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Restricted within-habitat movement and time-constrained egg laying of female Maculinea rebeli butterflies

Abstract

The movement of butterflies within habitat patches is usually assumed to be random, although few studies have shown this unambiguously. In the case of the highly specialized genus Maculinea, two contradictory hypotheses exist to explain the movement and distribution of imagos within patches: (1) due to the high spatial variance of survival rates among caterpillars, the “risk-spreading” hypothesis predicts that females will tend to make linear flight paths in order to maximize their net displacement and scatter the eggs as widely as possible; and (2) recent mark–release–recapture (MRR) data suggest that within-habitat displacement of some Maculinea species is constrained and that adults may establish home ranges. We tested both hypothesis by analysing the movement pattern of individuals. We also investigated whether egg laying is time constrained, which would enhance the trade-off between flying and egg laying. Thirty females of Maculinea rebeli (Lepidoptera: Lycaenidae) were tracked within a single population in Central Hungary. Their egg-laying behaviour and individual patterns of movement were recorded, and the latter were compared with random walk model predictions. The population was also sampled by MRR to estimate survival rates, and four non-mated, freshly eclosed females were dissected to assess their potential egg load. Net squared displacement of females was significantly lower than predicted by the random walk model and declined continuously after the 15th move. The ratio of net displacement and cumulative move length decreased with the number of moves, supporting the hypothesis that Maculinea butterflies establish home ranges. We found that low survival and a low rate of egg laying prevented females from laying their potential number of eggs within their lifespan. Time limitation increased the cost of movement, providing another possible explanation for the restricted movement of females.

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References

  1. Als TD, Vila R, Kandul NP, Nash DR, Yen SH, Hsu YF, Mignault AA, Boomsma JJ, Pierce NE (2004) The evolution of alternative parasitic life histories in large blue butterflies. Nature 432:386–390

  2. Árnyas E, Bereczki J, Tóth A, Varga Z (2005) Results of the mark–release–recapture studies of a Maculinea rebeli population in the Aggtelek karst (N Hungary) between 2002–2004. In: Settele J, Kühn E, Thomas JA (eds) Species ecology along a European gradient: Maculinea butterflies as a model. Studies on the ecology and conservation of butterflies in Europe, vol 2. PENSOFT, Sofia, pp 111–114

  3. Bereczki J, Pecsenye K, Peregovits L, Varga Z (2005) Pattern of genetic differentiation in the Maculinea alcon species group (Lepidoptera, Lycaenidae) in Central Europe. J Zool Syst Evol Res 43:157–165

  4. Caro T (1999) The behaviour–conservation interface. Trends Ecol Evol 14:366–369

  5. Clarke RT, Thomas JA, Elmes GW, Hochberg ME (1997) The effects of spatial patterns in habitat quality on community dynamics within a site. Proc R Soc Lond B 264:347–354

  6. Clarke RT, Thomas JA, Elmes GW, Wardlaw JC, Munguira ML, Hochberg ME (1998) Population modelling of the spatial interactions between Maculinea, their initial foodplant and Myrmica ants within a site. J Insect Conserv 2:29–38

  7. Conradt L, Roper TJ (2006) Nonrandom movement behavior at habitat boundaries in two butterfly species: implications for dispersal. Ecology 87:125–132

  8. Conradt L, Bodsworth EJ, Roper TJ, Thomas CD (2000) Non-random dispersal in the butterfly Maniola jurtina: implications for metapopulation models. Proc R Soc Lond B 267:1505–1510

  9. Conradt L, Roper TJ, Thomas CD (2001) Dispersal behaviour of individuals in metapopulations of two British butterflies. Oikos 95:416–424

  10. Doak P, Kareiva P, Kingsolver J (2006) Fitness consequences of choosy oviposition for a time-limited butterfly. Ecology 87:395–408

  11. Dolek M, Geyer A, Bolz R (1998) Distribution of Maculinea rebeli and hostplant use on sites along the river Danube. J Insect Conserv 2:85–89

  12. Elmes GW, Thomas JA, Wardlaw JC (1991a) Larvae of Maculinea rebeli, a large-blue butterfly, and their Myrmica host ants: wild adoption and behaviour in ant nests. J Zool 223:447–460

  13. Elmes GW, Thomas JA, Wardlaw JC (1991b) Larvae of Maculinea rebeli, a large-blue butterfly, and their Myrmica host ants: patterns of caterpillar growth and survival. J Zool 224:79–92

  14. Elmes GW, Clarke RT, Thomas JA, Hochberg ME (1996) Empirical tests of specific predictions made from a spatial model of the population dynamics of Maculinea rebeli, a parasitic butterfly of red ant colonies. Acta Oecol 17:61–80

  15. Fiedler K (1998) Lycaenid–ant interactions of the Maculinea type: tracing their historical roots in a comparative framework. J Insect Conserv 2:3–14

  16. Fisher NI (1993) Statistical analysis of circular data. Cambridge University Press, Cambridge

  17. Fownes S, Roland J (2002) Effects of meadow suitability on female behaviour in the alpine butterfly Parnassius smintheus. Ecol Entomol 27:457–466

  18. Grosjean P, Lecoutre E (2005) SciViews GUI API. R package version 0.8–8. http://www.sciviews.org/SciViews-R

  19. Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford

  20. Hochberg ME, Thomas JA, Elmes GW (1992) A modelling study of the population dynamics of a large blue butterfly, Maculinea rebeli, a parasite of red ant nests. J Anim Ecol 61:397–409

  21. Hochberg ME, Clarke RT, Elmes GW, Thomas JA (1994) Population dynamic consequences of direct and indirect interactions involving a large blue butterfly and its plant and red ant hosts. J Anim Ecol 63:375–391

  22. Hovestadt T (2005) A review of the role of dispersal for population persistence in Maculinea. In: Settele J, Kühn E, Thomas JA (eds) Species ecology along a European gradient: Maculinea butterflies as a model. Studies on the ecology and conservation of butterflies in Europe, vol 2. PENSOFT, Sofia, p 120

  23. Hovestadt T, Nowicki P (2005) Within-patch movement limitation in two species of Maculinea butterflies? Analysis of MRR data using randomisation procedures. In: Settele J, Kühn E, Thomas JA (eds) Species ecology along a European gradient: Maculinea butterflies as a model. Studies on the ecology and conservation of butterflies in Europe, vol 2. PENSOFT, Sofia, p 122

  24. Kareiva PM, Shigesada N (1983) Analyzing insect movement as a correlated random walk. Oecologia 56:234–238

  25. Kingsolver JG (1983) Ecological significance of flight activity in Colias butterflies: implications for reproductive strategy and population structure. Ecology 64:546–551

  26. Lindenmayer DB, Possingham HP, Lacy RC, McCarthy MA, Pope ML (2003) How accurate are population models? Lessons from landscape-scale tests in a fragmented system. Ecol Lett 6:41–47

  27. Mallet J (1986) Dispersal and gene flow in a butterfly with home range behaviour (Heliconius erato). Oecologia 68:210–217

  28. Morales JM, Ellner SP (2002) Scaling up animal movements in heterogeneous landscapes: the importance of behavior. Ecology 83:2240–2247

  29. Musche M, Anton C, Worgan A, Settele J (2006) No experimental evidence for host ant related oviposition in a parasitic butterfly. J Ins Behav 19:631–643. doi:10.1007/s10905-006-9053-0

  30. Nowicki P, Bonelli S, Barbero F, Balletto E (2005a) Population dynamics in the genus Maculinea revisited: comparative study of sympatric M. alcon and M. teleius. In: Settele J, Kühn E, Thomas JA (eds) Species ecology along a European gradient: Maculinea butterflies as a model. Studies on the ecology and conservation of butterflies in Europe, vol 2. PENSOFT, Sofia, pp 136–139

  31. Nowicki P, Witek M, Skórka P, Settele J, Woyciechowski M (2005b) Population ecology of the endangered butterflies Maculinea teleius and M. nausithous and the implications for conservation. Popul Ecol 47:193–202

  32. Odendaal FJ, Turchin P, Stermitz FR (1989) Influence of host-plant density and male harassment on the distribution of female Euphydryas anicia (Nymphalidae). Oecologia 78:283–288

  33. Ovaskainen O (2004) Habitat-specific movement parameters estimated using mark-recapture data and a diffusion model. Ecology 85:242–257

  34. Ovaskainen O, Hanski I (2004) From individual behavior to metapopulation dynamics: unifying the patchy population and classic metapopulation models. Am Nat 164:364–377

  35. Pech P, Fric Z, Konvicka M, Zrzavy J (2004) Phylogeny of Maculinea blues (Lepidoptera:Lycaenidae) based on morphological and ecological characters: evolution of parasitic myrmecophily. Cladistics 20:362–375

  36. Pfeifer MA, Andrick UR, Frey W, Settele J (2000) On the ethology and ecology of a small and isolated population of the dusky large blue butterfly Glaucopsyche (Maculinea) nausithous (Lycaenidae). Nota Lepid 23:147–172

  37. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York, pp 206–226

  38. R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org

  39. Ries L, Debinski DM (2001) Butterfly responses to habitat edges in the highly fragmented prairies of Central Iowa. J Anim Ecol 70:840–852

  40. Root RB, Kareiva PM (1984) The search for resources by cabbage butterflies (Pieris rapae): ecological consequences and adaptive significance of Markovian movements in a patchy environment. Ecology 65:147–165

  41. Schtickzelle N, Baguette M (2003) Behavioural responses to habitat patch boundaries restrict dispersal and generate emigration–patch area relationships in fragmented landscapes. J Anim Ecol 72:533–545

  42. Schtickzelle N, Joiris A, Van Dyck H, Baguette M (2007) Quantitative analysis of changes in movement behaviour within and outside habitat in a specialist butterfly. BMC Evol Biol 7. doi:10.1186/1471-2148-7-4

  43. Schultz CB (1998) Dispersal behavior and its implications for reserve design in a rare Oregon butterfly. Conserv Biol 12:284–292

  44. Schultz CB, Crone EE (2001) Edge-mediated dispersal behavior in a prairie butterfly. Ecology 82:1879–1892

  45. Settele J, Kühn E, Thomas JA (2005) Species ecology along a European gradient: Maculinea butterflies as a model. Studies on the ecology and conservation of butterflies in Europe, vol 2. PENSOFT, Sofia

  46. Sutherland WJ (1998) The importance of behavioural studies in conservation biology. Anim Behav 56:801–809

  47. Thomas JA (1995) The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In: Pullin A (ed) Ecology and conservation of butterflies. Chapman and Hall, London, pp 180–197

  48. Thomas JA (2002) Larval niche selection and evening exposure enhance adoption of a predacious social parasite, Maculinea arion (large blue butterfly), by Myrmica ants. Oecologia 132:531–537

  49. Thomas JA, Elmes GW (1998) Higher productivity at the cost of increased host-specificity when Maculinea butterfly larvae exploit ant colonies through trophallaxis rather than by predation. Ecol Entomol 23:457–464

  50. Thomas JA, Elmes GW (2001) Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. Proc R Soc Lond B 268:471–477

  51. Thomas JA, Settele J (2004) Butterfly mimics of ants. Nature 432:283–284

  52. Thomas JA, Elmes GW, Wardlaw JC, Woyciechowski M (1989) Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia 79:452–457

  53. Thomas JA, Munguira M, Martinez L, Elmes GW (1991) Basal hatching by Maculinea eggs: a consequence of advanced myrmecophily. Biol J Linn Soc 44:175–184

  54. Thomas JA, Elmes GW, Wardlaw JC (1993) Contest competition among Maculinea rebeli butterfly larvae in ant nests. Ecol Entomol 18:73–76

  55. Thomas JA, Elmes GW, Clarke RT, Kim KG, Munguira ML, Hochberg ME (1997) Field evidence and model predictions of butterfly-mediated apparent competition between gentian plants and red ants. Acta Oecol 18:671–684

  56. Thomas JA, Clarke RT, Elmes GW, Hochberg ME (1998a) Population dynamics in the genus Maculinea (Lepidoptera:Lycaenidae). In: Dempster JP, McLean IFG (eds) Insect population dynamics: in theory and practice. Symposia of the Royal Entomological Society 19. Chapman and Hall, London, pp 261–290

  57. Thomas JA, Elmes GW, Wardlaw JC (1998b) Polymorphic growth in larvae of the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc R Soc Lond B 265:1895–1901

  58. Turchin P (1991) Translating foraging movements in heterogeneous environments into the spatial distribution of foragers. Ecology 72:1253–1266

  59. Turchin P (1998) Quantitative analysis of movement. Sinauer, Sunderland

  60. Turchin P, Odendaal FJ, Rausher MD (1991) Quantifying insect movement in the field. Environ Entomol 20:955–963

  61. Van Dyck H, Baguette M (2005) Dispersal behaviour in fragmented landscapes: routine or special movements? Basic Appl Ecol 6:535–545

  62. Van Dyck H, Oostermeijer JGB, Talloen W, Feenstra V, Van der Hidde A, Wynhoff I (2000) Does the presence of ant nests matter for oviposition to a specialized myrmecophilous Maculinea butterfly? Proc R Soc Lond B 267:861–866

  63. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Suppl):120–138

  64. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

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Acknowledgments

We thank Márta Kocsis, Szabolcs Sáfián, Zoltán Soltész, Annamária Szabó, Róbert Szűcs and Ágnes Vozár for their help in the field work and Andrea Harnos for her assistance in statistical analyses. The authors are especially grateful to Michel Baguette, Thomas Hovestadt, Nicolas Schtickzelle, Jeremy Thomas and Zoltán Varga for their useful comments, which considerably improved the manuscript. This work was supported by the EU MacMan project (EVK2-CT-2001-00126) and by the nationally funded the origin and genezis of the fauna of the Carpathian Basin project (NKFP 3B023-04). All experiments comply with the current laws of Hungary, where the experiments were performed.

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Correspondence to Ádám Kőrösi.

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Communicated by Konrad Fiedler.

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Kőrösi, Á., Örvössy, N., Batáry, P. et al. Restricted within-habitat movement and time-constrained egg laying of female Maculinea rebeli butterflies. Oecologia 156, 455–464 (2008). https://doi.org/10.1007/s00442-008-0986-1

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Keywords

  • Home range
  • Myrmecophily
  • Oviposition
  • Random walk model
  • Risk spreading