Journal of Ethology

, Volume 28, Issue 3, pp 409–420 | Cite as

Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: conflict between attraction and repulsion signals?

  • André Luis Klein
  • Aldo Mellender de AraújoEmail author
Video Article


Previous observations of Heliconius erato phyllis females being intensively courted a few days after mating contradict the proposal of sexual repulsion caused by a male-transferred antiaphrodisiac. Furthermore, data on courtship in Heliconius butterflies are almost absent from the literature. In this work we aim to describe the courtship behavior of H. erato phyllis and to compare it towards virgin and mated females. Sexual interactions using both kinds of females were observed and filmed in seminatural conditions for subsequent analysis and quantification. Courtship of virgin and mated females differed qualitatively and quantitatively, but the results do not agree with the proposal of sexual repulsion. The differences found indicate that the courtship sequence towards mated females is interrupted in the transition that would lead to the behavior immediately prior to copulation, in such a way that the male continues courting the female in an intermediate phase. Preliminary tests even showed that older females, virgin or not, are much less courted by males. We suggest that there is a trade-off between an attraction pheromone, important for males to locate female pupae, and the male-transferred antiaphrodisiac, so that young, mated females may have both signals active.


Courtship behavior Antiaphrodisiac Female attractiveness Antagonistic signals Butterflies 



We are grateful to all the people who collaborated with rearing the individuals in the cage and laboratory (Adriano Ferreira, Gabriela Pasqualim, Janaína De Nardin, Julie Zanin, Nicolás O. Mega, and Pedro Vieira), and Professor Helga Winge for offering a fine space in her working area to install the cages used in the observations. We thank Professor Gilson R.P. Moreira and Luiz Ernesto Costa-Schmidt for suggestions that improved the final manuscript, and especially Nicolás O. Mega for discussions, suggestions, and productive criticism throughout most of this study. We also thank two anonymous referees for comments and criticisms on the first submission of this article. Finally, we thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

Supplementary material

Supplementary material 1 (AVI 16640 kb)


  1. Alcock J, Thornhill R (1983) The evolution of insect mating systems. Harvard University Press, USAGoogle Scholar
  2. Alexander RD, Marshall DC, Cooley JR (1997) Evolutionary perspectives on insect mating. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 4–31CrossRefGoogle Scholar
  3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  4. Andersson J, Borg-Karlson AK, Wiklund C (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B 267:1271–1275CrossRefGoogle Scholar
  5. Andersson J, Borg-Karlson AK, Wiklund C (2003) Antiaphrodisiacs in pierid butterflies: a theme with variation!. J Chem Ecol 29:1489–1499CrossRefPubMedGoogle Scholar
  6. Andersson J, Borg-Karlson AK, Wiklund C (2004) Sexual conflict and anti-aphrodisiac titre in a polyandrous butterfly: male ejaculate tailoring and absence of female control. Proc R Soc Lond B 271:1765–1770CrossRefGoogle Scholar
  7. Boppré M (1984) Chemically mediated interactions between butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic, London, pp 259–275Google Scholar
  8. Cordero C (1993) The courtship behavior of Callophrys xami (Lycaenidae). J Res Lepid 32:99–106Google Scholar
  9. Crane J (1955) Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoologica 40:167–196Google Scholar
  10. Daniels JC (2007) Courtship solicitation by females of the barred sulphur butterfly (Eurema daira) (Lepidoptera: Pieridae). J Insect Behav 20:129–135CrossRefGoogle Scholar
  11. Deinert EI (2003) Mate location and competition for mates in a pupal mating butterfly. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies: ecology and evolution taking flight. University of Chicago Press, Chicago, pp 91–108Google Scholar
  12. Delisle J, Simard J (2003) Age-related changes in the competency of the pheromone gland and the pheromonotropic activity of the brain of both virgin and mated females of two Choristoneura species. J Insect Physiol 49:91–97CrossRefPubMedGoogle Scholar
  13. Drummond BA III (1984) Multiple mating and sperm competition in the lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, London, pp 291–370Google Scholar
  14. Emsley M (1963) A morphological study of imagine Heliconiinae (Lep.: Nymphalidae) with a consideration of the evolutionary relationships within the group. Zoologica 48:85–130Google Scholar
  15. Estrada C, Yildizhan S, Schulz S, Gilbert LE (2009) Sex-specific chemicals cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proc R Soc B. doi: 10.1098/rspb.2009.1476
  16. Fagen RM, Young DY (1978) Temporal patterns of behavior: intervals, latencies and sequences. In: Colgan PW (ed) Quantitative ethology. Wiley, New York, pp 78–114Google Scholar
  17. Ferreira AA, Garcia RN, Araújo AM (2006) Pupal melanization in Heliconius erato phyllis (Lepidoptera; Nymphalidae): genetic and environmental effects. Genetica 126:133–140CrossRefPubMedGoogle Scholar
  18. Garcias GL (1983) Aspectos da Biologia Populacional de Cinco Espécies de Heliconíneos do Anel Mimético “Laranja” (Lepidoptera, Nymphalidae). Master thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  19. Gilbert LE (1976) Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac? Science 193:419–420CrossRefPubMedGoogle Scholar
  20. Hiroki M, Obara Y (1998) Changes in age-related reproductive tactics in the female of the butterfly, Eurema hecabe. Naturwissenschaften 85:551–552CrossRefGoogle Scholar
  21. Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411:302–305CrossRefPubMedGoogle Scholar
  22. Jiggins CD, Estrada C, Rodrigues A (2004) Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J Evol Biol 17:680–691CrossRefPubMedGoogle Scholar
  23. Kerpel S, Moreira GRP (2005) Absence of learning and local specialization on host plant selection by Heliconius erato. J Insect Behav 18:433–452CrossRefGoogle Scholar
  24. Krebs RA (1988) The mating behavior of Papilio glaucus (Papilionidae). J Res Lepid 26:27–31Google Scholar
  25. Martin P, Bateson P (1993) Measuring behaviour. An introductory guide, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  26. Mavárez J, Salazar CA, Birmingham E, Salcedo C, Jiggins C, Linares M (2006) Speciation by hybridization in Heliconius butterflies. Nature 441:868–871CrossRefPubMedGoogle Scholar
  27. McMillan WO, Jiggins CD, Mallet J (1997) What initiates speciation in passion-vine butterflies? Proc Natl Acad Sci USA 94:8628–8633CrossRefPubMedGoogle Scholar
  28. Mega NO, Araújo AM (2010) Analysis of mating behavior and some possible causes of male copulatory success in Dryas iulia alcionea (Lepidoptera; Nymphalidae; Heliconiinae). J Ethol 28:123–132 Google Scholar
  29. Pellmyr O (1982) Plebeian courtship revisited: studies on the female-produced male behavior-eliciting signals in Lycaeides idas (Lycaenidae). J Res Lepid 21:147–157Google Scholar
  30. Penz CM, Peggie D (2003) Phylogenetic relationships among Heliconiinae genera based on morphology (Lepidoptera: Nymphalidae). Syst Entomol 28:451–479CrossRefGoogle Scholar
  31. Périco E, Araújo AM (1991) Suitability of host plants (Passifloraceae) and their acceptableness by Heliconius erato and Dryas iulia (Lepidoptera; Nymphalidae). Evol Biol 5:59–74Google Scholar
  32. Rodrigues D, Moreira GRP (2002) Geographical variation in larval host-plant use by Heliconius erato (Lepidoptera: Nymphalidae) and consequences for adult life history. Braz J Biol 62:321–332CrossRefPubMedGoogle Scholar
  33. Rodrigues D, Moreira GRP (2004) Seasonal variation in larval host plants and consequences for Heliconius erato (Lepidoptera: Nymphalidae) adult body size. Austral Ecol 29:437–445CrossRefGoogle Scholar
  34. Rutowski RL (1979) Courtship behavior of the checkered White, Pieris protodice (Pieridae). J Lepid Soc 33:42–49Google Scholar
  35. Rutowski RL (1980) Courtship solicitation by females of the checkered White butterfly, Pieris protodice. Behav Ecol Sociobiol 7:113–117CrossRefGoogle Scholar
  36. Rutowski RL (1984) Sexual selection and the evolution of butterfly mating behavior. J Res Lepid 23:125–142Google Scholar
  37. Rutowski RL, Schaefer J (1984) Courtship behavior of the gulf fritillary Agraulis vanillae (Nymphalidae). J Lepid Soc 38:23–31Google Scholar
  38. Schulz S, Estrada C, Yildizhan S, Boppré M, Gilbert LE (2008) An antiaphrodisiac in Heliconius melpomene butterflies. J Chem Ecol 34:82–93CrossRefPubMedGoogle Scholar
  39. Scott JA (1973) Mating of butterflies. J Res Lepid 11:99–127Google Scholar
  40. Silberglied RE (1984) Visual communication and sexual selection among butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic, London, pp 207–223Google Scholar
  41. Silva LM, Araújo AM (1994) The genetic structure of Heliconius erato populations. Revista Brasileira de Genética 17:19–24Google Scholar
  42. Vane-Wright RI, Boppré M (1993) Visual and chemical signaling in butterflies: functional and phylogenetic perspectives. Philos Trans R Soc B 340:197–205CrossRefGoogle Scholar

Copyright information

© Japan Ethological Society and Springer 2010

Authors and Affiliations

  • André Luis Klein
    • 1
  • Aldo Mellender de Araújo
    • 1
    Email author
  1. 1.Laboratório de Genética Ecológica, Departamento de Genética, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil

Personalised recommendations