Journal of Insect Conservation

, Volume 21, Issue 3, pp 559–571 | Cite as

Isolated Asian steppe element in the Balkans: habitats of Proterebia afra (Lepidoptera: Nymphalidae: Satyrinae) and associated butterfly communities

  • Alena Bartoňová
  • Vojtěch Kolář
  • Jana Marešová
  • Martina Šašić
  • Jana Šlancarová
  • Pavel Sucháček
  • Martin Konvička


A characteristic butterfly of Asian steppes, Proterebia afra (Fabricius 1787), was studied in its two relic areas of occurrence within the Balkans—the Askion Mts (a single mountain massif in NW Greece) and Dalmatia (karstic inland S Croatia)—together with co-occurring butterfly communities during its early spring adult flight period. P. afra adults tolerate harsh continental conditions prevailing at its localities during its flight. Local densities were higher in the Askion Mts (up to 100 individuals per 50 m walk) than in Dalmatia (up to 30 individuals per 50 m). Within both areas of occurrence, it inhabits dry grasslands subject to intermediate grazing pressure that retains enough dry grass litter but still suppresses shrubs and trees. Hotter slopes are preferred in more northerly Dalmatia than in the more southerly Askion Mts. More co-occurring butterfly species and more Mediterranean species were recorded in the Askion Mts (69 vs 63; 23 vs 12), but more butterfly individuals and higher species’ richness per transect were observed in Dalmatia. In ordination analyses, the main gradients organising the grassland butterfly communities distinguished between grassy plains and rocky slopes containing more woody plants. Given the distribution extents, local densities and present land use conditions, the Balkan P. afra is not currently endangered, but this may swiftly change with grazing abandonment, especially in Dalmatia, and some conservation actions should be considered in the near future.


Proterebia afra Proterebia phegea Butterfly communities Mediterranean grasslands The Balkans Steppe 



This work was supported by The Explorers Club Exploration Fund, FAN(B), the University of South Bohemia in Ceske Budejovice (04-168/2013/P and 152/2016/P), and by the Czech Science Foundation (GACR 14-33733S). We would like to thank the Greek Ministry of Environment, Energy and Climate Change (research permit No. 170916/1344), Croatian Ministry of Environmental and Nature Protection (517-07-1-1-1-15-5) and our friends and colleagues who offered their assistance: Z. Faltýnek Fric, Z. Kolev, M. Krausová, R. Kučmerčík, R. Verovnik and M. Zapletal.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10841_2017_9995_MOESM1_ESM.docx (79 kb)
Supplementary material 1 (DOCX 79 KB)


  1. Allen JRM, Brandt U, Brauer A, Hubberten H-W, Huntley B, Keller J, Kraml M, Mackensen A, Mingram J, Negendank JFW, Nowaczyk NR, Oberhansli H, Watts WA, Wulf S, Zolitschka B (1999) Rapid environmental changes in southern Europe during the last glacial period. Nature 400:740–743. doi: 10.1038/23432 CrossRefGoogle Scholar
  2. Androulakakis N (2012) Geological Map of Greece [Internet]. c2012–2016. Using: ArcGIS [GIS software]. Version 10.0. Redlands (CA): Environmental Systems Research Institute. Accessed 10 Nov 2016
  3. Aufgebauer A, Panagiotopoulos K, Wagner B, Schaebitz F, Viehberg FA, Vogel H, Zanchetta G, Sulpizio R, Leng MJ, Damaschke M (2012) Climate and environmental change in the Balkans over the last 17 ka recorded in sediments from Lake Prespa (Albania/F.Y.R. of Macedonia/Greece). Quatern Int 274:122–135. doi: 10.1016/j.quaint.2012.02.015 CrossRefGoogle Scholar
  4. Cremene C, Groza G, Rakosy L, Schileyko AA, Baur A, Erhardt A, Baur B (2005) Alterations of steppe-like grasslands in Eastern Europe: a threat to regional biodiversity hotspots. Conserv Biol 19:1606–1618. doi: 10.1111/j.1523-1739.2005.00084.x CrossRefGoogle Scholar
  5. de Jong Y, Verbeek M, Michelsen V, Bjørn P de P, Los W, Steeman F, Bailly N, Basire C, Chylarecki P, Stloukal E et al (2014) Fauna Europaea—all European animal species on the web. Biodivers Data J 2:e4034. doi: 10.3897/BDJ.2.e4034 CrossRefGoogle Scholar
  6. Debussche M, Lepart J, Dervieux A (1999) Mediterranean landscape changes: evidence from old postcards. Glob Ecol Biogeogr 8:3–15. doi: 10.1046/j.1365-2699.1999.00316.x CrossRefGoogle Scholar
  7. Deodati T, Cesaroni D, Sbordoni V (2009) Molecular phylogeny, classification, and biogeographic origin of Callerebia and other related Sino-Himalayan genera (Insecta: Lepidoptera: Nymphalidae: Satyrinae). In: Hartmann M, Weipert J (eds) Biodiversität und Naturausstattung im Himalaya III (Biodiversity and natural heritage of the Himalaya III). Verein der Freunde und Förderer des Naturkundemuseums, Erfurt, pp 107–114Google Scholar
  8. Dercourt J, Zonenshain LP, Ricou L-E, Kazmin VG, Le Pichon X, Knipper AL, Grandjacquet C, Sbortshikov IM, Geyssant J, Lepvrier C, Pechersky DH, Boulin J, Sibuet JC, Savostin LA, Sorokhtin O, Westphal M, Bazhenov ML, Lauer JP, Biju-Duval B (1986) Geological evolution of the tethys belt from the atlantic to the pamirs since the LIAS. Tectonophysics 123:241–315. doi: 10.1016/0040-1951(86)90199-X CrossRefGoogle Scholar
  9. Dewey JF, Pitman WC, Ryan WBF, Bonnin J (1973) Plate tectonics and the evolution of the alpine system. Geol Soc Am Bull 84:3137–3180. doi: 10.1130/0016-7606(1973)84<3137:PTATEO>2.0.CO;2 CrossRefGoogle Scholar
  10. Eichel S, Fartmann T (2008) Management of calcareous grasslands for Nickerl’s fritillary (Melitaea aurelia) has to consider habitat requirements of the immature stages, isolation, and patch area. J Insect Conserv 12:677–688. doi: 10.1007/s10841-007-9110-9 CrossRefGoogle Scholar
  11. Ekroos J, Heliölä J, Kuussaari M (2010) Homogenization of lepidopteran communities in intensively cultivated agricultural landscapes. J Appl Ecol 47:459–467. doi: 10.1111/j.1365-2664.2009.01767.x CrossRefGoogle Scholar
  12. ESRI (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, RedlandsGoogle Scholar
  13. Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642. doi: 10.1038/342637a0 CrossRefGoogle Scholar
  14. Hambäck PA, Summerville KS, Steffan-Dewenter I, Krauss J, Englund G, Crist TO (2007) Habitat specialization, body size, and family identity explain lepidopteran density–area relationships in a cross-continental comparison. Proc Natl Acad Sci USA 104:8368–8373. doi: 10.1073/pnas.0611462104 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hesselbarth G, Oorschot H van, Wagener S (1995) Die Tagfalter der Türkei unter Berücksichtigung der angrenzenden Länder. Goecke & Evers, KeltnerGoogle Scholar
  16. Jepson P, Schepers F (2016) Making space for rewilding: Creating and enabling policy environment. University of Oxford, Oxford. doi: 10.13140/RG.2.1.1783.1287 Google Scholar
  17. Johnson CN (2009) Ecological consequences of Late Quaternary extinctions of megafauna. Proc R Soc B 276:2509–2519. doi: 10.1098/rspb.2008.1921 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jutzeler D, Lafranchis T (2011) Die Larvalstadien von Proterebia afra pyramus (de Louker) aus dem Norden Griechenlands. Larvalentwicklung der dalmatinischen P. afra dalmata (Godart, 1824) im Vergleich und zur Geschichte des Namens unserer Art (Lepidoptera Nymphalidae, Satyrinae). Entomol Romanica 16:5–18Google Scholar
  19. Kadlec T, Vrba P, Kepka P, Schmitt T, Konvicka M (2010) Tracking the decline of the once-common butterfly: delayed oviposition, demography and population genetics in the hermit Chazara briseis. Anim Conserv 13:172–183. doi: 10.1111/j.1469-1795.2009.00318.x CrossRefGoogle Scholar
  20. Koren T, Trkov D (2011) Proterebia afra damlata (Godart, 1824) (Lepidoptera, Satyrinae) recorded for the first time in Bosnia and Hercegovina. Nat Slov 13:57–58Google Scholar
  21. Koren T, Burić I, Štih A, Zakšek V, Verovnik (2010) New data about the distribution and altitudinal span of the Dalmatian Ringlet, Proterebia afra dalmata (Godart, [1824]) (Lepidoptera: Satyrinae) in Croatia = Novi podatki o razširjenosti in razponu nadmorskih višin pojavljanja dalmatinskega rjavčka, Proterebia afra dalmata (Godart, [1824]) (Lepidoptera: Satyrinae) na Hrvaškem. Acta Entomol Slov 18:143–150Google Scholar
  22. Kruess A, Tscharntke T (2002) Grazing intensity and the diversity of grasshoppers, butterflies, and trap-nesting bees and wasps. Conserv Biol 16:1570–1580. doi: 10.1046/j.1523-1739.2002.01334.x CrossRefGoogle Scholar
  23. Kryštufek B, Griffiths HI (2002) Species richness and rarity in european rodents. Ecography 25:120–128. doi: 10.1034/j.1600-0587.2002.250114.x CrossRefGoogle Scholar
  24. Kudrna O, Harpke A, Lux K, Pennerstorfer J, Schweiger O, Settele J, Wiemers M (2011) Distribution Atlas of Butterflies in Europe. Gesellschaft für Schmetterlingsschutz, HalleGoogle Scholar
  25. Kudrna O, Pennerstorfer J, Lux K (2015) Distribution atlas of European butterflies and skippers. Wiss. Verl. Peks., SchwanfeldGoogle Scholar
  26. Lawton JH (1993) Range, population abundance and conservation. Trends Ecol Evol 8:409–413. doi: 10.1016/0169-5347(93)90043-O CrossRefPubMedGoogle Scholar
  27. Loeffler F, Stuhldreher G, Fartmann T (2013) How much care does a shrub-feeding hairstreak butterfly, Satyrium spini (Lepidoptera: Lycaenidae), need in calcareous grasslands? Eur J Entomol 110:145–152. doi: 10.14411/eje.2013.020 CrossRefGoogle Scholar
  28. Loos J, Dorresteijn I, Hanspach J, Fust P, Rakosy L, Fischer J (2014) Low-intensity agricultural landscapes in transylvania support high butterfly diversity: implications for conservation. PLoS ONE 9:e103256. doi: 10.1371/journal.pone.0103256 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Magyari EK, Chapman JC, Gaydarska B, Marinova E, Deli T, Huntley JP, Allen JRM, Huntley B (2008) The “oriental” component of the Balkan flora: evidence of presence on the Thracian Plain during the Weichselian late-glacial. J Biogeogr 35:865–883. doi: 10.1111/j.1365-2699.2007.01849.x CrossRefGoogle Scholar
  30. Mazzoleni S, Pasquale G di, Mulligan M, Martino P di, Rego F (2008) Recent dynamics of the mediterranean vegetation and landscape. Wiley, ChichesterGoogle Scholar
  31. Mihoci I, Šašić M (2005) New findings of the butterfly Dalmatian Ringlet, Proterebia afra dalmata (Godart, [1824]) (Lepidoptera, Satyrinae) in Croatia. Nat Croat 14:121–129Google Scholar
  32. Mihoci I, Šašić M. (2007) New distribution data on the endemic butterfly Proterebia afra dalmata (Godart, [1824]) (Nymphalidae, Satyrinae) in Croatia. Nat Croat 16:205–210Google Scholar
  33. Milberg P, Akoto B, Bergman K-O, Fogelfors H, Paltto H, Talle M (2014) Is spring burning a viable management tool for species rich grasslands? Appl Veg Sci 17:429–441. doi: 10.1111/avsc.12091 CrossRefGoogle Scholar
  34. Mittermeier RA, Gil PR, Hoffman M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Fonseca GAB da, Seligmann PA, Ford H (2005) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions, 1st edn. Conservation International, Mexico CityGoogle Scholar
  35. Möllenbeck V, Hermann G, Fartmann T (2009) Does prescribed burning mean a threat to the rare satyrine butterfly Hipparchia fagi? Larval-habitat preferences give the answer. J Insect Conserv 13:77–87. doi: 10.1007/s10841-007-9128-z CrossRefGoogle Scholar
  36. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. doi: 10.1038/35002501 CrossRefPubMedGoogle Scholar
  37. Numa C, van Swaay C, Wynhoff I, Wiemers M, Barrios V, Allen D, Sayer C, Lopéz Munguira M, Balletto E, Benyamini D, Beshkov S, Bonelli S, Caruana R, Dapporto L, Franeta F, Garcia-Pereira P, Karacetin E, Katbeh-Bader A, Maes D, Micevski N, Miller R, Monteiro E, Moulai R, Nieto A, Pamperis L, Peer G, Power A, Sasic M, Thompson K, Tzirkalli E, Verovnik R, Warren M, Welch H (2016) The status and distribution of Mediterranean butterflies. IUCN, MalagaCrossRefGoogle Scholar
  38. Nylin S, Bergström A (2009) Threat status in butterflies and its ecological correlates: how far can we generalize? Biodivers Conserv 18:3243. doi: 10.1007/s10531-009-9640-4 CrossRefGoogle Scholar
  39. Örvössy N, Kőrösi Á, Batáry P, Vozár Á, Peregovits L (2013) Potential metapopulation structure and the effects of habitat quality on population size of the endangered False Ringlet butterfly. J Insect Conserv 17:537–547. doi: 10.1007/s10841-012-9538-4 CrossRefGoogle Scholar
  40. Pamperis LN (2009) The butterflies of Greece. Editions Pamperis, AthensGoogle Scholar
  41. Pamperis LN (2011) The presence of Proterebia afra (Fabricius, 1787) (Lepidoptera: Satyridae) in the Rhodope Mts, NE. Greece. Entomol Gaz 62.Google Scholar
  42. Peña C, Witthauer H, Klečková I, Fric Z, Wahlberg N (2015) Adaptive radiations in butterflies: evolutionary history of the genus Erebia (Nymphalidae: Satyrinae). Biol J Linn Soc 116:449–467. doi: 10.1111/bij.12597 CrossRefGoogle Scholar
  43. Pokluda P, Hauck D, Cizek L (2012) Importance of marginal habitats for grassland diversity: fallows and overgrown tall-grass steppe as key habitats of endangered ground-beetle Carabus hungaricus. Insect Conserv Diver 5: 27–36. doi: 10.1111/j.1752-4598.2011.00146.x CrossRefGoogle Scholar
  44. Pollard E (1977) A method for assessing changes in the abundance of butterflies. Biol Conserv 12:115–134. doi: 10.1016/0006-3207(77)90065-9 CrossRefGoogle Scholar
  45. Polunin O (1980) Flowers of Greece and the Balkans: a field guide. Oxford University Press, OxfordGoogle Scholar
  46. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  47. Radovic J, Civic K, Topic R, Posavec Vukelic V (eds) (2009) Biodiversity of Croatia. State institute for nature protection. Ministry of Culture—Republic of Croatia, ZagrebGoogle Scholar
  48. Roos P, Arnscheid W, Stangelmaier G, Beil B (1984) Praimaginale Merkmale in der Gattung Proterebia Roos & Arnscheid: Beweise fur die phylogenetische Distanz zur Gattung Erebia Dalman (Satyridae). Nota Lepidopterol 7:361–374Google Scholar
  49. Ryan WBF, Pitman WC, Major CO, Shimkus K, Moskalenko V, Jones GA, Dimitrov P, Gorür N, Sakinç M, Yüce H (1997) An abrupt drowning of the Black Sea shelf. Mar Geol 138:119–126. doi: 10.1016/S0025-3227(97)00007-8 CrossRefGoogle Scholar
  50. Sagarin RD, Gaines SD (2002) The “abundant centre” distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147. doi: 10.1046/j.1461-0248.2002.00297.x CrossRefGoogle Scholar
  51. Sandom CJ, Ejrnæs R, Hansen MDD, Svenning JC (2014) High herbivore density associated with vegetation diversity in interglacial ecosystems. Proc Natl Acad Sci USA 111:4162–4167. doi: 10.1073/pnas.1311014111 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sasic M, Mihoci I, Kucinic M (2013) Crveni popis danjih leptira Hrvatske. Drzavni zavod za zastitu prirode, Ministarstvo zastite okolisa i prirode, Zagreb. Accessed 6 Feb 2017
  53. Shreeve TG, Dennis RLH, Roy DB, Moss D (2001) An ecological classification of British butterflies: ecological attributes and biotope occupancy. J Insect Conserv 5:145–161. doi: 10.1023/A:1017556113534 CrossRefGoogle Scholar
  54. Slamova I, Klecka J, Konvicka M (2011) Diurnal behavior and habitat preferences of Erebia aethiops, an Aberrant Lowland Species of a Mountain Butterfly Clade. J Insect Behav 24:230–246. doi: 10.1007/s10905-010-9250-8 CrossRefGoogle Scholar
  55. Slancarova J, Vrba P, Platek M, Zapletal M, Spitzer L, Konvicka M (2015) Co-occurrence of three Aristolochia-feeding Papilionids (Archon apollinus, Zerynthia polyxena and Zerynthia cerisy) in Greek Thrace. J Nat Hist 49:1825–1848. doi: 10.1080/00222933.2015.1006281 CrossRefGoogle Scholar
  56. Slancarova J, Bartonova A, Zapletal M, Kotilinek M, Fric ZF, Micevski N, Kati V, Konvicka M (2016) Life history traits reflect changes in mediterranean butterfly communities due to forest encroachment. PLoS ONE 11:e0152026. doi: 10.1371/journal.pone.0152026 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Stuhldreher G, Fartmann T (2014) When habitat management can be a bad thing: effects of habitat quality, isolation and climate on a declining grassland butterfly. J Insect Conserv 18:965–979. doi: 10.1007/s10841-014-9704-y CrossRefGoogle Scholar
  58. Svenning J-C, Pedersen PBM, Donlan J, Ejrnaesd R, Faurbya S, Galettie M, Hansen DM, Sandel B, Sandom CJ, Terborgh JW, Vera FWM (2015) Science for a wilder Anthropocene: synthesis and future directions for trophic rewilding research. Proc Natl Acad Sci USA 113:898–906. doi: 10.1073/pnas.1502556112 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ter Braak CJF, Šmilauer P (2012) CANOCO Reference Manual and User’s Guide: Software for Ordination (version 5.0). Biometris, WageningenGoogle Scholar
  60. Thomas JA, Rose RJ, Clarke RT, Thomas CD, Webb NR (1999) Intraspecific variation in habitat availability among ectothermic animals near their climatic limits and their centres of range. Funct Ecol 13:55–64. doi: 10.1046/j.1365-2435.1999.00008.x CrossRefGoogle Scholar
  61. Tolman T, Lewington R (2008) Collins butterfly guide: the Most complete field guide to the butterflies of Britain and Europe. Collins, LondonGoogle Scholar
  62. Tshikolovets VV, Kosterin O, Gorbunov P, Yakovlev R (2016) The butterflies of Kazakhstan. Tshikolovets, KievGoogle Scholar
  63. Tvrtković N, Verovnik R, Lovrenčić L, Vuković M, Šašić M (2015) New contributions to the butterfly fauna of Mt Velebit and the neighbouring area of Lika (Croatia). Nat Croat 24:281–292.CrossRefGoogle Scholar
  64. Van Andel TH, Tzedakis PC (1996) Palaeolithic landscapes of Europe and environs, 150,000–25,000 years ago: an overview. Quat Sci Rev 15:481–500. doi: 10.1016/0277-3791(96)00028-5 CrossRefGoogle Scholar
  65. van Strien AJ, van Swaay CAM, Kery M (2011) Metapopulation dynamics in the butterfly Hipparchia semele changed decades before occupancy declined in The Netherlands. Ecol Appl 21:2510–2520. doi: 10.2307/41416675 CrossRefPubMedGoogle Scholar
  66. Vermeire LT, Gillen RL (2001) Estimating herbage standing crop with visual obstruction in tallgrass prairie. J Range Manag 54:57–60. doi: 10.2458/azu_jrm_v54i1_vermeire CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Alena Bartoňová
    • 1
    • 2
  • Vojtěch Kolář
    • 1
    • 2
    • 3
  • Jana Marešová
    • 1
    • 2
  • Martina Šašić
    • 4
  • Jana Šlancarová
    • 1
    • 2
  • Pavel Sucháček
    • 3
  • Martin Konvička
    • 1
    • 2
  1. 1.Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  2. 2.Institute of EntomologyBiology Centre CASCeske BudejoviceCzech Republic
  3. 3.Faculty of AgricultureCeske BudejoviceCzech Republic
  4. 4.Croatian Natural History MuseumZagrebCroatia

Personalised recommendations