Living on the edge: population ecology of Phengaris teleius in Serbia

Abstract

Due to their complex and interesting life cycle and alarming conservation status the Large Blue butterflies have become one of the most studied group of insects in Europe. In Serbia, however, Phengaris teleius has recently been discovered (in the far north of the country) and, since this initial finding, significant efforts have been made to map the local distribution of this species and to implement conservation measures. A mark-release-recapture study was initiated to obtain a more detailed report about population size and structure in Serbia. Results have shown that localities and patches within these localities are well connected by migration of butterflies and gave some evidence for metapopulation organisation. The total number of individuals was estimated at 15,000, which makes it one of the largest known metapopulations in Europe. Unusual for populations at the edge of the distribution range, these are characterized with large population estimates and relative stability. Compared to other areas in Europe, butterflies in Serbia start to fly 2 weeks later in the summer, probably a consequence of a late mowing regime initiated during July. Some evidence of a negative relationship between the survival of P. teleius adults and local population density was also found. With favourable management, these populations could remain stable for the foreseeable future. The preservation of large, healthy populations of P. teleius supported by a favourable management and monitoring programme along with the sustainability of individual dispersal translocation between patches should be a prime aim.

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References

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

    CAS  Article  PubMed  Google Scholar 

  2. Anderson DR, Burnham KP (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  3. Barbero F, Thomas JA, Bonelli S, Balletto E, Schönrogge K (2009) Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science 323:782–785

    CAS  Article  PubMed  Google Scholar 

  4. Batáry P, Orvossy N, Korosi A, Nagy MV, Peregovits L (2007) Microhabitat preferences of Maculinea teleius (Lepidoptera: Lycaenidae) in a mosaic landscape. Eur J Entomol 104:731–736

    Article  Google Scholar 

  5. Bonelli S, Vrabec V, Witek M, Barbero F, Patricelli D, Nowicki P (2013) Selection on dispersal in isolated butterfly metapopulations. Popul Ecol 55:469–478. doi:10.1007/s10144-013-0377-2

    Article  Google Scholar 

  6. Bourn NA, Thomas J (2002) The challenge of conserving grassland insects at the margins of their range in Europe. Biol Conserv 104:285–292. doi:10.1016/S0006-3207(01)00193-8

    Article  Google Scholar 

  7. Brakefield PM (1982) Ecological studies on the butterfly Maniola jurtina in Britain. II. Population dynamics: the present position. J Anim Ecol 51:727–738

    Article  Google Scholar 

  8. Burnham KP, Anderson DR, White GC, Brownie C, Pollock KH (1987) Design and analysis methods for fish survival experiments based on release-recapture. American Fisheries Society, Bethesda

    Google Scholar 

  9. Dias PC (1996) Sources and sinks in population biology. Trends Ecol Evol 11:326–330. doi:10.1016/0169-5347(96)10037-9

    CAS  Article  PubMed  Google Scholar 

  10. Dierks A, Fischer K (2009) Habitat requirements and niche selection of Maculinea nausithous and M. teleius (Lepidoptera: Lycaenidae) within a large sympatric metapopulation. Biodivers Conserv 18:3663–3676. doi:10.1007/s10531-009-9670-y

    Article  Google Scholar 

  11. Elmes GW, Thomas JA (1992) Complexity of species conservation in managed habitats: interaction between Maculinea butterflies and their ant hosts. Biodivers Conserv 1:155–169

    Article  Google Scholar 

  12. Gajić M (1986) Flora i vegetacija Subotičko-horgoške peščare. Šumarski fakultet Beograd, Šumsko gazdinstvo Subotica, Subotica

  13. Gao K, Li X, Chen F, Guo Z, Settele J (2015) Distribution and habitats of Phengaris (Maculinea) butterflies and population ecology of Phengaris teleius in China. J Insect Conserv. doi:10.1007/s10841-015-9834-x

    Google Scholar 

  14. Grill A, Cleary DFR, Stettmer C, Bräu M, Settele J (2008) A mowing experiment to evaluate the influence of management on the activity of host ants of Maculinea butterflies. J Insect Conserv 12:617–627. doi:10.1007/s10841-007-9098-1

    Article  Google Scholar 

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

    Google Scholar 

  16. Hardie DC, Hutchings JA (2010) Evolutionary ecology at the extremes of species’ ranges. Environ Rev 18:1–20. doi:10.1139/A09-014

    Article  Google Scholar 

  17. Hochberg M, Clarke R, Elmes G, Thomas J (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

    Article  Google Scholar 

  18. Johst K, Drechsler M, Thomas J, Settele J (2006) Influence of mowing on the persistence of two endangered large blue butterfly species: influence of mowing on butterfly persistence. J Appl Ecol 43:333–342. doi:10.1111/j.1365-2664.2006.01125.x

    Article  Google Scholar 

  19. Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342. doi:10.1146/annurev.ecolsys.38.091206.095622

    Article  Google Scholar 

  20. Kӧrösi Á, Szentirmai I, Batáry P, Kövér S, Örvössy N, Peregovits L (2014) Effects of timing and frequency of mowing on the threatened scarce large blue butterfly—a fine-scale experiment. Agric Ecosyst Environ 196:24–33

    Article  Google Scholar 

  21. Lakušić D, Blaženčić J, Ranđelović V, Butorac B, Vukojičić S, Zlatković B, Jovanović S, Šinžar-Sekulić J, Žukovec D, Ćalić I, Pavićević D (2005) Staništa Srbije: Priručnik sa opisima i osnovnim podacima. Institut za botaniku i botanička bašta “Jevremovac”, Biološki fakultet, Univerzitet u Beogradu, Ministarstvo za nauku i zaštitu životne sredine Republike Srbije, Beograd

  22. Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118. doi:10.2307/2937171

    Article  Google Scholar 

  23. Mouquet N, Thomas JA, Elmes GW, Clarke RT, Hochberg ME (2005) Population dynamics and conservation of a specialized predator: a case study of Maculinea arion. Ecol Monogr 75:525–542

    Article  Google Scholar 

  24. Munguira ML, Martín J (1999) Action plan for Maculinea butterflies in Europe. Council of Europe, Strasbourg

    Google Scholar 

  25. Nowicki P, Vrabec V (2011) Evidence for positive density-dependent emigration in butterfly metapopulations. Oecologia 167:657–665. doi:10.1007/s00442-011-2025-x

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nowicki P, Richter A, Glinka U, Holzschuh A, Toelke U, Henle K, Woyciechowski M, Settele J (2005a) Less input same output: simplified approach for population size assessment in Lepidoptera. Popul Ecol 47:203–212. doi:10.1007/s10144-005-0223-2

  27. Nowicki P, Settele J, Thomas JA, Woyciechowski M (2005b) A review of population structure of Maculinea butterflies. In: Settele J, Kühn E, Thomas J (eds) Studies on the ecology and conservation of butterflies in Europe Vol. 2: species ecology along a European gradient: Maculinea butterflies as a model. Pensoft, Sofia-Moscow, pp 144–149

  28. Nowicki P, Witek M, Skórka P, Settele J, Woyciechowski M (2005c) Population ecology of the endangered butterflies Maculinea teleius and M. nausithous and the implications for conservation. Popul Ecol 47:193–202. doi:10.1007/s10144-005-0222-3

  29. Nowicki P, Pepkowska A, Kudlek J, Skórka P, Witek M, Settele J, Woyciechowski M (2007) From metapopulation theory to conservation recommendations: lessons from spatial occurrence and abundance patterns of Maculinea butterflies. Biol Conserv 140:119–129. doi:10.1016/j.biocon.2007.08.001

    Article  Google Scholar 

  30. Nowicki P, Bonelli S, Barbero F, Balletto E (2009) Relative importance of density-dependent regulation and environmental stochasticity for butterfly population dynamics. Oecologia 161:227–239. doi:10.1007/s00442-009-1373-2

    Article  PubMed  Google Scholar 

  31. Nowicki P, Vrabec V, Binzenhöfer B, Feil J, Zakšek B, Hovestadt T, Settele J (2014) Butterfly dispersal in inhospitable matrix: rare, risky, but long-distance. Landsc Ecol 29:401–412. doi:10.1007/s10980-013-9971-0

    Article  Google Scholar 

  32. Popović M (2016) Distribution, ecology and local spatial ecology of the scarce large blue butterfly in Serbia. In: 12th Symposium on the Flora of Southeastern Serbia and Neighbouring Regions: Book of Abstracts. University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Biological Society “Dr Sava Petrović,” Kopaonik, p 63

  33. Popović M, Šašić M (2016) New findings of the butterfly Phengaris teleius at the border between Hungary and Serbia (Lepidoptera: Lycaenidae). Biodivers Data J 4:e8078. doi:10.3897/BDJ.4.e8078

    Article  Google Scholar 

  34. Popović M, Radaković M, Đurđević A, Franeta F, Verovnik R (2014a) Distribution and threats of Phengaris teleius (Lepidoptera: Lycaenidae) in Northern Serbia. Acta Zool Hungarica 60:173–183

  35. Popović M, Radevski Đ, Miljević M, Đurić M (2014b) First record of Pyrgus cinarae (Lepidoptera: Hesperiidae) in Serbia. Acta Entomol Serbica 19:45–51

  36. Schwarz CJ, Seber GA (1999) Estimating animal abundance: review III. Stat Sci 14:427–456

    Article  Google Scholar 

  37. Settele J, Thomas J, Kühn E (eds) (2005) Studies on the ecology and conservation of butterflies in Europe Vol. 2: Species ecology along a European gradient: Maculinea butterflies as a model. Pensoft, Sofia-Moscow

    Google Scholar 

  38. Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436. doi:10.1146/annurev.ecolsys.110308.120317

    Article  Google Scholar 

  39. Tabashnik BE (1980) Population structure of Pierid butterflies. III. Pest Populations of Colias philodice eriphyle. Oecologia 47:175–183

    Article  PubMed  Google Scholar 

  40. Tartally A, Varga Z (2008) Host ant use of Maculinea teleius in the Carpathian Basin (Lepidoptera: Lycaenidae). Acta Zool Hungary 54:257–268

    Google Scholar 

  41. Thomas J (1984) The behaviour and habitat requirements of Maculinea nausithous (the dusky large blue butterfly) and M. teleius (the scarce large blue) in France. Biol Conserv 28:325–347

    Article  Google Scholar 

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

    Google Scholar 

  43. Thomas JA, Elmes GW, Schönrogge K, Simcox DJ, Settele J (2005) Primary hosts, secondary hosts and “non-hosts”: common confusions in the interpretation of host specificity in Maculinea butterflies and other social parasites of ants. In: Settele J, Thomas J, Kühn E (eds) Studies on the ecology and conservation of butterflies in Europe Vol. 2: species ecology along a European gradient: Maculinea butterflies as a model. Pensoft, Sofia-Moscow, pp 99–104

    Google Scholar 

  44. Thomas JA, Simcox DJ, Clarke RT (2009) Successful conservation of a threatened Maculinea butterfly. Science 325:80–83. doi:10.1126/science.1175726

    CAS  Article  PubMed  Google Scholar 

  45. van Langevelde F, Wynhoff I (2009) What limits the spread of two congeneric butterfly species after their reintroduction: quality or spatial arrangement of habitat? Anim Conserv 12:540–548. doi:10.1111/j.1469-1795.2009.00281.x

    Article  Google Scholar 

  46. Van Swaay C, Wynhoff I, Verovnik R, Wiemers M, Munguira ML, Maes D, Šašić M, Verstrael T, Warren M, Settele J (2010) Phengaris teleius. The IUCN Red List of Threatened Species. In: IUCN Red List Threat. Species. http://www.iucnredlist.org/details/12664/1. Accessed 21 Oct 2015

  47. Vodă R, Timuș N, Paulini I, Popa R, Mihali C, Crişan A, Rákosy L (2010) Demographic parameters of two sympatric Maculinea species in a Romanian site (Lepidoptera: Lycaenidae). Entomol Romanica 15:25–32

    Google Scholar 

  48. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139

    Article  Google Scholar 

  49. Witek M, Sliwinska EB, Skórka P, Nowicki P, Settele J, Woyciechowski M (2006) Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects. Oecologia 148:729–733. doi:10.1007/s00442-006-0404-5

    Article  PubMed  Google Scholar 

  50. Witek M, Nowicki P, Śliwińska EB, Skórka P, Settele J, Schönrogge K, Woyciechowski M (2010) Local host ant specificity of Phengaris (Maculinea) teleius butterfly, an obligatory social parasite of Myrmica ants. Ecol Entomol 35:557–564. doi:10.1111/j.1365-2311.2010.01213.x

    Article  Google Scholar 

  51. Wynhoff I (1998a) Lessons from the reintroduction of Maculinea teleius and M. nausithous in the Netherlands. J Insect Conserv 2:47–57

  52. Wynhoff I (1998b) REVIEW: the recent distribution of the European Maculinea species. J Insect Conserv 2:15–27

  53. Wynhoff I (2001) At home on foreign meadows: the reintroduciton of two Maculinea butterfly species. Wageningen University, Wageningen

    Google Scholar 

  54. Wynhoff I, Munguira ML (2001) Action plan for Maculinea Butterflies in Europe.

  55. Wynhoff I, van Gestel R, van Swaay C, van Langevelde F (2011) Not only the butterflies: managing ants on road verges to benefit Phengaris (Maculinea) butterflies. J Insect Conserv 15:189–206. doi:10.1007/s10841-010-9337-8

    Article  Google Scholar 

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Acknowledgments

This study was financed by the Butterfly Conservation Europe and Rufford Small Grants Project No. 14884-2, with kind support from Public Enterprise “Palić-Ludaš”. MP and JCI were supported by Grants No. 173025 and 1613051 of Ministry of Education, Science and Technological Development of Republic of Serbia. Positive opinion, allowing field studies, was obtained from the Serbian Institute for Nature Protection, No. 019-1290/2. We would like to give special thanks to anonymous reviewers and the editors for kind and constructive comments and Martin Gascoigne-Pees for valuable language corrections of the manuscript.

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Correspondence to Miloš Popović.

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Popović, M., Šašić, M., Medenica, I. et al. Living on the edge: population ecology of Phengaris teleius in Serbia. J Insect Conserv 21, 401–409 (2017). https://doi.org/10.1007/s10841-016-9922-6

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Keywords

  • Maculinea teleius
  • Mark-release-recapture
  • Butterfly conservation
  • Density dependence
  • Dispersal