Skip to main content

Advertisement

Log in

Distribution and conservation of the relict interaction between the butterfly Agriades zullichi and its larval foodplant (Androsace vitaliana nevadensis)

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Although Mediterranean mountains are considered biodiversity hot-spots, the presence of relict biotic interactions as a testimony of a past colder climate is an aspect frequently missed. Herein we investigate the distribution and conservation problems of a relict interaction in the Sierra Nevada mountains (southern Europe) between the butterfly Agriades zullichi—a rare and threatened butterfly—and its larval foodplant Androsace vitaliana subsp. nevadensis. We designed an intensive field survey to obtain a comprehensive presence dataset. This was used to calibrate species distribution models with absences taken at local and regional extents, analyze the potential distribution, evaluate the influence of environmental factors in different geographical contexts, and evaluate conservation threats for both organisms. We found 39 presence localities inhabited by the larval foodplant and the butterfly comprising 60.93 ha, with 82 % of the area concentrated in ten larger localities. The local and regional distribution models explained 68.7 and 85.0 % deviance, indicating a suitable area of 1,884.8 and 9,621.22 ha respectively. Topography and soil properties were the most important variables in the local model and temperature in the regional model. We observed several threats such as restricted extent of occurrence, lack of larval foodplant regeneration, the negative effect of the ski resort and a potential high sensitivity to climate change. Finally, we recommend some management measures in order to improve the conservation of key populations of both species, reinforcing A. vitaliana nevadensis populations and researching the importance of phenology in the persistence of this interaction under climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alvarez NC, Thiel-Egenter A, Tribsch R, Holderegger S, Manel P, Schonswetter P, Taberlet S, Brodbeck M, Gaudeul L, Gielly L, Küpfer P, Mansion G, Negrini R, Paun O, Pellecchia M, Rioux D, Schüpfer F, Van Loo M, Winkler M, Gugerli F, IntraBioDiv Consortium (2009) History or ecology? Substrate type as a major driver of patial genetic structure in Alpine plants. Ecol Lett 12:632–640. doi:10.1111/j.1461-0248.2009.01312.x

    Article  PubMed  Google Scholar 

  • Anderson RS, Jiménez-Moreno G, Carrión JS, Pérez-Martínez C (2011) Holocene vegetation history from Laguna de Río Seco, Sierra Nevada, southern Spain. Quat Sci Rev 30:1615–1629. doi:10.1016/j.quascirev.2011.03.005

    Article  Google Scholar 

  • Benito B, Lorite J, Peñas J (2011) Simulating potential effects of climatic warming on altitudinal patterns of key species in Mediterranean-alpine ecosystems. Clim Change 108(3):471–483. doi:10.1007/s10584-010-0015-3

    Article  Google Scholar 

  • Benito BM, Cayuela L, Albuquerque FS (2013) The impact of modelling choices in the predictive performance of richness maps derived from species-distribution models: guidelines to build better diversity models. Methods Ecol Evolut 4:327–335. doi:10.1111/2041-210x.12022

    Article  Google Scholar 

  • Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529. doi:10.1111/j.1469-185X.1968.tb00968.x

    Article  Google Scholar 

  • Blanca G, López MR, Lorite J, Martínez MJ, Molero J, Quintas S, Ruiz M, Varo MA, Vidal S (2002) Flora amenazada de Sierra Nevada. University of Granada, Granada

    Google Scholar 

  • Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford

    Google Scholar 

  • Boucher FC, Thuiller W, Roquet C, Douzet R, Aubert S, Alvarez N, Lavergne S (2012) Reconstructing the origins of high-alpine niches and cushion life form in the genus Androsace s.l. (Primulaceae). Evolution 66(4):1255–1268. doi:10.1111/j.1558-5646.2011.01483.x

    Article  PubMed  Google Scholar 

  • Breiman L (2001) Random forest. Mach Learn 45:15–32. doi:10.1023/A:1010933404324

    Google Scholar 

  • Bykova O, Chuine I, Morin X, Higgins SI (2012) Temperature dependence of the reproduction niche and its relevance for plant species distributions. J Biogeogr 39(12):2191–2200. doi:10.1111/j.1365-2699.2012.02764.x

    Article  Google Scholar 

  • Cabezudo B, Talavera S, Blanca G, Cueto M, Valdés B, Hernández JE, Rodríguez-Hiraldo C, Navas D, Vega C (2005) Lista Roja de la Flora Vascular de Andalucía. Consejería Medio Ambiente (Junta de Andalucía), Sevilla

    Google Scholar 

  • Cutler DR, Edwards TC Jr, Beard KH, Cutler A, Hess KT, Gibson J, Lawler JJ (2007) Random forests for classification in ecology. Ecology 88(11):2783–2792. doi:10.1890/07-0539.1

    Article  PubMed  Google Scholar 

  • Demattê JAM, Garcia GJ (1999) Alteration of soil properties through a weathering sequence as evaluated by spectral reflectance. Soil Sci Soc Am J 63:327–342. doi:10.2136/sssaj1999.03615995006300020010x

    Article  Google Scholar 

  • Demattê JAM, Nanni MR (2003) Weathering sequence of soils developed from basalt as evaluated by laboratory (IRIS), airborne (AVIRIS) and orbital (TM) sensors. Int J Remote Sens 24(23):4715–4738. doi:10.1080/0143116031000075116

    Article  Google Scholar 

  • Dixon CJ, Schönswetter P, Vargas P, Ertl S, Schneeweiss GM (2009) Bayesian hypothesis testing supports long-distance Pleistocene migrations in a European high mountain plant (Androsace vitaliana, Primulaceae). Mol Phylogenet Evol 53(2):580–591. doi:10.1016/j.ympev.2009.07.016

    Article  CAS  PubMed  Google Scholar 

  • Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29(2):129–151. doi:10.1111/j.2006.0906-7590.04596.x

    Article  Google Scholar 

  • Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence. Environ Conserv 24(1):38–49

    Article  Google Scholar 

  • Foose TJ, de Boer L, Seal US, Lande R (1995) Conservation managements strategies based on viable populations. In: Ballou JD, Gilpin ME, Foose TJ (eds) Population management for survival and recovery: Analytical methods and strategies in small population conservation. Columbia University Press, NewYork, pp 273–294

    Google Scholar 

  • Frazier BE, Cheng Y (1989) Remote sensing of soils in the eastern Palouse region with landsat thematic mapper. Remote Sens Environ 28:317–325

    Article  Google Scholar 

  • Gottfried M, Pauli H, Futschik A, Akhalkatsi M, Barancok P, Alonso JLB, Coldea G, Dick J, Erschbamer B, Fernández Calzado MR, Kazakis G, Krajci J, Larsson P, Mallaun M, Michelsen O, Moiseev D, Moiseev P, Molau U, Merzouki A, Nagy L, Nakhutsrishvili G, Pedersen B, Pelino G, Puscas M, Rossi G, Stanisci A, Theurillat JP, Tomaselli M, Villar L, Vittoz P, Vogiatzakis I, Grabherr G (2012) Continent-wide response of mountain vegetation to climate change. Nat Clim Change 2:111–115. doi:10.1038/NCLIMATE1329

    Article  Google Scholar 

  • Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135(2–3):147–186. doi:10.1016/S0304-3800(00)00354-9

    Article  Google Scholar 

  • Guisan A, Weiss SB, Weiss AD (1999) GLM versus CCA spatial modeling of plant species distribution. Plant Ecol 143:107–122. doi:10.1023/A:1009841519580

    Article  Google Scholar 

  • Guisan A, Broennimann O, Engler R, Vust M, Yoccoz NG, Lehmann A, Zimmermann NE (2006) Using niche-based models to improve the sampling of rare species. Conserv Biol 20(2):501–511. doi:10.1111/j.1523-1739.2006.00354.x

    Article  PubMed  Google Scholar 

  • Habel JC, Ivinskis P, Schmitt T (2010) On the limit of altitudinal range shifts - Population genetics of relict butterfly populations. Acta Zoologica Academiae Scientiarum Hungaricae 56(4):383–393

    Google Scholar 

  • Hastie T (2011) Gam: generalized additive models. R package version 1.06.2. http://CRAN.R-project.org/package=gam

  • Haubrich K, Schmitt T (2007) Cryptic differentiation in alpine-endemic, high-altitude butterflies reveals down-slope glacial refugia. Mol Ecol 16(17):3643–3658. doi:10.1111/j.1365-294X.2007.03424.x

    Article  CAS  PubMed  Google Scholar 

  • Heiberger RM (2012) HH: statistical analysis and data display: Heiberger and Holland. R package version 2.3-23. http://CRAN.R-project.org/package=HH

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Google Scholar 

  • Hewson RD, Cudahy TJ, Huntington JF (2001) Geologic and atleration mapping at Mt fitton, South Australia, using ASTER satellite-borne data. Int Geosci Remote Sens Symp (IGARSS) 2:724–726. doi:10.1109/IGARS.2001.976615

    Google Scholar 

  • Hijmans RJ, Phillips S, Leathwick J, Elith J (2012) dismo, species distribution modeling. R package version 0.6-10

  • Hovestadt T, Kubisch A, Poethke HJ (2010) Information processing in models for density-dependent emigration: a comparison. Ecol Model 221:405–410. doi:10.1016/j.ecolmodel.2009.11.005

    Article  Google Scholar 

  • Illán JG, Gutiérrez D, Díez SB, Wilson RJ (2012) Elevational trends in butterfly phenology: implications for species responses to climate change. Ecol Entom 37(2):134–144. doi:10.1111/j.1365-2311.2012.01345.x

    Article  Google Scholar 

  • James M, Gilbert F, Zalat S (2003) Thyme and isolation for the sinai baton blue butterfly (Pseudophilotes sinaicus). Oecologia 134:445–453. doi:10.1007/s00442-002-1123-1

    Article  PubMed  Google Scholar 

  • Jetz W, Rahbek C, Lichstein JW (2005) Local and global approaches to spatial data analysis in ecology. Glob Ecol Biogeogr 14(1):97–98

    Article  Google Scholar 

  • Ji J, Zhao L, Balsam W, Chen J, Wu T, Liu L (2006) Detecting chlorite in the Chinese loess sequence by diffuse reflectance spectroscopy. Clays Clay Miner 54(2):266–273. doi:10.1346/CCMN.2006.0540211

    Article  CAS  Google Scholar 

  • Karatzoglou A, Smola A, Hornik K, Zeileis A (2004) kernlab-An S4 package for Kernel methods in R. J Stat Softw 11(9):1–20

    Google Scholar 

  • Kress A (1997) Androsace. In: Castroviejo S, Aedo C, Laínz M, Morales R, Muñoz-Garmendia F, Nieto-Feliner G, Paiva J (eds) Flora Iberica, 5th edn. Real Jardín Botánico, CSIC, Madrid, pp 22–40

    Google Scholar 

  • Larcher WC, Kainmuller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205:3–18. doi:10.1016/j.flora.2008.12.005

    Article  Google Scholar 

  • Lesica P, Allendorf FW (1995) When peripheral populations are valuable for conservation. Conserv Biol 9:753–760

    Article  Google Scholar 

  • Liaw A, Wiener M (2002) Classification and regression by random Forest. R News 2(3):18–22

    Google Scholar 

  • Liu C, Berry PM, Dawson TP, Pearson RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28(3):385–393. doi:10.1111/j.0906-7590.2005.03957.x

    Article  Google Scholar 

  • Marmion M, Parviainen M, Luoto M, Heikkinen RK, Thuiller W (2009) Evaluation of consensus methods in predictive species distribution modelling. Divers Distrib 15:59–69. doi:10.1111/j.1472-4642.2008.00491.x

    Article  Google Scholar 

  • Martín-García JM, Delgado G, Párraga JF, Bech J, Delgado R (1998) Mineral formation in micaceous Mediterranean red soils of Sierra Nevada, Granada, Spain. Eur J Soil Sci 49:253–268. doi:10.1046/j.1365-2389.1998.00155.x

    Article  Google Scholar 

  • Médail F, Quézel P (1999) Biodiversity hotspots in the Mediterranean Basin: setting global conservation priorities. Conserv Biol 13(6):1510–1513. doi:10.1046/j.1523-1739.1999.98467.x

    Article  Google Scholar 

  • Merrill RM, Gutiérrez D, Lewis OT, Gutiérrez J, Díez SB, Wilson RJ (2008) Combined effects of climate and biotic interactions on the elevational range of a phytophagous insect. J Anim Ecol 77:145–155. doi:10.1111/j.1365-2656.2007.01303.x

    Article  PubMed  Google Scholar 

  • Milborrow S (2012). Earth, multivariate adaptive regression spline models. R package version 3.2-2

  • Munguira ML (1989) Biología y biogeografía de los licénidos ibéricos en peligro de extinción (Lepidoptera: Lycaenidae). Ediciones Universidad Autónoma de Madrid, Madrid

    Google Scholar 

  • Munguira ML, Martín J, Garcia-Barros E, López J (2008) Agriades zullichi Hemming, 1933. In: Verdú JR, Galante E (eds) Atlas de los Invertebrados Amenazados de España (Especies En Peligro Crítico y En Peligro). Dirección General para la Biodiversidad, Ministerio de Medio Ambiente, Madrid, pp 176–179

    Google Scholar 

  • Nieto-Feliner G (2011) Southern European glacial refugia: a tale of tales. Taxon 60(2):365–372

    Google Scholar 

  • Ninyerola M, Pons X, Roure JM (2000) A methodological approach of climatological modelling of air temperature and precipitation through GIS techniques. Int J Climatol 20(14):1823–1841. doi:10.1002/1097-0088(20001130)20:14<1823:AID-JOC566>3.0.CO;2-B

    Article  Google Scholar 

  • Ohsaki N (1986) Body temperatures and behavioural thermoregulation strategies of three Pieris butterflies in relation to solar radiation. J Ethol 4(1):1–9. doi:10.1007/BF02348247

    Article  Google Scholar 

  • Pauli H, Gottfried M, Dullinger S, Abdaladze O, Akhalkatsi M, Alonso JLB, Coldea G, Dick J, Erschbamer B, Fernández Calzado R, Ghosn D, Holten JI, Kanka R, Kazakis G, Kollár J, Larsson P, Moiseev P, Moiseev D, Molau U, Molero Mesa J, Nagy L, Pelino G, Puşcaş M, Rossi G, Stanisci A, Syverhuset AO, Theurillat JP, Tomaselli M, Unterluggauer P, Villar L, Vittoz P, Grabherr G (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336(6079):353–355. doi:10.1126/science.1219033

    Article  CAS  PubMed  Google Scholar 

  • Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 12:361–371. doi:10.1046/j.1466-822X.2003.00042.x

    Article  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259

    Article  Google Scholar 

  • R Development Core Team (2012). R, A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. www.R-project.org/

  • Roura-Pascual N, Suarez AV, McNyset K, Gómez C, Pons P, Touyama Y, Wild AL, Gascon F, Peterson AT (2006) Niche differentiation and fine-scale projections for Argentine ants based on remotely sensed data. Ecol Appl 16:1832–1841. doi:10.1890/1051-0761(2006)016[1832:NDAFPF]2.0.CO;2

    Google Scholar 

  • Roy DB, Sparks TH (2000) Phenology of British butterflies and climate change. Glob Change Biol 6:407–416. doi:10.1046/j.1365-2486.2000.00322.x

    Article  Google Scholar 

  • Sánchez-Marañón M, Gámiz E, Delgado G, Delgado R (1999) Mafic-ultramafic soils affected by silicic colluvium in the Sierra Nevada Mountains (southern Spain). Can J Soil Sci 79:431–442. doi:10.4141/S98-063

    Article  Google Scholar 

  • Schmitt T, Haubrich K (2008) The genetic structure of the mountain forest butterfly Erebia euryale unravels the late Pleistocene and postglacial history of the mountain coniferous forest biome in Europe. Mol Ecol 17(9):2194–2207. doi:10.1111/j.1365-294X.2007.03687.x

    Article  PubMed  Google Scholar 

  • Schweiger O, Heikkinen RK, Harpke A, Hickler T, Klotz S, Kudrna O, Kühn I, Pöyry J, Settele J (2012) Increasing range mismatching of interacting species under global change is related to their ecological characteristics. Glob Ecol Biogeogr 21:88–99. doi:10.1111/j.1466-8238.2010.00607.x

    Article  Google Scholar 

  • Settele J, Kühn E (2009) Insect conservation. Science 325(5936):41–42. doi:10.1126/science.1176892

    Article  CAS  PubMed  Google Scholar 

  • Shao GF, Wu JG (2008) On the accuracy of landscape pattern analysis using remote sensing data. Landsc Ecol 23:505–511. doi:10.1007/s10980-008-9215-x

    Article  Google Scholar 

  • Shirley SM, Yang Z, Hutchinson RA, Alexander JD, McGarigal K, Betts MG (2013) Species distribution modelling for the people: unclassified landsat TM imagery predicts bird occurrence at fine resolutions. Divers Distrib 19:855–866. doi:10.1111/ddi.12093

    Article  Google Scholar 

  • Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Phil Trans R Soc B 365(1555):3161–3176. doi:10.1098/rstb 2010.0144

    Article  PubMed Central  PubMed  Google Scholar 

  • Stefanescu C, Carnicer J, Peñuelas J (2011) Determinants of species richness in generalist and specialist Mediterranean butterflies: the negative synergistic forces of climate and habitat change. Ecography 34:353–363. doi:10.1111/j.1600-0587.2010.06264.x

    Article  Google Scholar 

  • Stoner ER, Baumgardner MF (1981) Characteristic variations in reflectance of surface soils. Soil Sci Soc Am J 45:1161–1165

    Article  Google Scholar 

  • Suri M, Hofierka J (2004) A new GIS-based solar radiation model and its application to photovoltaic assessments. Trans GIS 8:175–190. doi:10.1111/j.1467-9671.2004.00174.x

    Article  Google Scholar 

  • Theseira MA, Thomas G, Sannier CAD (2002) An evaluation of spectral mixture modeling applied to a semi-arid environment. Int J Remote Sens 23:687–700. doi:10.1080/01431160010019652

    Article  Google Scholar 

  • Thomas CD (1992) The establishment of rare insects in vacant habitat patches. Antenna 16:89–93

    Google Scholar 

  • Travesí R, Pérez-López FJ (2002) Nuevas poblaciones de Agriades zullichi Hemming, 1930 (Lepidoptera: Lycaenidae). Acta Granatense 1(1–2):158–160

    Google Scholar 

  • Travesí R, Pérez-López FJ, Barea-Azcón JM, Fuentes F (2008) Agriades zullichi Hemming, 1933. In: Barea-Azcón JM, Ballesteros-Duperón E, Moreno D (eds) Libro Rojo de los Invertebrados de Andalucía. Consejería de Medio Ambiente. Junta de Andalucía, Sevilla, pp 1115–1119

    Google Scholar 

  • Tucker CJ (1979) Red and infrared linear combinations for monitoring vegetation. Remote Sens Environ 8:127–150. doi:10.1016/0034-4257(79)90013-0

    Article  Google Scholar 

  • Van Swaay CAM, Cuttelod A, Collins S, Maes D, Munguira ML, Šašić M, Settele J, Verovnik R, Verstrael T, Warren M, Wiemers M, Wynhof I (2010a) European red list of butterfies. IUCN (International Union for Conservation of Nature) and butterfly conservation Europe in collaboration with the European Union. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Van Swaay CAM, Wynhoff I, Verovnik R, Wiemers M, Munguira, ML, Maes D, Šašić M, Verstrael T, Warren M, Settele J (2010b) Plebejus zullichi. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.2. www.iucnredlist.org. Downloaded on 01 Dec 2012

  • Vande Velde L, Turlure C, Van Dyck H (2011) Body temperature and territory selection by males of the speckled wood butterfly (Pararge aegeria): What makes a forest sunlit patch a rendezvous site? Ecol Entomol 36(2):161–169. doi:10.1111/j.1365-2311.2010.01257.x

    Article  Google Scholar 

  • VanDerWal J, Shoo LP, Graham C, Williams SE (2009) Selecting pseudo-absence data for presence-only distribution modeling: how far should you stray from what you know? Ecol Model 220:589–594. doi:10.1111/j.2041-210X.2011.00172.x

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Book  Google Scholar 

  • Wilson RJ, Gutiérrez D, Gutiérrez J, Montserrat VJ (2007) An elevational shift in butterfly species richness and composition accompanying recent climate change. Glob Change Biol 13(9):1873–1887. doi:10.1111/j.1365-2486.2007.01418.x

    Article  Google Scholar 

  • Wipf S, Rixen C, Fischer M, Schmid B, Stoeckli V (2005) Effects of ski piste preparation on alpine vegetation. J Appl Ecol 42:306–316. doi:10.1111/j.1365-2664.2005.01011.x

    Article  Google Scholar 

Download references

Acknowledgments

We thank to Mario Ruiz, Ignacio Henares and Mariano Guerrero for their help in the field work. Alberto Tinaut and Roberto Travesí contributed with important field data. Javier Sánchez, Blanca Ramos and Ignacio Maldonado provided technical and administrative support. We also thank Prof. Regino Zamora for his useful comments on the draft manuscript. We thank Neil Thompson, Irene Ballesta, María Carbayo and Blanca Ramos for improving the English editing of this manuscript. Peter White, Miguel L. Munguira and two anonymous referees for constructive criticism on the manuscript. The research was funded by the Consejería de Medio Ambiente y Ordenación del Territorio through the European Union (FEDER Project) and is part of the Global Change Observatory of Sierra Nevada. BMB was Granted by the MIGRAME research Project (RNM-6734, Government of Andalusia).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Miguel Barea-Azcón.

Additional information

Communicated by Peter J. T. White.

José Miguel Barea-Azcón and Blas M. Benito have contributed equally to this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barea-Azcón, J.M., Benito, B.M., Olivares, F.J. et al. Distribution and conservation of the relict interaction between the butterfly Agriades zullichi and its larval foodplant (Androsace vitaliana nevadensis). Biodivers Conserv 23, 927–944 (2014). https://doi.org/10.1007/s10531-014-0643-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-014-0643-4

Keywords

Navigation