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Journal of Chemical Ecology

, Volume 41, Issue 7, pp 662–669 | Cite as

Southern Monarchs do not Develop Learned Preferences for Flowers With Pyrrolizidine Alkaloids

  • Marina Vasconcelos de Oliveira
  • José Roberto Trigo
  • Daniela Rodrigues
Article

Abstract

Danaus butterflies sequester pyrrolizidine alkaloids (PAs) from nectar and leaves of various plant species for defense and reproduction. We tested the hypothesis that the southern monarch butterfly Danaus erippus shows innate preferences for certain flower colors and has the capacity to develop learned preferences for artificial flowers presenting advantageous floral rewards such as PAs. We predicted that orange and yellow flowers would be innately preferred by southern monarchs. Another prediction is that flowers with both sucrose and PAs would be preferred over those having sucrose only, regardless of flower color. In nature, males of Danaus generally visit PA sources more often than females, so we expected that males of D. erippus would exhibit a stronger learned preference for PA sources than the females. In the innate preference tests, adults were offered artificial non-rewarding yellow, orange, blue, red, green, and violet flowers. Orange and yellow artificial flowers were most visited by southern monarchs, followed by blue and red ones. No individual visited either green or violet flowers. For assessing learned preferences for PA flowers over flowers with no PAs, southern monarchs were trained to associate orange flowers with sucrose plus the PA monocrotaline vs. yellow flowers with sucrose only; the opposite combination was used to train another set of butterflies. In the tests, empty flowers were offered to trained butterflies. Neither males nor females showed learned preferences for flower colors associated with PAs in the training set. Thus, southern monarchs resemble the sister species Danaus plexippus in their innate preferences for orange and yellow flowers. Southern monarchs, similarly to temperate monarchs, might not be as PA-demanding as are other danaine species.

Keywords

Visual signals Flower visitors Insect cognition Danaini Nectar Dihydropyrrolizines Sex pheromones Chemical defense Monocrotaline 

Notes

Acknowledgments

We thank Bruna C.M. Ramos for assistance with data analysis and use of the R environment. We also are grateful to Leonice Coelho at the Departamento de Química Inorgânica / IQ / UFRJ for measuring the reflectance of the colored artificial flowers and the background. Pedro Paulo Ferreira, Lucy de Oliveira, and João Paulo Monteiro helped us in the laboratory, and Ricardo and Margarete Monteiro provided space to perform some trials. Leandro Freitas, Angela Sanseverino, John I. Glendinning, Steve Malcolm, Janet W. Reid and one anonymous reviewer critically read previous drafts of the manuscript. MVO was funded by a FAPERJ senior student scholarship (grant 100.889/2013). JRT is grateful for grants from FAPESP (2011/17708-0) and CNPq (306103/2013-3). DR was supported by grants from CNPq (480264/2010-4) and FAPERJ (110.726/2013).

References

  1. Ackery PR, Vane-Wright RI (1984) Milkweed butterflies: their cladistics and biology. Cornell University Press, IthacaGoogle Scholar
  2. Agrawal A, Petschenka G, Bingham R, Weber M, Rasmann S (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45PubMedCrossRefGoogle Scholar
  3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  4. Barth FG (1991) Insects and flowers: the biology of a partnership. Princeton University Press, PrincetonGoogle Scholar
  5. Beccaloni GW, Viloria AL, Hall KS, Robinson GS (2008) Catalogue of the hostplants of the Neotropical butterflies. The Natural History Museum, LondonGoogle Scholar
  6. Blackiston DJ, Brisoce AD, Weiss MR (2011) Color vision and learning in the monarch butterfly, Danaus plexippus (Lepidoptera). J Exp Biol 214:509–520PubMedCrossRefGoogle Scholar
  7. Boppré M (1978) Chemical communication, plant relationships, and mimicry in the evolution of danaid butterflies. Entomol Exp Appl 24:64–77CrossRefGoogle Scholar
  8. Boppré M (1983) Leaf scratching – a specialized behavior of danaine butterflies (Lepidoptera) for gathering secondary plant substances. Oecologia 59:414–416CrossRefGoogle Scholar
  9. Boppré M (1984) Redefining “phamacophagy”. J Chem Ecol 10:1151–1154PubMedCrossRefGoogle Scholar
  10. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510PubMedCrossRefGoogle Scholar
  11. Brower AVZ, Jeansonne MM (2004) Geographical population and “subspecies” of New world monarch butterflies (Nymphalidae) share a recent origin and are not phylogenetically distinct. Ann Entomol Soc Am 97:519–523CrossRefGoogle Scholar
  12. Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 161:1349–1351PubMedCrossRefGoogle Scholar
  13. Brower AVZ, Wahlberg N, Ogawa JR, Boppré M, Vane-Wright RI (2010) Phylogenetic relationships among genera of Danainae butterflies (Lepidoptera: Nymphalidae) as implied by morphology and DNA sequences. Syst Biodivers 8:75–89CrossRefGoogle Scholar
  14. Brown KS (1984) Chemical ecology of dehydropyrrolizidine alkaloids in adult Ithominae (Lepidoptera: Nymphalidae). Rev Bras Biol 44:435–460Google Scholar
  15. Brown KS, Trigo JR, Francini RB, Morais ABB, Motta PC (1991) Aposematic insects on toxic host plants: coevolution, colonization, and chemical emancipation. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 375–402Google Scholar
  16. Chittka L, Spaethe J, Schmidt A, Hickelsberger A (2001) Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination: animal behavior and evolution. Cambridge University Press, Cambridge, pp 106–126CrossRefGoogle Scholar
  17. Crawley MJ (2013) The R book, 2nd edn. Wiley, ChichesterGoogle Scholar
  18. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  19. Dingemanse NJ, Wolf M (2013) Between – individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039CrossRefGoogle Scholar
  20. Edgar JA, Cockrum PA, Frahn JL (1976) Pyrrolizidine alkaloids in Danaus plexippus L. and Danaus chrysippus L. Experientia 32:1535–1537CrossRefGoogle Scholar
  21. Flores AS, Tozzi AMGA, Trigo JR (2009) Pyrrolizidine alkaloid profiles in Crotalaria species from Brazil: chemotaxonomic significance. Biochem Syst Ecol 37:459–469CrossRefGoogle Scholar
  22. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227PubMedCrossRefGoogle Scholar
  23. Hay-Roe MM, Lamas G, Nation JL (2007) Pre- and postzygotic isolation and Haldane rule effects in reciprocal crosses of Danaus plexippus and Danaus erippus, supported by differentiation of cuticular hydrocarbons, establish their status as separate species. Biol J Linn Soc 91:445–453CrossRefGoogle Scholar
  24. Hoina A, Martins CZ, Trigo JR, Cogni R (2013) Preference for high concentration of plant pyrrolizidine alkaloids in the specialist arctiid moth Utetheisa ornatrix depends on previous experience. Arthropod Plant Interact 7:169–175CrossRefGoogle Scholar
  25. Kandori I, Ohsaki N (1998) Effect of experience on foraging behavior towards artificial nectar guide in the cabbage butterfly, Pieris rapae crucivora (Lepidoptera: Pieridade). Appl Entomol Zool 33:35–42Google Scholar
  26. Kandori I, Yamaki T (2012) Reward and non-reward learning of flower colours in the butterfly Byasa alcinous (Lepidoptera: Papilionidae). Naturwissenschaften 99:705–713PubMedCrossRefGoogle Scholar
  27. Kelber A (2002) Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc R Soc Lond B 269:2573–2577CrossRefGoogle Scholar
  28. Kelley RB, Seiber JN, Jones AD, Segall HJ, Brower LP (1987) Pyrrolizidine alkaloids in overwintering monarch butterflies (Danaus plexippus) from Mexico. Experientia 43:943–946CrossRefGoogle Scholar
  29. Kinoshita M, Arikawa K (2000) Colour constancy of the swallowtail butterfly Papilio xuthus. J Exp Biol 203:3521–3530PubMedGoogle Scholar
  30. Landolt PJ, Lenczewski B (1993) Lack of evidence for the toxic nectar hypothesis: a plant alkaloid did not deter nectar feeding by Lepidoptera. Fla Entomol 76:556–566CrossRefGoogle Scholar
  31. Malcolm SB, Slager BH (2015) Migration and host plant use by the southern monarch butterfly, Danaus erippus. In: Oberhauser KA, Altizer S, Nail K (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell University Press, Ithaca, pp 225–235Google Scholar
  32. Masters RA (1991) Dual role of pyrrolizidine alkaloids in nectar. J Chem Ecol 17:195–205PubMedCrossRefGoogle Scholar
  33. Meinwald J, Chalmers AM, Pliske TE, Eisner T (1968) Pheromones III. Identification of trans, trans 10-dydroxy-3,7-dimethyl-2,6-decadienoic acid as a major component in the “hairpencil” secretion of the male monarch butterfly. Tetrahedron Lett 9:4893–4896CrossRefGoogle Scholar
  34. Meinwald J, Chalmers AM, Pliske TE, Eisner T (1969) Identification and synthesis of trans, trans-3,7-dimethyl-2,6-decadien-l,10-dioic acid, a component of the pheromonal secretion of the male monarch butterfly. Chem Commun 3:86–87CrossRefGoogle Scholar
  35. Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154CrossRefGoogle Scholar
  36. Pliske TE (1975a) Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids. Environ Entomol 4:4445–473Google Scholar
  37. Pliske TE (1975b) Pollination of pyrrolizidine alkaloid-containing plants by male Lepidoptera. Environ Entomol 4:474–479CrossRefGoogle Scholar
  38. Pliske TE (1975c) Courtship behavior of the monarch butterfly, Danaus plexippus L. Ann Entomol Soc Am 68:143–151CrossRefGoogle Scholar
  39. Pliske TE, Eisner T (1969) Sex pheromone of the queen butterfly. Biology Science 164:1170–1172PubMedGoogle Scholar
  40. Pliske TE, Edgar JN, Culvenor CCJ (1976) The chemical basis of attraction of ithomine butterflies to plants containing pyrrolizidine alkaloids. J Chem Ecol 3:255–262CrossRefGoogle Scholar
  41. Rodrigues D (2015) Both associative learning and speed accuracy trade-off occur in the southern monarch butterfly when visiting flowers. Ethol Ecol Evol in press  10.1080/03949370.2015.1016118
  42. Rodrigues D, Weiss MR (2012) Reward tracking and memory decay in the monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae). Ethology 118:1122–1131CrossRefGoogle Scholar
  43. Rodrigues D, Goodner BW, Weiss MR (2010a) Reversal learning and risk-averse behavior in the monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae). Ethology 116:270–280CrossRefGoogle Scholar
  44. Rodrigues D, Maia PHS, Trigo JR (2010b) Sabotaging behavior and minimal latex of Asclepias curassavica incur no cost for the larvae of the southern monarch butterfly Danaus erippus. J Ecol Entomol 35:504–513Google Scholar
  45. Rothschild M, Edgar JA (1978) Pyrrolizidine alkaloids from Senecio vulgaris sequestered and stored by Danaus plexippus. J Zool 186:347–349CrossRefGoogle Scholar
  46. Schneider D, Boppré M, Schneider H, Thompson WR, Boriack CJ, Petty RL, Meinwald J (1975) A pheromone precursor and its uptake in Danaus butterflies. J Comp Physiol 97:245–256CrossRefGoogle Scholar
  47. Singer MC (2000) Reducing ambiguity in describing plant-insect interactions: “preference”, “acceptability” and “electivity”. Ecol Lett 3:159–162CrossRefGoogle Scholar
  48. Slager BH, Malcolm SB (2015) Evidence for partial migration in the southern monarch butterfly, Danaus erippus, in Bolivia and Argentina. Biotropica: in pressGoogle Scholar
  49. Smith DAS, Lushai G, Allen JA (2005) A classification of Danaus butterflies (Lepidoptera: Nymphalidae) based upon data from morphology and DNA. Zool J Linnean Soc 144:191–212CrossRefGoogle Scholar
  50. Trigo JR (2011) Effects of pyrrolizidine alkaloids through different trophic levels. Phytochem Rev 10:83–98CrossRefGoogle Scholar
  51. Trigo JR, Brown KS, Witte L, Hartmann T, Ernst L, Barata LES (1996) Pyrrolizidine alkaloids: different acquisition and use patterns in Apocynaceae and Solanaceae feeding ithomiine butterflies (Lepidoptera: Nymphalidae). Biol J Linn Soc 58:99–123CrossRefGoogle Scholar
  52. Weiss MR (1995) Floral color change: a widespread functional convergence. Am J Bot 82:167–185CrossRefGoogle Scholar
  53. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Marina Vasconcelos de Oliveira
    • 1
  • José Roberto Trigo
    • 2
  • Daniela Rodrigues
    • 1
  1. 1.Laboratório de Interações Inseto-Planta, Departamento de Ecologia, Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Laboratório de Ecologia Química, Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil

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