, Volume 100, Issue 10, pp 901–911 | Cite as

Behavioral and life-history evidence for interspecific competition in the larvae of two heliconian butterflies

  • Carolina Millan
  • Simone Silva Borges
  • Daniela RodriguesEmail author
  • Gilson Rudinei Pires Moreira
Original Paper


Interspecific competition in herbivorous insects remains a controversial issue. To date, many studied systems have not met assumptions of the traditional competition theory, and a new paradigm has been emerging. We examined the behavioral and life-history consequences of common host plant use of Heliconius erato and Dryas iulia (Nymphalidae) in relation to Passiflora suberosa (Passifloraceae). Larvae of the former use the apical portion of this host; the latter is presumably able to explore all plant parts. We assessed host use pattern in relation to leaf age, when reared either alone (D. iulia) or together (D. iulia and H. erato). Larval feeding choice tests with respect to leaf age were performed, and performance was recorded. Observations were made to assess antagonistic behavior of H. erato and D. iulia towards each other, if any. Similarly to H. erato, D. iulia fed on the young leaves significantly more than the mature ones; larvae were not induced to prefer mature leaves. First instars of H. erato used only the apical parts of P. suberosa and displayed aggressive behavior towards D. iulia, which moved to the lower shoot portions. Larval mortality and development time of both species significantly increased when reared together; such performance costs were more pronounced in D. iulia than H. erato. Our study gathers evidences that use of P. suberosa by these heliconian butterflies represent a case of competitive exclusion resulting in niche differentiation, where costs are higher for D. iulia than H. erato.


Competition exclusion Coexistence Niche differentiation Heliconiini Passifloraceae 



We are grateful to José R. Trigo for help with statistical analysis and comments on early drafts of the manuscript. We also thank Ian Kaplan and three anonymous reviewers for comments that have improved the manuscript. CM and SSB received grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), respectively. Conselho Nacional de Pesquisa (CNPq) supported DR (grant no. 480264/2010-4) and GRPM (grant no. 309676/2011-8).

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  1. Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers, and natural enemies. Princeton University Press, PrincetonGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267Google Scholar
  3. Beccaloni GW, Viloria AL, Hall SK, Robinson GS (2008) Catalogue of the hostplants of the neotropical butterflies, Vol. 8. Monografias Tercer Milenio, ZaragozaGoogle Scholar
  4. Beltran M, Jiggins CD, Brower AVZ, Bermingham E, Mallet J (2007) Do pollen feeding, pupal mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biol J Linn Soc 92:221–239CrossRefGoogle Scholar
  5. Benson WW (1978) Resource partitioning in passion on vine butterflies. Evolution 32:493–518CrossRefGoogle Scholar
  6. Benson WW, Brown KS Jr, Gilbert LE (1976) Coevolution of plants and herbivores: passion flowers butterflies. Evolution 29:659–680CrossRefGoogle Scholar
  7. Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New YorkGoogle Scholar
  8. Brown KS Jr (1981) The biology of Heliconius and related genera. Annu Rev Entomol 26:427–456CrossRefGoogle Scholar
  9. Connell JH (1980) Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35:131–138CrossRefGoogle Scholar
  10. Conover WJ (1999) Practical nonparametric statistics, 3rd edn. Wiley , New YorkGoogle Scholar
  11. Dell’Erba R, Kaminski LA, Moreira GRP (2005) O estágio de ovo dos Heliconiini (Lepidoptera, Nymphalidae) do Rio Grande do Sul, Brasil. Ihering Ser Zool 95:29–46CrossRefGoogle Scholar
  12. Denno RF, McClure MS, Ott JR (1995) Interespecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331CrossRefGoogle Scholar
  13. Elpino-Campos A (2012) Feeding behavior of Heliconius erato phyllis (Fabricius) (Lepidoptera: Nymphalidae) larvae on passion vines. Acta ethol 15:107–118CrossRefGoogle Scholar
  14. Faeth S (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494CrossRefGoogle Scholar
  15. Ferro VG (1998) Criação de Heliconius erato phyllis (Fabricus) (Lepidoptera: Nymphalidae) em condições semi-naturais. Senior Thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  16. Garcias GL (1983) Aspectos da biologia populacional de cinco espécies de heliconíneos do anel mimético laranja (Lepidoptera: Nymphalidae). Unpublished MSc Thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  17. Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference-performance relationships in phytophagous insects. Ecol Lett 13:383–393PubMedCrossRefGoogle Scholar
  18. Hairston NH, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425CrossRefGoogle Scholar
  19. Hanson FE (1983) The behavioral and neurophysiological basis of food plant selection by lepidopterous larvae. In: Ahmad S (ed) Herbivorous insects: host-seeking behavior and mechanisms. Academic, New York, pp 3–23CrossRefGoogle Scholar
  20. Haukioja E (1993) Effects of food and predation on population dynamics. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 425–447Google Scholar
  21. Honék A (1993) Intraespecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492CrossRefGoogle Scholar
  22. Kaminski LA, Tavares M, Ferro VG, Moreira GRP (2002) Morfologia externa dos estágios imaturos de heliconíneos neotropicais. III. Heliconius erato phyllis (Fabricius) (Lepidoptera: Nymphalidae: Heliconinae). Revta Bras Zool 19:977–993Google Scholar
  23. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994PubMedCrossRefGoogle Scholar
  24. Karban R (1986) Interspecific competition between folivorous insects on Erigeron glaucus. Ecology 67:1063–1072CrossRefGoogle Scholar
  25. Karban R (1989) Community organization of Erigeron glaucus folivores: effects of competition, predation, and host plant. Ecology 70:1028–1039CrossRefGoogle Scholar
  26. Kerpel SM, Moreira GRP (2005) Absence of learning and local specialization on host plant selection by Heliconius erato. J Ins Behav 18:433–452CrossRefGoogle Scholar
  27. Long JD, Hamilton RS, Mitchell JL (2007) Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations. Ecology 88:1232–1240PubMedCrossRefGoogle Scholar
  28. Mega NO, Araújo A (2008) Do caterpillars of Dryas iulia alcionea (Lepidoptera, Nymphalidae) show evidence of adaptive behaviour to avoid predation by ants? J Nat Hist 42:129–137CrossRefGoogle Scholar
  29. Moreira GRP, Ferrari A, Mondin C, Cervi A (2011) Panbiogeographical analysis of passion vines at their southern limit of distribution in the Neotropics. Rev Bras Biocienc 9:28–40Google Scholar
  30. Mugrabi-Oliveira E, Moreira GRP (1996a) Conspecific mimics and low host plant availability reduce egg laying by Heliconius erato phyllis (Lepidoptera: Nymphalidae). Revta Bras Zool 13:929–937CrossRefGoogle Scholar
  31. Mugrabi-Oliveira E, Moreira GRP (1996b) Size of and damage on shoots of Passiflora suberosa (Passifloraceae) influence oviposition site selection of Heliconius erato phyllis (Fabricius) (Lepidoptera, Nymphalidae). Revta Bras Zool 13:939–953CrossRefGoogle Scholar
  32. Paim AC, Kaminski LA, Moreira GRP (2004) Morfologia externa dos estágios imaturos de heliconíneos neotropicais. IV. Dryas iulia alcionea (Lepidoptera: Nymphalidae: Heliconinae). Ihering Ser Zool 94:25–35Google Scholar
  33. Park T (1948) Experimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium confusum Duvall and Tribolium castaneum Herbst. Ecol Monog 18:267–307CrossRefGoogle Scholar
  34. Périco E (1995) Interação entre quatro espécies de Heliconiinae (Lepidoptera: Nymphalidae) e suas plantas hospedeiras (Passifloraceae) em uma floresta secundaria do Rio Grande de Sul, Brasil. Biociências 3:3–18Google Scholar
  35. Périco E, Araujo AM (1991) Suitability of host plants (Passifloraceae) and their acceptableness by Heliconius erato and Dryas iulia (Lepidoptera: Nymphalidae). Evol Biol 5:59–74Google Scholar
  36. Rathcke BJ (1976) Competition and coexistence within a guild of herbivorous insects. Ecology 57:76–87CrossRefGoogle Scholar
  37. Redman AM, Scriber JM (2000) Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids. Oecologia 125:218–228CrossRefGoogle Scholar
  38. Rodrigues D, Moreira GRP (1999) Feeding preference of Heliconius erato phyllis (Lepidoptera, Nymphalidae) in relation to leaf age and consequences for larval performance. J Lep Soc 53:108–113Google Scholar
  39. Rodrigues D, Moreira GRP (2002) Geographical variation in larval host plant used by Heliconius erato (Lepidoptera: Nymphalidae) and consequences for adult life history. Braz J Biol 62:321–332PubMedCrossRefGoogle Scholar
  40. Roemer GW, Donlan CJ, Courchamp F (2002) Golden eagles, feral pigs, and insular carnivores: how exotic species turn native predators into prey. Proc Natl Acad Sci USA 99:791–796PubMedCrossRefGoogle Scholar
  41. Schoener TW (1974) Resource partitioning in ecological communities: research on how similar species divide resources helps reveal the natural regulation of species diversity. Science 185:27–39PubMedCrossRefGoogle Scholar
  42. Silveira MAPA (2002) Variação da dureza da folha em Passiflora, efeito no desgaste das mandíbulas de Heliconius erato phyllis (Lepidoptera: Nymphalidae) e conseqüências sobre a herbivoria. Porto Alegre, Unpublished MSc Thesis, Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
  43. Thomas CD (1987) Behavioral determination of diet breadth in insect herbivores: the effect of leaf age on choice of host species by beetles feeding on Passiflora vines. Oikos 48:211–216CrossRefGoogle Scholar
  44. Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Ent Exp Appl 47:3–14CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Carolina Millan
    • 1
  • Simone Silva Borges
    • 2
  • Daniela Rodrigues
    • 3
    Email author
  • Gilson Rudinei Pires Moreira
    • 1
    • 2
  1. 1.PPG Ecologia, Departamento de Ecologia, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  2. 2.Departamento de Zoologia, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.Departamento de Ecologia, Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil

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