Disentangling the effects of host resources, local, and landscape variables on the occurrence pattern of the dusky large blue butterfly (Phengaris nausithous) in upland grasslands

  • Antonio J. Pérez-SánchezEmail author
  • Anett Schibalski
  • Boris Schröder
  • Sebastian Klimek
  • Jens Dauber


Determining the effects of local and landscape drivers on endangered species and predicting potential suitable habitats for their persistence is crucial for effective conservation management. Here, we applied a multi-scale approach to disentangle the effects of host resources, local, and landscape variables on the occurrence pattern of Phengaris (= Maculinea) nausithous in semi-natural upland grasslands. Our approach comprised the assessment of host parameters (plant cover, density, height, flower heads density, ant nest density, ant colony size), local grassland management (pasture, meadow), site conditions (area, shape, terrain attributes), and landscape variables (landscape composition, connectivity). We used ensemble of small models based on bivariate generalized linear models for explaining and predicting the butterfly occurrence pattern. Bivariate models revealed that host ant nest density, plant cover and height, local grassland management type (pasture), slope and eastness, landscape forest cover and grassland connectivity had a positive effect on the occurrence of P. nausithous (average explained deviance 20.5%). Host ant density, host plant cover, and local grassland management were the most influential factors on the ensemble predictions. The presence of P. nausithous in upland grasslands is not only determined by host resources, but also by local and landscape factors. Such factors proved to be relevant for identifying and predicting suitable grassland sites for this endangered species. Consequently, we recommend that conservation actions should include a landscape perspective to promote connectivity by facilitating coherent grazing networks enabling dispersal between semi-natural upland grasslands and thus species persistence.


Butterfly conservation Connectivity Ensemble of small models Grazing Land use Site occupancy 



We are grateful to Katja Steininger, Ute Petersen, Elke Tietz, Maren Darnauer, Gerd Kuna, and the land owners for their assistance in carrying out the fieldwork. We also thank Stefan Mecke, Antonia Ortmann, Clara van Waveren and Jan Thiele for their support with GIS analysis and valuable comments on the R appendix. Finally, the authors are grateful to Piotr Nowicki, Josef Settele and an anonymous reviewer for their constructive comments on an earlier draft which improved the manuscript considerably. This study was funded by a research Grant (Grant No. 91563454) from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) to Antonio J. Pérez-Sánchez.


This study was funded by a research Grant (Grant No. 91563454) from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) to Antonio J. Pérez-Sánchez.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

No specimens of P. nausithous or S. officinalis were collected in accordance with the Habitats Directive (Annex II + IV) and Bern Convention (Annex II) conservation actions, and standard methods were followed for ant data collection.

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  1. Anton C, Musche M, Hula V, Settele J (2005) Which factors determine the population density of the predatory butterfly Maculinea nausithous? In: Settele J, Kühn E, Thomas J (eds) Studies on the ecology and conservation of European, butterflies in Europe. Species ecology along a gradient: Maculinea butterflies as a model, vol 2. Pensoft, Sofia, pp 57–59Google Scholar
  2. Anton C, Musche M, Hula V, Settele J (2008) Myrmica host-ants limit the density of the ant-predatory large blue Maculinea nausithous. J Insect Conserv 12:511–517. CrossRefGoogle Scholar
  3. Arndt E, Grunert H, Schuler J (2011) Influence of inundation pattern on the epigaean ant fauna in a European floodplain forest complex (Hymenoptera: Formicidae). Entomol Gen 33:39–48. CrossRefGoogle Scholar
  4. Ashcroft MB, Chisholm LA, French KO (2008) The effect of exposure on landscape scale soil surface temperatures and species distribution models. Landsc Ecol 23:211–225. CrossRefGoogle Scholar
  5. Barua M, Gurdak DJ, Ahmed RA, Tamuly J (2012) Selecting flagships for invertebrate conservation. Biodivers Conserv 21:1457–1476. CrossRefGoogle Scholar
  6. Batáry P, Kőrösi Á, Örvössy N et al (2009) Species-specific distribution of two sympatric Maculinea butterflies across different meadow edges. J Insect Conserv 13:223–230. CrossRefGoogle Scholar
  7. Beers TW, Dress PE, Wensel LC (1966) Aspect transformation in site productivity research. J For 64:691–692. CrossRefGoogle Scholar
  8. Bengtsson J, Bullock JM, Egoh B et al (2019) Grasslands—more important for ecosystem services than you might think. Ecosphere 10:1–20. CrossRefGoogle Scholar
  9. Bennie J, Huntley B, Wiltshire A et al (2008) Slope, aspect and climate: Spatially explicit and implicit models of topographic microclimate in chalk grassland. Ecol Modell 216:47–59. CrossRefGoogle Scholar
  10. Beukema W, Martel A, Nguyen TT et al (2018) Environmental context and differences between native and invasive observed niches of Batrachochytrium salamandrivorans affect invasion risk assessments in the Western Palearctic. Divers Distrib 24:1788–1801. CrossRefGoogle Scholar
  11. Binzenhöfer B, Schröder B, Strauss B et al (2005) Habitat models and habitat connectivity analysis for butterflies and burnet moths—the example of Zygaena carniolica and Coenonympha arcania. Biol Conserv 126:247–259. CrossRefGoogle Scholar
  12. Binzenhöfer B, Biedermann R, Settele J, Schröder B (2008) Connectivity compensates for low habitat quality and small patch size in the butterfly Cupido minimus. Ecol Res 23:259–269. CrossRefGoogle Scholar
  13. Breiner FT, Guisan A, Bergamini A, Nobis MP (2015) Overcoming limitations of modelling rare species by using ensembles of small models. Methods Ecol Evol 6:1210–1218. CrossRefGoogle Scholar
  14. Broennimann O, Di Cola V, Guisan A (2018) ecospat: spatial ecology miscellaneous methods. R package version 3.0.
  15. Curtis RJ, Brereton TM, Dennis RLH et al (2015) Butterfly abundance is determined by food availability and is mediated by species traits. J Appl Ecol 52:1676–1684. CrossRefGoogle Scholar
  16. Dauber J, Wolters V (2004) Edge effects on ant community structure and species richness in an agricultural landscape. Biodivers Conserv 13:901–915. CrossRefGoogle Scholar
  17. Della Rocca F, Bogliani G, Milanesi P (2017) Patterns of distribution and landscape connectivity of the stag beetle in a human-dominated landscape. Nat Conserv 19:19–37. CrossRefGoogle Scholar
  18. Deutscher Wetterdienst (2017) Deutsche Klimaatlas, Klima und Welt, Thuringia. Accessed 26 Apr 2019
  19. 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. CrossRefGoogle Scholar
  20. Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:027–046. CrossRefGoogle Scholar
  21. Dover J, Settele J (2009) The influences of landscape structure on butterfly distribution and movement: a review. J Insect Conserv 13:3–27. CrossRefGoogle Scholar
  22. Gillman R (2002) Geometry and gerrymandering. Math Horizons 10:10–12. CrossRefGoogle Scholar
  23. Habel JC, Dengler J, Janišová M et al (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodivers Conserv 22:2131–2138. CrossRefGoogle Scholar
  24. Halada L, Evans D, Romão C, Petersen JE (2011) Which habitats of European importance depend on agricultural practices? Biodivers Conserv 20:2365–2378. CrossRefGoogle Scholar
  25. Hovestadt T, Binzenhöfer B, Nowicki P, Settele J (2011) Do all inter-patch movements represent dispersal? A mixed kernel study of butterfly mobility in fragmented landscapes. J Anim Ecol 80:1070–1077. CrossRefPubMedGoogle Scholar
  26. Jansen SHDR, Holmgren M, van Langevelde F, Wynhoff I (2012) Resource use of specialist butterflies in agricultural landscapes: conservation lessons from the butterfly Phengaris (Maculinea) nausithous. J Insect Conserv 16:921–930. CrossRefGoogle Scholar
  27. Johst K, Drechsler M, Thomas J, Settele J (2006) Influence of mowing on the persistence of two endangered large blue butterfly species. J Appl Ecol 43:33–342. CrossRefGoogle Scholar
  28. Kajzer-Bonk J, Nowicki P, Bonk M et al (2013) Local populations of endangered Maculinea (Phengaris) butterflies are flood resistant. J Insect Conserv 17:1105–1112. CrossRefGoogle Scholar
  29. Kajzer-Bonk J, Skórka P, Nowicki P et al (2016) Relative contribution of matrix structure, patch resources and management to the local densities of two large blue butterfly species. PLoS ONE 11:e0168679. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kempe C, Nowicki P, Harpke A et al (2016) The importance of resource distribution: spatial co-occurrence of host plants and host ants coincides with increased egg densities of the Dusky Large Blue Maculinea nausithous (Lepidoptera: Lycaenidae). J Insect Conserv 20:1033–1045. CrossRefGoogle Scholar
  31. Kőrösi Á, Örvössy N, Batáry P et al (2012) Different habitat selection by two sympatric Maculinea butterflies at small spatial scale. Insect Conserv Divers 5:118–126. CrossRefGoogle Scholar
  32. Krämer B, Poniatowski D, Fartmann T (2012) Effects of landscape and habitat quality on butterfly communities in pre-alpine calcareous grasslands. Biol Conserv 152:253–261. CrossRefGoogle Scholar
  33. Krauss J, Steffan-Dewenter I, Tscharntke T (2003) How does landscape context contribute to effects of habitat fragmentation on diversity and population density of butterflies? J Biogeogr 30:889–900. CrossRefGoogle Scholar
  34. Krauss J, Bommarco R, Guardiola M et al (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Liivamägi A, Kuusemets V, Kaart T et al (2014) Influence of habitat and landscape on butterfly diversity of semi-natural meadows within forest-dominated landscapes. J Insect Conserv 18:1137–1145. CrossRefGoogle Scholar
  36. Loritz H, Settele J (2005) Effects of human land-use on availability and quality of habitats of the Large Blue butterfly. In: Settele J, Kühn E, Thomas JA (eds) Studies on the ecology and conservation of European, Butterflies in Europe. Species ecology along a gradient: Maculinea butterflies as a model, vol 2. Pensoft, Sofia, pp 225–227Google Scholar
  37. McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724. CrossRefPubMedGoogle Scholar
  38. McRae B, Shah V, Mohapatra T (2013) Circuitscape user guide. Nat Conserv 28Google Scholar
  39. Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145.;2 CrossRefGoogle Scholar
  40. Mortelliti A, Amori G, Boitani L (2010) The role of habitat quality in fragmented landscapes: a conceptual overview and prospectus for future research. Oecologia 163:535–547. CrossRefPubMedGoogle Scholar
  41. Munguira ML, Martín J (1999) Action plan for Maculinea butterflies in Europe. Nat Environ 97:1–72Google Scholar
  42. Musche M, Settele J (2005) Patterns of resource allocation and adaptive response to mowing in the plant Sanguisorba officinalis (Rosaceae). In: Settele J, Kühn E, Thomas J (eds) Studies on the ecology and conservation of butterflies in Europe: Species ecology along a European gradient: Maculinea butterflies as a model, vol 2. Pensoft, Sofia, p 228Google Scholar
  43. Nowicki P (2017) Survey precision moderates the relationship between population size and stability. Biol Conserv 212:310–315. CrossRefGoogle Scholar
  44. Nowicki P, Vrabec V (2011) Evidence for positive density-dependent emigration in butterfly metapopulations. Oecologia 167:657–665. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Nowicki P, Witek M, Skórka P et al (2005) Population ecology of the endangered butterflies Maculinea teleius and M. nausithous and the implications for conservation. Popul Ecol 47:193–202. CrossRefGoogle Scholar
  46. Nowicki P, Pepkowska A, Kudlek J et al (2007) From metapopulation theory to conservation recommendations: lessons from spatial occurrence and abundance patterns of Maculinea butterflies. Biol Conserv 140:119–129. CrossRefGoogle Scholar
  47. Nowicki P, Halecki W, Kalarus K (2013) All natural habitat edges matter equally for endangered Maculinea butterflies. J Insect Conserv 17:139–146CrossRefGoogle Scholar
  48. Nowicki P, Vrabec V, Binzenhöfer B et al (2014) Butterfly dispersal in inhospitable matrix: rare, risky, but long-distance. Landsc Ecol 29:401–412. CrossRefGoogle Scholar
  49. Nowicki P, Marczyk J, Kajzer-Bonk J (2015) Metapopulations of endangered Maculinea butterflies are resilient to large-scale fire. Ecohydrology 8:398–405. CrossRefGoogle Scholar
  50. Öckinger E, Smith HG (2006) Landscape composition and habitat area affects butterfly species richness in semi-natural grasslands. Oecologia 149:526–534. CrossRefPubMedGoogle Scholar
  51. Öckinger E, Lindborg R, Sjödin NE, Bommarco R (2012) Landscape matrix modifies richness of plants and insects in grassland fragments. Ecography 35:259–267. CrossRefGoogle Scholar
  52. Pellet J, Fleishman E, Dobkin DS et al (2007) An empirical evaluation of the area and isolation paradigm of metapopulation dynamics. Biol Conserv 136:483–495. CrossRefGoogle Scholar
  53. Pérez-Sánchez A, Zopt D, Klimek S, Dauber J (2018) Differential responses of ant assemblages (Hymenoptera: Formicidae) to long-term grassland management in Central Germany. Myrmecol News 27:13–23. CrossRefGoogle Scholar
  54. Plieninger T, Höchtl F, Spek T (2006) Traditional land-use and nature conservation in European rural landscapes. Environ Sci Policy 9:317–321. CrossRefGoogle Scholar
  55. Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman & Hall, LondonGoogle Scholar
  56. Poniatowski D, Stuhldreher G, Löffler F, Fartmann T (2018) Patch occupancy of grassland specialists: habitat quality matters more than habitat connectivity. Biol Conserv 225:237–244. CrossRefGoogle Scholar
  57. Ranius T, Nilsson SG, Franzén M (2011) How frequent is metapopulation structure among butterflies in grasslands? Occurrence patterns in a forest-dominated landscape in southern Sweden. Écoscience 18:138–144. CrossRefGoogle Scholar
  58. Schröder B, Richter O (2000) Are habitat models transferable in space and time? Zeitschrift für Ökologie und Naturschutz 8:195–205Google Scholar
  59. Schröder B, Strauss B, Biedermann R et al (2009) Predictive species distribution modelling in butterflies. In: Settele J, Shreeve TG, Konvicka M, van Dyck H (eds) Ecology of butterflies in Europe, 1st edn. Cambridge University Press, Cambridge, pp 62–78Google Scholar
  60. Science for Environment Policy, SEP (2017) Agri-environmental schemes: how to enhance the agriculture-environment relationship. Thematic Issue 57. Science Communication Unit, European Commission DG Environment, UWE, Bristol.
  61. Seifert B (2017) The ecology of Central European non-arboreal ants—37 years of a broad-spectrum analysis under permanent taxonomic control. Soil Org 89:1–67Google Scholar
  62. Seifert B (2018) The ants of Central and North Europe. lutra Verlags- und Vertriebsgesellschaft, Tauer, 408 ppGoogle Scholar
  63. Settele J, Henle K (2009) Grazing and cutting regimes for old grassland in temperate zones. In: Gherardi F, Corti C, Gualtieri M (eds) Biodiversity conservation and habitat management. Eolss Publishers, Oxford, pp 261–276Google Scholar
  64. Settele J, Kühn E (2009) Insect conservation. Science 80(325):41–42. CrossRefGoogle Scholar
  65. Skórka P, Witek M, Woyciechowski M (2006) A simple and nondestructive method for estimation of worker population size in Myrmica ant nests. Insectes Soc 53:97–100. CrossRefGoogle Scholar
  66. Skórka P, Nowicki P, Lenda M et al (2013) Different flight behaviour of the endangered scarce large blue butterfly Phengaris teleius (Lepidoptera: Lycaenidae) within and outside its habitat patches. Landsc Ecol 28:533–546. CrossRefGoogle Scholar
  67. Smith RS, Shiel RS, Millward D et al (2002) Soil seed banks and the effects of meadow management on vegetation change in a 10-year meadow field trial. J Appl Ecol 39:279–293. CrossRefGoogle Scholar
  68. Spitzer L, Benes J, Dandova J et al (2009) The large Blue butterfly, Phengaris [Maculinea] arion, as a conservation umbrella on a landscape scale: the case of the Czech Carpathians. Ecol Indic 9:1056–1063. CrossRefGoogle Scholar
  69. Tartally A, Thomas JA, Anton C et al (2019) Patterns of host use by brood parasitic Maculinea butterflies across Europe. Philos Trans R Soc B Biol Sci 374:20180202. CrossRefGoogle Scholar
  70. Thomas JA (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. CrossRefGoogle Scholar
  71. 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 B Biol Sci 268:471–477. CrossRefGoogle Scholar
  72. Thomas CD, Hanski I (1997) Butterfly metapopulations. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Elsevier, Amsterdam, pp 359–386CrossRefGoogle Scholar
  73. Thomas JA, Simcox DJ, Wardlaw JC et al (1998) Effects of latitude, altitude and climate on the habitat and conservation of the endangered butterfly Maculinea arion and its Myrmica ant hosts. J Insect Conserv 2:39–46. CrossRefGoogle Scholar
  74. Thomas JA, Bourn NAD, Clarke RT et al (2001) The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proc R Soc B Biol Sci 268:1791–1796. CrossRefGoogle Scholar
  75. Thuiller W, Georges D, Engler R, Breiner F (2019) biomod2: ensemble platform for species distribution modeling. R package version 3.3-7.
  76. Thüringer Landesanstalt für Umwelt und Geologie, TLUG (2009) Schmetterlinge: Glaucopsyche nausithous. In: Artensteckbriefe Thüringen, pp 1–4Google Scholar
  77. 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. CrossRefGoogle Scholar
  78. van Swaay C, Collins S, Dušej G et al (2012) Dos and don’ts for butterflies of the habitats directive of the European union. Nat Conserv 1:73–153. CrossRefGoogle Scholar
  79. Villemey A, van Halder I, Ouin A et al (2015) Mosaic of grasslands and woodlands is more effective than habitat connectivity to conserve butterflies in French farmland. Biol Conserv 191:206–215. CrossRefGoogle Scholar
  80. Vrabec V, Kulma M, Bubová T, Nowicki P (2017) Long-term monitoring of Phengaris (Lepidoptera: Lycaenidae) butterflies in the Přelouč surroundings (Czech Republic): is the waterway construction a serious threat? J Insect Conserv 21:393–400. CrossRefGoogle Scholar
  81. WallisDeVries MF (2004) A quantitative conservation approach for the endangered butterfly Maculinea alcon. Conserv Biol 18:489–499. CrossRefGoogle Scholar
  82. Weiss SB, Murphy DD, White RR (1988) Sun, slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha. Ecology 69:1486–1496. CrossRefGoogle Scholar
  83. Weiss N, Zucchi H, Hochkirch A (2013) The effects of grassland management and aspect on Orthoptera diversity and abundance: site conditions are as important as management. Biodivers Conserv 22:2167–2178. CrossRefGoogle Scholar
  84. Wikum DA, Shanholtzer GF (1978) Application of the Braun-Blanquet cover-abundance scale for vegetation analysis in land development studies. Environ Manag 2:323–329. CrossRefGoogle Scholar
  85. Winter C, Lehmann S, Diekmann M (2008) Determinants of reproductive success: a comparative study of five endangered river corridor plants in fragmented habitats. Biol Conserv 141:1095–1104. CrossRefGoogle Scholar
  86. Witek M, Sliwinska EB, Skórka P et al (2006) Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects. Oecologia 148:729–733. CrossRefPubMedGoogle Scholar
  87. Witek M, Śliwińska EB, Skórka P et al (2008) Host ant specificity of large blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands in East-central Europe. Eur J Entomol 105:871–877. CrossRefGoogle Scholar
  88. 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. CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Thünen Institute of BiodiversityBrunswickGermany
  2. 2.Biodiversity of Agricultural Landscapes, Institute of GeoecologyTechnische Universität BraunschweigBrunswickGermany
  3. 3.Landscape Ecology and Environmental Systems Analysis, Institute of GeoecologyTechnische Universität BraunschweigBrunswickGermany
  4. 4.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany

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