007a) Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense. J Chem Ecol 33:1556–1569PubMedGoogle Scholar
  46. Harvey JA, van Dam NM, Witjes L, Soler R, Gols R (2007b) Effects of dietary nicotine on the development of an insect herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels. Ecol Entomol 32:15–23Google Scholar
  47. Harvey JA, van Dam NM, Raaijmakers CE, Bullock JM, Gols R (2011) Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 166:421–431PubMedGoogle Scholar
  48. Harvey JA, Ximenez de Embun MG, Bukovinszky T, Gols R (2012) The roles of ecological fitting, phylogeny and physiological equivalence in understanding realized and fundamental host ranges in endoparasitoid wasps. J Evol Biol 25:2139–2148PubMedGoogle Scholar
  49. Hawkins BA, Cornell H, Hochberg M (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152Google Scholar
  50. Holzinger F, Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+ , K + -ATPase. J Chem Ecol 22:1921–1937PubMedGoogle Scholar
  51. Hunter MD, Malcolm SB, Hartley SE (1996) Population-level variation in plant secondary chemistry, and the population biology of herbivores. Chemoecology 7:45–56Google Scholar
  52. Jackman S (2015) pscl: classes and methods for R developed in the political science computational laboratory, Stanford University. Department of Political Science, Stanford University. Stanford, California. R package version 1.4.9.
  53. Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286Google Scholar
  54. Ladner DT, Altizer S (2005) Oviposition preference and larval performance of North American monarch butterflies on four Asclepias species. Entomol Exp Appl 116:9–20Google Scholar
  55. Lampert EC, Zangerl AR, Berenbaum MR, Ode PJ (2011) Generalist and specialist host–parasitoid associations respond differently to wild parsnip (Pastinaca sativa) defensive chemistry. Ecol Entomol 36:52–61Google Scholar
  56. Lasota J, Kok L (1986) Parasitism and utilization of imported cabbageworm pupae by Pteromalus puparum (Hymenoptera: Pteromalidae). Environ Entomol 15:994–998Google Scholar
  57. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33Google Scholar
  58. Levins R (1968) Evolution in changing environments. Princeton University Press, PrincetonGoogle Scholar
  59. Malcolm SB (1990) Chemical defence in chewing and sucking insect herbivores: plant-derived cardenolides in the monarch butterfly and oleander aphid. Chemoecology 1:12–21Google Scholar
  60. Malcolm SB (1991) Cardenolide-mediated interactions between plants and herbivores. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, vol I. The chemical participants. Academic Press Inc, New York, pp 251–296Google Scholar
  61. Malcolm SB (1995) Milkweeds, monarch butterflies and the ecological significance of cardenolides. Chemoecology 5:101–117Google Scholar
  62. Malcolm SB, Rothschild M (1983) A danaid mullerian mimic, Euploea core amymone (Cramer) lacking cardenolides in the pupal and adult stages. Biol J Linn Soc 27:27–33Google Scholar
  63. Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol Exp Appl 80:193–196Google Scholar
  64. MacArthur RH, Connell JH (1966) The biology of populations. Wiley, New YorkGoogle Scholar
  65. Milonas PG (2005) Influence of initial egg density and host size on the development of the gregarious parasitoid Bracon hebetor on three different host species. Biocontrol 50:415–428Google Scholar
  66. Moss J (1933) The natural control of the cabbage caterpillars, Pieris spp. J Anim Ecol 2:210–231Google Scholar
  67. Muesebeck C, Krombein K, Townes H (1951) Hymenoptera of America North of Mexico, US Dep Agric Monogr, 2:809–810Google Scholar
  68. Mullahy J (1986) Specification and testing of some modified count data models. J Econ 33:341–365Google Scholar
  69. Murphy SM, Lill JT, Bowers MD, Singer MS (2014) Enemy-free space for parasitoids. Environ Entomol 43:1465–1474PubMedGoogle Scholar
  70. (MLMP) (2018) Monarch Larva Monitoring Project. Accessed 17 December 2018
  71. Nail KR, Stenoien CM, Oberhauser KS (2015) Immature monarch survival: effects of site characteristics, density, and time. Ann Entomol Soc Am 108:680–690Google Scholar
  72. Nelson CJ (1993) Sequestration and storage of cardenolides and cardenolide glycosides by Danaus plexippus plexippus and D. chrysippus petilia when reared on Asclepias fruticosa: with a review of some factors that influence sequestration. In: Malcolm SB, Zalucki MP (eds) Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County, Los Angeles, pp 91–105Google Scholar
  73. Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92PubMedGoogle Scholar
  74. Noyes JS (2017) Universal Chalcidoidea Database. Accessed 8 June 2017
  75. Oberhauser KS, Anderson M, Anderson S, Caldwell W, De Anda A, Hunter M, Kaiser MC, Solensky MJ (2015) Lacewings, wasps, and flies—oh my: insect enemies take a bite out of monarchs. In: Oberhauser KS, Nail KR, Altizer S (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell University Press, Ithaca, pp 71–82Google Scholar
  76. Oberhauser KS, Elmquist D, Perilla-López JM, Gebhard I, Lukens L, Stireman J (2017) Tachinid fly (Diptera: Tachinidae) parasitoids of Danaus plexippus (Lepidoptera: Nymphalidae). Ann Entomol Soc Am 110:536–543Google Scholar
  77. Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185PubMedGoogle Scholar
  78. Ode PJ (2013) Plant defences and parasitoid chemical ecology. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Chichester, pp 9–36Google Scholar
  79. Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154Google Scholar
  80. Parsons J (1965) A digitalis-like toxin in the monarch butterfly, Danaus plexippus L. J Physiol 178:290–304PubMedPubMedCentralGoogle Scholar
  81. Peck O (1963) A Catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). Mem Entomol Soc Can 95(S30):5–1092. CrossRefGoogle Scholar
  82. Petschenka G, Agrawal AA (2015) Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc R Soc Lond B. CrossRefGoogle Scholar
  83. Pocius VM, Debinski DM, Pleasants JM, Bidne KG, Hellmich RL (2018) Monarch butterflies do not place all of their eggs in one basket: oviposition on nine Midwestern milkweed species. Ecosphere 9:e02064. CrossRefGoogle Scholar
  84. Price PW, Bouton C, Gross P (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65Google Scholar
  85. Prysby MD (2004) Natural enemies and survival of monarch eggs and larvae. In: Oberhauser KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 27–37Google Scholar
  86. R Core Team, version 3.3.3 (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  87. Rafter JL, Agrawal AA, Preisser EL (2013) Chinese mantids gut toxic monarch caterpillars: avoidance of prey defence? Ecol Entomol 38:76–82Google Scholar
  88. Rafter JL, Gonda-King L, Niesen D, Seeram NP, Rigsby CM, Preisser EL (2017) Impact of consuming ‘toxic’ monarch caterpillars on adult chinese mantid mass gain and fecundity. Insects 8:23PubMedCentralGoogle Scholar
  89. Rahman H, Zalucki MP, Scheermeyer E (1985) Effect of host plant on the development and survival of the immature stages of Euploea core corinna (Lepidoptera: Nymphalidae). J Aust Entomol Soc 24:95–98Google Scholar
  90. Ramsay G (1964) Overwintering swarms of the monarch butterfly (Danaus plexippus (L.)) in New Zealand. N Z Entomol 3:10–16Google Scholar
  91. Rayor LS (2004) Effects of monarch larval host plant chemistry and body size on Polistes wasp predation. In: Oberhause KS, Solensky MJ (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 39–46Google Scholar
  92. Reudler JH, van Nouhuys S (2018) The roles of foraging environment, host species, and host diet for a generalist pupal parasitoid. Entomol Exp Appl 166:251–264Google Scholar
  93. Reudler JH, Biere A, Harvey JA, van Nouhuys S (2011) Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata. J Chem Ecol 37:765–778PubMedPubMedCentralGoogle Scholar
  94. Roeske CN, Seiber JN, Brower LP, Moffitt CM (1976) Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexippus L.). Recent Adv Phytochem 10:93–167Google Scholar
  95. Rothschild M, Gardiner B, Mummery R (1978) The role of carotenoids in the “golden glance” of danaid pupae (Insecta: Lepidoptera). J Zool 186:351–358Google Scholar
  96. Rowell-Rahier M, Pasteels JM (1992) Third trophic level influences of plant allelochemicals. In: Rosenthal GA, Berenbaum (eds) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes, vol II, 2nd edn. Academic Press, Inc, San Diego, pp 243–279Google Scholar
  97. Semmens BX, Semmens DJ, Thogmartin WE, Wiederholt R, López-Hoffman L, Diffendorfer JE, Pleasants JM, Oberhauser KS, Taylor OR (2016) Quasi-extinction risk and population targets for the eastern, migratory population of monarch butterflies (Danaus plexippus). Sci Rep 6:23265PubMedPubMedCentralGoogle Scholar
  98. Stenoien CM, McCoshum S, Oberhauser KS, Caldwell W, De Anda A (2015) New reports that monarch butterflies (Lepdiotera: Nymphalidae, Danaus plexippus Linnaeus) serve as hosts for a pupal parasitoid (Hymenoptera: Chalcidoidae, Pteromalus cassotis Walker) in the Eastern United States. J Kansas Entomol Soc 88:16–26Google Scholar
  99. Stenoien CM, Nail KR, Zalucki JM, Parry H, Oberhauser KS, Zalucki MP (2016) Monarchs in decline: a collateral landscape-level effect of modern agriculture. Insect Sci. CrossRefPubMedGoogle Scholar
  100. Stireman JO, Singer M (2003) What determines host range in parasitoids? An analysis of a tachinid parasitoid community. Oecologia 135:629–638PubMedGoogle Scholar
  101. Tao L, Hoang KM, Hunter MD, de Roode JC (2016) Fitness costs of animal medication: antiparasitic plant chemicals reduce fitness of monarch butterfly hosts. J Anim Ecol 85:1246–1254PubMedGoogle Scholar
  102. Wiegrebe H, Wichtl M (1993) High-performance liquid chromatographic determination of cardenolides in Digitalis leaves after solid-phase extraction. J Chromatogr 630:402–407PubMedGoogle Scholar
  103. Wilson DD, Yoshimura J (1994) On the coexistence of specialists and generalists. Am Nat 144:692–707Google Scholar
  104. Zalucki MP, Freebairn C (1982) An additional parasitoid for Danaus plexippus L. News Bull Entomol Soc Qld 10:68Google Scholar
  105. Zalucki MP, Kitching R (1982) Temporal and spatial variation of mortality in field populations of Danaus plexippus L. and D. chrysippus L. larvae (Lepidoptera: Nymphalidae). Oecologia 53:201–207PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Ecology, Evolution, and BehaviorUniversity of MinnesotaSaint PaulUSA
  2. 2.Conservation Biology Graduate ProgramUniversity of MinnesotaSaint PaulUSA
  3. 3.School of Biological SciencesThe University of QueenslandBrisbaneAustralia
  4. 4.University of Wisconsin Madison Arboretum, University of WisconsinMadisonUSA

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