Abstract
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.
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References
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 57–59
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. https://doi.org/10.1007/s10841-007-9091-8
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. https://doi.org/10.1127/entom.gen/33/2011/39
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. https://doi.org/10.1007/s10980-007-9181-8
Barua M, Gurdak DJ, Ahmed RA, Tamuly J (2012) Selecting flagships for invertebrate conservation. Biodivers Conserv 21:1457–1476. https://doi.org/10.1007/s10531-012-0257-7
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. https://doi.org/10.1007/s10841-008-9158-1
Beers TW, Dress PE, Wensel LC (1966) Aspect transformation in site productivity research. J For 64:691–692. https://doi.org/10.1093/jof/64.10.691
Bengtsson J, Bullock JM, Egoh B et al (2019) Grasslands—more important for ecosystem services than you might think. Ecosphere 10:1–20. https://doi.org/10.1002/ecs2.2582
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. https://doi.org/10.1016/j.ecolmodel.2008.04.010
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. https://doi.org/10.1111/ddi.12795
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. https://doi.org/10.1016/j.biocon.2005.05.009
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. https://doi.org/10.1007/s11284-007-0376-x
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. https://doi.org/10.1111/2041-210X.12403
Broennimann O, Di Cola V, Guisan A (2018) ecospat: spatial ecology miscellaneous methods. R package version 3.0. https://cran.r-project.org/package=ecospat
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. https://doi.org/10.1111/1365-2664.12523
Dauber J, Wolters V (2004) Edge effects on ant community structure and species richness in an agricultural landscape. Biodivers Conserv 13:901–915. https://doi.org/10.1023/B:BIOC.0000014460.65462.2b
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. https://doi.org/10.3897/natureconservation.19.12457
Deutscher Wetterdienst (2017) Deutsche Klimaatlas, Klima und Welt, Thuringia. https://www.dwd.de/DE/klimaumwelt/klimaatlas/klimaatlas_node.html. Accessed 26 Apr 2019
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. https://doi.org/10.1007/s10531-009-9670-y
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. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dover J, Settele J (2009) The influences of landscape structure on butterfly distribution and movement: a review. J Insect Conserv 13:3–27. https://doi.org/10.1007/s10841-008-9135-8
Gillman R (2002) Geometry and gerrymandering. Math Horizons 10:10–12. https://doi.org/10.1080/10724117.2002.11974602
Habel JC, Dengler J, Janišová M et al (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodivers Conserv 22:2131–2138. https://doi.org/10.1007/s10531-013-0537-x
Halada L, Evans D, Romão C, Petersen JE (2011) Which habitats of European importance depend on agricultural practices? Biodivers Conserv 20:2365–2378. https://doi.org/10.1007/s10531-011-9989-z
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. https://doi.org/10.1111/j.1365-2656.2011.01848.x
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. https://doi.org/10.1007/s10841-012-9479-y
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. https://doi.org/10.1111/j.1365-2664.2006.01125.x
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. https://doi.org/10.1007/s10841-013-9591-7
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. https://doi.org/10.1371/journal.pone.0168679
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. https://doi.org/10.1007/s10841-016-9937-z
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. https://doi.org/10.1111/j.1752-4598.2011.00138.x
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. https://doi.org/10.1016/j.biocon.2012.03.038
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. https://doi.org/10.1046/j.1365-2699.2003.00878.x
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. https://doi.org/10.1111/j.1461-0248.2010.01457.x
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. https://doi.org/10.1007/s10841-014-9724-7
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 225–227
McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724. https://doi.org/10.1890/07-1861.1
McRae B, Shah V, Mohapatra T (2013) Circuitscape user guide. Nat Conserv 28
Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145. https://doi.org/10.1890/0012-9658(2002)083%5b1131:scmise%5d2.0.co;2
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. https://doi.org/10.1007/s00442-010-1623-3
Munguira ML, Martín J (1999) Action plan for Maculinea butterflies in Europe. Nat Environ 97:1–72
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 228
Nowicki P (2017) Survey precision moderates the relationship between population size and stability. Biol Conserv 212:310–315. https://doi.org/10.1016/j.biocon.2017.06.041
Nowicki P, Vrabec V (2011) Evidence for positive density-dependent emigration in butterfly metapopulations. Oecologia 167:657–665. https://doi.org/10.1007/s00442-011-2025-x
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. https://doi.org/10.1007/s10144-005-0222-3
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. https://doi.org/10.1016/j.biocon.2007.08.001
Nowicki P, Halecki W, Kalarus K (2013) All natural habitat edges matter equally for endangered Maculinea butterflies. J Insect Conserv 17:139–146
Nowicki P, Vrabec V, Binzenhöfer B et al (2014) Butterfly dispersal in inhospitable matrix: rare, risky, but long-distance. Landsc Ecol 29:401–412. https://doi.org/10.1007/s10980-013-9971-0
Nowicki P, Marczyk J, Kajzer-Bonk J (2015) Metapopulations of endangered Maculinea butterflies are resilient to large-scale fire. Ecohydrology 8:398–405. https://doi.org/10.1002/eco.1484
Öckinger E, Smith HG (2006) Landscape composition and habitat area affects butterfly species richness in semi-natural grasslands. Oecologia 149:526–534. https://doi.org/10.1007/s00442-006-0464-6
Öckinger E, Lindborg R, Sjödin NE, Bommarco R (2012) Landscape matrix modifies richness of plants and insects in grassland fragments. Ecography 35:259–267. https://doi.org/10.1111/j.1600-0587.2011.06870.x
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. https://doi.org/10.1016/j.biocon.2006.12.020
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. https://doi.org/10.25849/myrmecol.news_027:013
Plieninger T, Höchtl F, Spek T (2006) Traditional land-use and nature conservation in European rural landscapes. Environ Sci Policy 9:317–321. https://doi.org/10.1016/j.envsci.2006.03.001
Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman & Hall, London
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. https://doi.org/10.1016/j.biocon.2018.07.018
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. https://doi.org/10.2980/18-2-3396
Schröder B, Richter O (2000) Are habitat models transferable in space and time? Zeitschrift für Ökologie und Naturschutz 8:195–205
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 62–78
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. http://ec.europa.eu/science-environmentpolicy
Seifert B (2017) The ecology of Central European non-arboreal ants—37 years of a broad-spectrum analysis under permanent taxonomic control. Soil Org 89:1–67
Seifert B (2018) The ants of Central and North Europe. lutra Verlags- und Vertriebsgesellschaft, Tauer, 408 pp
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 261–276
Settele J, Kühn E (2009) Insect conservation. Science 80(325):41–42. https://doi.org/10.1126/science.1176892
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. https://doi.org/10.1007/s00040-005-0841-x
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. https://doi.org/10.1007/s10980-013-9855-3
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. https://doi.org/10.1046/j.1365-2664.2002.00715.x
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. https://doi.org/10.1016/j.ecolind.2008.12.006
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. https://doi.org/10.1098/rstb.2018.0202
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. https://doi.org/10.1016/0006-3207(84)90040-5
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. https://doi.org/10.1098/rspb.2000.1398
Thomas CD, Hanski I (1997) Butterfly metapopulations. In: Hanski I, Gilpin ME (eds) Metapopulation biology. Elsevier, Amsterdam, pp 359–386
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. https://doi.org/10.1023/A:1009640706218
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. https://doi.org/10.1098/rspb.2001.1693
Thuiller W, Georges D, Engler R, Breiner F (2019) biomod2: ensemble platform for species distribution modeling. R package version 3.3-7. https://cran.r-project.org/package=biomod2
Thüringer Landesanstalt für Umwelt und Geologie, TLUG (2009) Schmetterlinge: Glaucopsyche nausithous. In: Artensteckbriefe Thüringen, pp 1–4
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. https://doi.org/10.1111/j.1469-1795.2009.00281.x
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. https://doi.org/10.3897/natureconservation.1.2786
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. https://doi.org/10.1016/j.biocon.2015.06.030
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. https://doi.org/10.1007/s10841-017-9982-2
WallisDeVries MF (2004) A quantitative conservation approach for the endangered butterfly Maculinea alcon. Conserv Biol 18:489–499. https://doi.org/10.1111/j.1523-1739.2004.00336.x
Weiss SB, Murphy DD, White RR (1988) Sun, slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha. Ecology 69:1486–1496. https://doi.org/10.2307/1941646
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. https://doi.org/10.1007/s10531-012-0398-8
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. https://doi.org/10.1007/BF01866672
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. https://doi.org/10.1016/j.biocon.2008.02.002
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. https://doi.org/10.1007/s00442-006-0404-5
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. https://doi.org/10.14411/eje.2008.115
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. https://doi.org/10.1007/s10841-010-9337-8
Acknowledgements
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.
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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.
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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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Pérez-Sánchez, A.J., Schibalski, A., Schröder, B. et al. 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. J Insect Conserv 24, 327–341 (2020). https://doi.org/10.1007/s10841-019-00204-3
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DOI: https://doi.org/10.1007/s10841-019-00204-3