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Scale-dependent resource use in the Euphydryas aurinia complex

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Abstract

Butterflies of the European Euphydryas aurinia complex include a series of taxa, showing morphological and eco-ethological differences. All of them are threatened by changes in land use affecting both the structural and functional connectivity of habitat patches, as well as habitat quality. In this framework, we analysed the use of resources by two of the three taxa occurring in Italy, E. (a.) glaciegenita (Alpine) and E. (a.) provincialis (Mediterranean), at ‘landscape’, ‘patch’ and ‘microhabitat’ scale. We collected data on spatial distribution of adults by Mark-Release-Recapture to understand which parameters affect adult distributions at landscape scale and to test the degree of adult aggregation at patch scale. We sampled first instar larvae within fixed plots and compared the microhabitat characteristics of occupied vs. unoccupied host plants. We found that both populations were affected by management at landscape scale, with contrasting patterns depending on both sites and sex. The food plants were not a limiting factor for adult distribution, probably because they were abundant in the study areas. Within patches, males of E. (a.) glaciegenita showed aggregate distributions in comparison to those of E. (a.) provincialis, suggesting the existence of a “lek strategy”. At microhabitat scale, we observed that females carefully chose their egg-laying sites according to host plant density and microclimatic cues, even though selection was driven by distinct factors in the two populations. Understanding the ecological requirements of all life stages is essential to develop appropriate conservation strategies to preserve butterflies of the E. aurinia complex in Italy.

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References

  • Anthes N, Fartmann T, Hermann G, Kaule G (2003) Combining larval habitat quality and metapopulation structure—the key for successful management of pre-alpine Euphydryas aurinia colonies. J Insect Conserv 7:175–185

    Article  Google Scholar 

  • 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 

  • Bakker ES, Ritchie ME, Olff H, Milchunas DG, Knops JM (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9:780–788

    Article  PubMed  Google Scholar 

  • Balletto E, Cassulo L, Bonelli S (2014) An annotated checklist of the Italian butterflies and skippers (Papilionoidea, Hesperiioidea). Zootaxa 3853:1–14

    Article  PubMed  Google Scholar 

  • Barton K (2016) MuMIn: Multi-Model Inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Becker RA, Chambers JM, Wilks AR (1988) The new S language. Wadsworth & Brooks/Cole, Monterey

    Google Scholar 

  • Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188

    Article  Google Scholar 

  • Bonari G, Fajmon K, Malenovský I, Zelený D, Holuša J, Jongepierová I, Kočárek P, Konvička O, Uřičář J, Chytrý M (2017) Management of semi-natural grasslands benefiting both plant and insect diversity: the importance of heterogeneity and tradition. Agric Ecosyst Environ 246:243–252

    Article  Google Scholar 

  • Bonelli S, Cerrato C, Loglisci N, Balletto E (2011) Population extinctions in the Italian diurnal Lepidoptera: an analysis of possible causes. J Insect Conserv 15:879–890

    Article  Google Scholar 

  • Bonelli S, Casacci LP, Barbero F, Cerrato C, Dapporto L, Sbordoni V, Scalercio S, Zilli A, Battistoni A, Teofili C, Rondinini C (2018) The first red list of Italian butterflies. Insect Conserv Divers 11:506–521

    Article  Google Scholar 

  • Brunbjerg AK, Høye TT, Eskildsen A, Nygaard B, Damgaard CF, Ejrnæs R (2017) The collapse of marsh fritillary (Euphydryas aurinia) populations associated with declining host plant abundance. Biol Conserv 211:117–124

    Article  Google Scholar 

  • Buckley LB, Kingsolver JG (2012) The demographic impacts of shifts in climate means and extremes on alpine butterflies. Funct Ecol 26:969–977

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2004) Multimodel inference understanding AIC and BIC in model selection. Socio Meth Res 33:261–304

    Article  Google Scholar 

  • Casacci LP, Barbero F, Balletto E (2014) The “Evolutionarily Significant Unit” concept and its applicability in biological conservation. Ital J Zool 81:182–193

    Article  Google Scholar 

  • Casacci LP, Cerrato C, Barbero F, Bosso L, Ghidotti S, Paveto M, Pesce M, Plazio E, Panizza G, Balletto E, Viterbi R, Bonelli S (2015) Dispersal and connectivity effects at different altitudes in the Euphydryas aurinia complex. J Insect Conserv 19:265–277

    Article  Google Scholar 

  • Cates RG (1980) Feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores: the effect of resource abundance and plant chemistry. Oecologia 46:22–31

    Article  PubMed  Google Scholar 

  • Čelik T, Bräu M, Bonelli S, Cerrato C, Vres B, Balletto E, Stettmer C, Dolek M (2015) Winter-green host-plants, litter quantity and vegetation structure are key determinants of habitat quality for Coenonympha oedippus in Europe. J Insect Conserv 19:359–375

    Article  Google Scholar 

  • Cerrato C, Lai V, Balletto E, Bonelli S (2016) Direct and indirect effects of weather variability in a specialist butterfly. Ecol Entomol 41:263–275

    Article  Google Scholar 

  • Clark PJ, Evans FC (1954) Distance to nearest neighbour as a measure of spatial relationships in populations. Ecology 35:445–453

    Article  Google Scholar 

  • Cushman SA, McGarigal K (2004) Patterns in the species environment relationship depend on both scale and choice of response variables. Oikos 1:117–124

    Article  Google Scholar 

  • Dennis RHL (1993) Butterflies and climate change. Manchester University Press, Manchester

    Google Scholar 

  • Dennis RLH (2004) Landform resources for territorial nettle-feeding nymphalid butterflies: biases at different spatial scales. Anim Biodivers Conserv 27:37–45

    Google Scholar 

  • Dennis RLH (2010) A resource-based habitat view for conservation: butterflies in the British landscape. Wiley-Blackwell, Chichester

    Book  Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, Garcia Marquez JR, Gruber B, Lafoourcade B, Leitao PJ, Münkemüller T, Mcclean C, Osborne PE, Reineking B, Schroder B, Skidmore AK, Zurell D, Lautenbach S (2012) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 35:1–20

    Article  Google Scholar 

  • ESRI (2014) ArcGIS Desktop, Release 10.3. Redlands, CA. Environmental Systems Research Institute. http://www.esri.com

  • Griffith DM, Veech JA, Marsh CJ (2016) Cooccur: probabilistic species co-occurrence analysis in R. J Stat Softw 69:1–17

    Article  Google Scholar 

  • Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186

    Article  Google Scholar 

  • Hula V, Konvicka M, Pavlicko A, Fric Z (2004) Marsh Fritillary (Euphydryas aurinia) in the Czech Republic: monitoring, metapopulation structure, and conservation of an endangered butterfly. Entomol Fennica 15:231–241

    Google Scholar 

  • Janovsky Z, Janovskáa M, Weisera M, Horcicková E, Ríhová D, Münzbergová Z (2016) Surrounding vegetation mediates frequency of plant–herbivore interactions in leaf-feeders but not in other herbivore groups. Basic Appl Ecol 17:352–359

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  PubMed  Google Scholar 

  • Junker M, Zimmermann M, Ramos AA, Gros P, Konvička M, Nève G, Ràkosy L, Tammaru T, Castilho R, Schmitt T (2015) Three in one—multiple faunal elements within an endangered European butterfly species. PLoS ONE 10(11):e0142282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalarus K, Nowicki P (2017) Resource use by the dryad butterfly is scale-dependent. Popul Ecol 59:179–187

    Article  Google Scholar 

  • Knapton RW (1985) Lek structure and territoriality in the chryxus arctic butterfly, Oeneis chryxus (Satyridae). Behav Ecol Sociobiol 17:389–395

    Article  Google Scholar 

  • Konvicka M, Hula V, Fric Z (2003) Habitat of pre-hibernating larvae of the endangered butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae): What can be learned from vegetation composition and architecture? Eur J Entomol 100:313–322

    Article  Google Scholar 

  • Korb SK, Bolshakov LV, Fric ZF, Bartonova A (2016) Cluster biodiversity as a multidimensional structure evolution strategy: checkerspot butterflies of the group Euphydryas aurinia (Rottemburg, 1775) (Lepidoptera: Nymphalidae). Syst Entomol. https://doi.org/10.1111/syen.12167

    Article  Google Scholar 

  • Krämer B, Kämpf I, Enderle J, Poniatowski D, Fartmann T (2012) Microhabitat selection in a grassland butterfly: a trade-off between microclimate and food availability. J Insect Conserv 16:857–865

    Article  Google Scholar 

  • Lederhouse RC (1982) Territorial defense and lek behavior of the black swallowtail butterfly, Papilio polyxenes. Behav Ecol Sociobiol 10:109–118

    Article  Google Scholar 

  • Lewis OT, Hurford C (1997) Assessing the status of the marsh fritillary butterfly (Eurodryas aurinia): An example from Glamorgan, UK. J Insect Conserv 1:159–166

    Article  Google Scholar 

  • Loxdale HD, Lushai G (1999) Slaves of the environment: the movement of herbivorous insects in relation to their ecology and genotype. Phil Trans R Soc B 354:1479–1495

    Article  Google Scholar 

  • Luppi M, Dondina O, Orioli V, Bani L (2018) Local and landscape drivers of butterfly richness and abundance in a human-dominated area. Agric Ecosyst Environ 254:138–148

    Article  Google Scholar 

  • MacDonald D, Crabtree JR, Wiesinger G, Dax T, Stamou N, Fleury P, Guttierez Lazpita G, Gibon A (2000) Agricultural abandonment in mountain areas of Europe: environmental consequences and policy response. J Environ Manage 59:47–69

    Article  Google Scholar 

  • Marini L, Fontana P, Battisti A, Gaston KJ (2009a) Response of orthopteran diversity to abandonment of semi-naturals meadows. Agric Ecosyst Environ 132:232–236

    Article  Google Scholar 

  • Marini L, Fontana P, Klimek S, Battisti A, Gaston KJ (2009b) Impact of farm size and topography on plant and insect diversity of managed pastures in the Alps. Biol Conserv 142:394–403

    Article  Google Scholar 

  • Marshall EJP, Moonen AC (2002) Field margins in northern Europe: their functions and interactions with agriculture. Agric Ecosyst Environ 89:5–21

    Article  Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • Molina G, Poggio S, Ghersa C (2014) Epigeal arthropod communities in intensively farmed landscapes: effects of land use mosaics, neighbourhood heterogeneity, and field position. Agric Ecosyst Environ 192:135–143

    Article  Google Scholar 

  • Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Mottet A, Ladet S, Coque N, Gibon A (2006) Agricultural land-use change and its drivers in mountain landscapes: a case study in the Pyrenees. Agric Ecosyst Environ 114:296–310

    Article  Google Scholar 

  • Munguira ML, Martin C, García-Barros E, Viejo LJ (1997) Use of space and resources in a Mediterranean population of the butterfly Euphydryas aurinia. Acta Oecol 18:597–612

    Article  Google Scholar 

  • New TR (1997) Are Lepidoptera an effective ‘umbrella group’ for biodiversity conservation? J Insect Conserv 1:5–12

    Article  Google Scholar 

  • Nguyen HDD, Nansen C (2018) Edge-biased distributions of insects. A review. Agron Sustain Dev 38:11

    Article  Google Scholar 

  • Pinzari M, Pinzari M, Sbordoni V (2016) Egg laying behaviour, host plants and larval survival of Euphydryas aurinia provincialis (Lepidoptera Nymphalidae) in a Mediterranean population (central Italy). Boll Soc Entomol Ital 148:121–140

    Article  Google Scholar 

  • Porter K (1982) Basking behaviour in larvae of the butterfly Euphydryas aurinia. Oikos 38:08–312

    Article  Google Scholar 

  • Porter K (1984) Sunshine, sex-ratio and behaviour of the Euphydryas aurinia larvae. In: Vane-Wright HT, Ackery PR (eds) The biology of butterflies: symposium of the Royal Entomological Society of London. Academic press, London, pp 309–315

    Google Scholar 

  • Quantum GIS Development Team—Version 2.14.2 (2016). Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Schenk W, Bätzing W (2003) Die Alpen. Geschichte und Zukunft einer europäischen Kulturlandschaft. Beck, München

    Google Scholar 

  • Settele J, Shreeve T, Konvička M, Dyck HV (2009) Ecology of butterflies in Europe. Cambridge University Press, Cambridge

    Google Scholar 

  • Skórka P, Settele J, Woyciechowski M (2007) Effects of management cessation on grassland butterflies in southern Poland. Agric Ecosyst Environ 121:319–324

    Article  Google Scholar 

  • Stefanescu C, Peñuelas J, Filella I (2009) Rapid changes in butterfly communities following the abandonment of grasslands: a case study. Insect Conserv Divers 2:261–269

    Article  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

    Article  Google Scholar 

  • Tarquini S, Vinci S, Favalli M, Doumaz F, Fornaciai A, Nannipieri L (2012) Release of a 10-m-resolution DEM for the Italian territory: comparison with global-coverage DEMs and anaglyph-mode exploration via the web. Comput Geosci 38:168–170

    Article  Google Scholar 

  • Thomas JA (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philos Trans R Soc B 360:339–357

    Article  CAS  Google Scholar 

  • Thornton DH, Branch LC, Sunquist ME (2011) The influence of landscape, patch, and within-patch factors on species presence and abundance: a review of focal patch studies. Landsc Ecol 26:7–18

    Article  Google Scholar 

  • Tjørnløv RS, Kissling WD, Barnagaud JY, Bøcher PK, Høye TT (2015) Oviposition site selection of an endangered butterfly at local spatial scales. J Insect Conserv 19:377–391

    Article  Google Scholar 

  • Tocco C, Negro M, Rolando A, Palestrini C (2013) Does natural reforestation represent a potential threat to dung beetle diversity in the Alps? J Insect Conserv 17:207–217

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • van Swaay C, Wynhoff I, Verovnik R, Wiemers M, López Munguira M, Maes D, Sasic M, Verstrael T, Warren M, Settele J (2010) Euphydryas aurinia. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. http://www.iucnredlist.org

  • van Swaay CAM, Collins S, Dusej G, Maes D, Munguira ML, Rakosy L, Ryrholm N, Šašid M, Settele J, Thomas J, Verovnik R, Verstrael T, Warren MS, Wiemers M, Wynhoff I (2012) Do’s and don’ ts for butterflies of the habitats directive of the European Union. Nat Conserv 1:73–153

    Article  Google Scholar 

  • Veech JA (2013) A probabilistic model for analysing species co-occurrence: probabilistic model. Global Ecol Biogeogr 22:252–260

    Article  Google Scholar 

  • Venables W, Ripley B (2002) Modern applied statistics using S-PLUS. Springer, New York

    Google Scholar 

  • Wahlberg N, Klemetti T, Hanski I (2002) Dynamic populations in a dynamic landscape: the metapopulation structure of the marsh fritillary butterfly. Ecography 25:224–232

    Article  Google Scholar 

  • Wallis De Vries MF, van Swaay CAM (2006) Global warming and excess nitrogen may induce butterfly decline by microclimate cooling. Glob Change Biol 12:1620–1626

    Article  Google Scholar 

  • Weiss SB, Murphy DD, White RR (1988) Sun, slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha. Ecology 69:1486–1496

    Article  Google Scholar 

  • West SA, Cunningham JP (2002) A general model for host plant selection in phytophagous insects. J Theor Biol 214:499–513

    Article  PubMed  Google Scholar 

  • Williams M (2003) Deforesting the earth: from the prehistory to global crisis. The University of Chicago Press, Chicago

    Google Scholar 

  • Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annu Rev Entomol 47:361–393

    Article  CAS  PubMed  Google Scholar 

  • Zangerl AR, Berenbaum MR (1993) Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47–54

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank the authorities of Gran Paradiso National Park and Protected Areas of the Piedmont Apennines for financial and logistic support and for having strongly encouraged this work. The work was carried out with the authorization (prot. 0039115/PNM, 20/06/2013) by the Italian Ministry of the Environment MATTM and within the project “A multi-taxa approach to study the impact of climate change on the biodiversity of Italian ecosystems” of the Italian Ministry of Education, University and Research (MIUR). Authors are also very grateful to Eleonora Rossi, Giulia Marangoni and Alessandro Girodo for their fundamental help in the fieldwork.

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Correspondence to Luca Pietro Casacci.

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Ghidotti, S., Cerrato, C., Casacci, L.P. et al. Scale-dependent resource use in the Euphydryas aurinia complex. J Insect Conserv 22, 593–605 (2018). https://doi.org/10.1007/s10841-018-0088-2

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