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Vegetation composition and structure are important predictors of oviposition site selection in an alpine butterfly, the Mountain Ringlet Erebia epiphron

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Abstract

Knowledge of species’ ecological requirements is key for designing effective conservation management. In butterflies, the needs of larval stages are often the most specialised part of the life-cycle, but for many species information on this is lacking. The Mountain Ringlet Erebia epiphron is a cold-adapted butterfly found in alpine grasslands in mountainous regions of Europe. Efforts to devise conservation strategies for this climate change-threatened species are hampered due to its basic ecology being poorly understood. Here, we describe a study on the autecology of Mountain Ringlets at sites across its British distribution, focusing on the habitat preferences of egg-laying females as a proxy for larval preferences. Female Mountain Ringlets placed their eggs predominantly on Nardus stricta and Festuca ovina, but also on several other host plant species, suggesting larvae may be more broadly polyphagous than previously realised. Sites chosen for eggs had higher abundance of larval host plants, intermediate leaf litter cover, and lower cover of grass tussocks than random locations, as well as a shorter and sparser grass sward. Although the main host plant is ubiquitous in upland areas of Britain, our findings suggest that this butterfly’s egg and larval stages have specialised ecological requirements, requiring specific microhabitat features characterised by a narrow range of vegetation composition and structural characteristics. Many habitat associations are liable to be explicable as adaptations to ensure placement of eggs and larvae in sites within optimal (warm or buffered) microclimates. We tentatively suggest that the distribution of Mountain Ringlets in the landscape is thermally-constrained.

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References

  • Asher J, Warren M, Fox R, Harding P, Jeffcoate G, Jeffcoate S (2001) The millennium atlas of butterflies in Britain and Ireland. Oxford University Press, Oxford

    Google Scholar 

  • Barton K (2018) MuMIn: multi-model inference. R package version 1.42.1

  • Bayfield N, McGowan GM, Taylor P, French DD, Mackie E, Waterhouse C, Hartley S (1995) Small Mountain Ringlet project: field studies rearing programme and questionaire survey 1994-95. Institute of Terrestrial Ecology

  • Boyd-Wallis W (1994) Survey of Creag Meagaidh NNR for colonies of Small Mountain Ringlet butterfly. Scottish Natural Heritage Report

  • Britton AJ, Beale CM, Towers W, Hewison RL (2009) Biodiversity gains and losses: evidence for homogenisation of Scottish alpine vegetation. Biol Conserv 142:1728–1739

    Google Scholar 

  • Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Machler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400

    Google Scholar 

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

    Google Scholar 

  • Čelik T, Vreš B (2018) Microtopography determines the habitat quality of a threatened peatland butterfly at its southern range margin. J Insect Conserv 22:707–720

    Google Scholar 

  • Curtis RJ, Brereton TM, Dennis RL, Carbone C, Isaac NJ (2015) Butterfly abundance is determined by food availability and is mediated by species traits. J Appl Ecol 52:1676–1684

    Google Scholar 

  • Davies ZG, Wilson RJ, Brereton TM, Thomas CD (2005) The re-expansion and improving status of the silver-spotted skipper butterfly (Hesperia comma) in Britain: a metapopulation success story. Biol Conserv 124:189–198

    Google Scholar 

  • Dennis P, Skartveit J, McCracken DI, Pakeman RJ, Beaton K, Kunaver A, Evans DM (2008) The effects of livestock grazing on foliar arthropods associated with bird diet in upland grasslands of Scotland. J Appl Ecol 45:279–287

    Google Scholar 

  • Dennis RL, Shreeve TG, Van Dyck H (2003) Towards a functional resource-based concept for habitat: a butterfly biology viewpoint. Oikos 102:417–426

    Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, Marquez JRG, Gruber B, Lafourcade B, Leitao PJ, Munkemuller T, McClean C, Osborne PE, Reineking B, Schroder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Google Scholar 

  • 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

    Google Scholar 

  • ESRI (2017) ArcGIS desktop. In: Release 10.5.1. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Evans DM, Villar N, Littlewood NA, Pakeman RJ, Evans SA, Dennis P, Skartveit J, Redpath SM (2015) The cascading impacts of livestock grazing in upland ecosystems: a 10-year experiment. Ecosphere 6:1–15

    CAS  Google Scholar 

  • Fartmann T, Hermann G (2006) Larvalökologie von Tagfaltern und Widderchen in Mitteleuropa–von den Anfängen bis heute. Abh Westf Mus Naturk 68:11–57

    Google Scholar 

  • Fox R, Brereton T, Asher J, August T, Botham M, Bourn N, Cruickshanks K, Bulman C, Ellis S, Harrower C (2015) The state of the UK’s Butterflies 2015. Butterfly Conservation & Centre for Ecology and Hydrology, Wareham, Dorset

    Google Scholar 

  • Franco AM, Hill JK, Kitschke C, Collingham YC, Roy DB, Fox R, Huntley B, Thomas CD (2006) Impacts of climate warming and habitat loss on extinctions at species' low-latitude range boundaries. Glob Change Biol 12:1545–1553

    Google Scholar 

  • Frohawk FW (1924) Natural history of British butterflies. London

    Google Scholar 

  • Galipaud M, Gillingham MA, Dechaume-Moncharmont FX (2017) A farewell to the sum of Akaike weights: the benefits of alternative metrics for variable importance estimations in model selection. Methods Ecol Evol 8:1668–1678

    Google Scholar 

  • García-Barros E, Fartmann T (2009) Butterfly oviposition: sites, behaviour and modes. In: Settele J, Shreeve TG, Konvička M, Van Dyck H (eds) Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 29–42

    Google Scholar 

  • Grant SA, Torvell L, Sim EM, Small J, Armstrong R (1996) Controlled grazing studies on Nardus grassland: effects of between-tussock sward height and species of grazer on Nardus utilization and floristic composition in two fields in Scotland. J Appl Ecol 33:1053–1064

    Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    CAS  Google Scholar 

  • Hartig F (2018) DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.2.0

  • Hill MO, Gauch HG (1980) Detrended correspondence analysis: an improved ordination technique. In: van der Maarel E (ed) Classification and ordination. Advances in vegetation science. Springer, Dordrecht, pp 47–58

    Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Johnson CJ, Nielsen SE, Merrill EH, McDonald TL, Boyce MS (2006) Resource selection functions based on use–availability data: theoretical motivation and evaluation methods. J Wildl Manag 70(2):347–357

    Google Scholar 

  • Konvička M, Beneš J, Kuras T (2002) Microdistribution and diurnal behaviour of two sympatric mountainous butterflies (Erebia epiphron and E. euryale): relations to vegetation and weather. Biol Bratisl 57:225–235

    Google Scholar 

  • Konvicka M, Benes J, Cízek O, Kuras T, Klecková I (2016) Has the currently warming climate affected populations of the mountain ringlet butterfly, Erebia epiphron (Lepidoptera: Nymphalidae), in low-elevation mountains? Eur J Entomol 113:295

    Google Scholar 

  • Kudrna O, Harpke A, Lux K, Pennerstorfer J, Schweiger O, Settele J, Wiemers M (2011) Distribution atlas of butterflies in Europe. Gesellschaft für Schmetterlingsschutz eV Halle

  • Kuras T, Beneš J, Konvička M, Honč L (2001) Life histories of Erebia sudetica sudetica and E. epiphron silesiana with description of immature stages (Lepidoptera Nymphalidae, Satyrinae). Atalanta 32:187–196

    Google Scholar 

  • Kuras T, Benes J, Fric Z, Konvicka M (2003) Dispersal patterns of endemic alpine butterflies with contrasting population structures: Erebia epiphron and E. sudetica. Popul Ecol 45:115–123

    Google Scholar 

  • Kuussaari M, van Nouhuys S, Hellmann JJ, Singer MC (2004) Larval biology of checkerspots. In: Ehrlich PR, Hanski I (eds) On the wings of checkerspots: a model system for population biology. Oxford University Press, Oxford

    Google Scholar 

  • Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291

    PubMed  Google Scholar 

  • Massey FP, Ennos AR, Hartley SE (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. J Anim Ecol 75:595–603

    PubMed  Google Scholar 

  • Masterman (2008) The distribution and habitat of Mountain Ringlet Erebia epiphron (Knoch) in Scotland. Atropos 41:10–18

    Google Scholar 

  • Mattila N, Kaitala V, Komonen A, Paivinen J, Kotiaho JS (2011) Ecological correlates of distribution change and range shift in butterflies. Insect Conserv Divers 4:239–246

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17-4. http://cran.r-project.org

  • Pakeman R, Hulme P, Torvell L, Fisher J (2003) Rehabilitation of degraded dry heather [Calluna vulgaris (L.) Hull] moorland by controlled sheep grazing. Biol Conserv 114:389–400

    Google Scholar 

  • Scalercio S, Bonacci T, Mazzei A, Pizzolotto R, Brandmayr P (2014) Better up, worse down: bidirectional consequences of three decades of climate change on a relict population of Erebia cassioides. J Insect Conserv 18:643–650

    Google Scholar 

  • Schmitt T, Louy D, Zimmermann E, Habel JC (2016) Species radiation in the Alps: multiple range shifts caused diversification in Ringlet butterflies in the European high mountains. Org Divers Evol 16:791–808

    Google Scholar 

  • Shannon S (1995) A study of the Small Mountain Ringlet butterfly Erebia epiphron Knoch. South West Cumbria. University of Leicester, Leicester

    Google Scholar 

  • Slamova I, Klecka J, Konvicka M (2013) Woodland and grassland mosaic from a butterfly perspective: habitat use by Erebia aethiops (L. epidoptera: S. atyridae). Insect Conserv Divers 6:243–254

    Google Scholar 

  • Stewart K, Bourn N, Thomas J (2001) An evaluation of three quick methods commonly used to assess sward height in ecology. J Appl Ecol 38:1148–1154

    Google Scholar 

  • 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

    Google Scholar 

  • Stuhldreher G, Fartmann T (2015) Oviposition-site preferences of a declining butterfly Erebia medusa (Lepidoptera: Satyrinae) in nutrient-poor grasslands. Eur J Entomol 112:493–499

    Google Scholar 

  • Ter Braak CJ (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179

    Google Scholar 

  • Thomas J, Thomas C, Simcox D, Clarke R (1986) Ecology and declining status of the silver-spotted skipper butterfly (Hesperia comma) in Britain. J Appl Ecol 23:365–380

    Google Scholar 

  • Thomas JA, Simcox D, Clarke RT (2009) Successful conservation of a threatened Maculinea butterfly. Science 325:80–83

    CAS  PubMed  Google Scholar 

  • Thomas CD, Hill JK, Anderson BJ, Bailey S, Beale CM, Bradbury RB, Bulman CR, Crick HQ, Eigenbrod F, Griffiths HM (2011a) A framework for assessing threats and benefits to species responding to climate change. Methods Ecol Evol 2:125–142

    Google Scholar 

  • Thomas J, Simcox D, Hovestadt T (2011b) Evidence based conservation of butterflies. J Insect Conserv 15:241–258

    Google Scholar 

  • Trivedi MR, Morecroft MD, Berry PM, Dawson TP (2008) Potential effects of climate change on plant communities in three montane nature reserves in Scotland, UK. Biol Conserv 141:1665–1675

    Google Scholar 

  • Van Noordwijk C, Flierman DE, Remke E, WallisDeVries MF, Berg MP (2012) Impact of grazing management on hibernating caterpillars of the butterfly Melitaea cinxia in calcareous grasslands. J Insect Conserv 16:909–920

    Google Scholar 

  • van Strien AJ, van Swaay CA, van Strien-van WT, Liempt MJ, Poot, WallisDeVries MF (2019) Over a century of data reveal more than 80% decline in butterflies in the Netherlands. Biol Conserv 234:116–122

    Google Scholar 

  • Van Swaay C, Maes D, Warren M (2009) Conservation status of European butterflies. In: Settele J, Shreeve TG, Konvička M, van Dyck H (eds) Ecology of butterflies in Europe. Cambridge University Press, Cambridge, pp 322–338

    Google Scholar 

  • WallisDeVries MF (2006) Larval habitat quality and its significance for the conservation of Melitaea cinxia in northwestern Europe. In: Fartmann T, Hermann G (eds) Larvalökologie von Tagfaltern und Widderchen in Mitteleuropa. Abhandlungen aus dem Westfälischen Museum für Naturkunde, Münster, Germany, pp 281–294

    Google Scholar 

  • Warren M (1991) The successful conservation of an endangered species, the heath fritillary butterfly Mellicta athalia, in Britain. Biol Conserv 55:37–56

    Google Scholar 

  • Warren M, Hill J, Thomas J, Asher J, Fox R, Huntley B, Roy D, Telfer M, Jeffcoate S, Harding P (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65–69

    CAS  PubMed  Google Scholar 

  • Weking S, Hermann G, Fartmann T (2013) Effects of mire type, land use and climate on a strongly declining wetland butterfly. J Insect Conserv 17:1081–1091

    Google Scholar 

  • Wheeler AS (1982) Erebia epiphron Knoch (Lep., Satyridae) reared on a two-year life cycle. Proc Br Entomol Nat Hist Soc 15:28

    Google Scholar 

  • Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host plants. Oecologia 63:23–29

    PubMed  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Google Scholar 

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Acknowledgements

We would like to thank James Gordon, Mark Yeldham, Ewan Munro, Mark Whiffin and Pete Howard for their assistance with data collection in the field. Thanks are also due to Martin Tordoff from the Butterfly Conservation Cumbria Branch, Dave Wainwright from Butterfly Conservation, John Hooson and Matthew Oates from the National Trust, and Helen Cole from the National Trust for Scotland for help designing this project, arranging access permissions and generally providing support and assistance. Funding for this work was provided by the Royal Society for the Protection of Birds. We also thank the generosity of 55 supporters who contributed donations to our ‘Giving Mountain Ringlets a brighter future’ crowdfunding campaign. Earlier drafts of this paper were substantially improved by comments from Graeme Buchanan, Jerry Wilson and two anonymous referees.

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Correspondence to S. R. Ewing.

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Ewing, S.R., Menéndez, R., Schofield, L. et al. Vegetation composition and structure are important predictors of oviposition site selection in an alpine butterfly, the Mountain Ringlet Erebia epiphron. J Insect Conserv 24, 445–457 (2020). https://doi.org/10.1007/s10841-020-00229-z

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