, Volume 175, Issue 3, pp 861–873 | Cite as

Climate conditions and resource availability drive return elevational migrations in a single-brooded insect

  • David GutiérrezEmail author
  • Robert J. Wilson
Population ecology - Original research


Seasonal elevational migrations have important implications for life-history evolution and ecological responses to environmental change. However, for most species, particularly invertebrates, evidence is still scarce for the existence of such migrations, as well as for the potential causes. We tested the extent to which seasonal abundance patterns in central Spain for overwintering (breeding) and summer (non-breeding) individuals of the butterfly Gonepteryx rhamni were consistent with three hypotheses explaining elevational migration: resource limitation (host plant and flower availability), physiological constraints of weather (maximum temperatures) and habitat limitation (forest cover for overwintering). For overwintering adults, abundance was positively associated with host plant density during two intensive survey seasons (2007–2008), and the elevational distribution was relatively stable over a 7-year period (2006–2012). The elevational distribution of summer adults was highly variable, apparently related both to temperature and habitat type. Sites occupied by adults in the summer were on average 3 °C cooler than their breeding sites, and abundance showed negative associations with summer temperature, and positive associations with forest cover and host plant density in 2007 and 2008. The results suggest that the extent of uphill migration in summer could be driven by different factors, depending on the year, and are mostly consistent with the physiological constraint and habitat limitation hypotheses. In contrast, the patterns for overwintering adults suggest that downhill migration can be explained by resource availability. Climate change could generate bottlenecks in the populations of elevational migrant species by constraining the area of specific seasonal habitat networks or by reducing the proximity of environments used at different times of year.


Climate change Elevational distribution Gonepteryx rhamni Lepidoptera Seasonal movements 



J. Gutiérrez Illán and S.B.Díez assisted with fieldwork and S. Nieto-Sánchez and T. Izquierdo helped with climate data. The research was funded by Universidad Rey Juan Carlos/Comunidad de Madrid (URJC-CM-2006-CET-0592), the Spanish Ministry of Economy and Competitiveness (REN2002-12853-E/GLO, CGL2005-06820/BOS, CGL2008-04950/BOS and CGL2011-30259), the British Ecological Society and the Royal Society. Access and research permits were provided by Comunidad de Madrid, Parque Natural de Peñalara, Parque Regional de la Cuenca Alta del Manzanares, Parque Regional del Curso Medio del Río Guadarrama, Patrimonio Nacional and Ayuntamiento de Cercedilla.

Supplementary material

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Supplementary material 1 (PDF 415 kb)


  1. Bartoń K (2012) MuMIn: multi-model inference. R package version 1.6.6. Available at: Accessed 19 Jan 2012
  2. Boyle WA (2008) Can variation in risk of nest predation explain altitudinal migration in tropical birds? Oecologia 155:397–403PubMedCrossRefGoogle Scholar
  3. Boyle WA (2010) Does food abundance explain altitudinal migration in a tropical frugivorous bird? Can J Zool 88:204–213CrossRefGoogle Scholar
  4. Boyle WA, Norris DR, Guglielmo CG (2010) Storms drive altitudinal migration in a tropical bird. Proc R Soc B 277:2511–2519PubMedCentralPubMedCrossRefGoogle Scholar
  5. Brambilla M, Falco R, Negri I (2012) A spatially explicit assessment of within-season changes in environmental suitability for farmland birds along an altitudinal gradient. Anim Conserv 15:638–647CrossRefGoogle Scholar
  6. Brattström O, Bensch S, Wassenaar LI, Hobson KA, Åkesson S (2010) Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography 33:720–729CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  8. Chapman JW, Bell JR, Burgin LE, Reynolds DR, Pettersson LB, Hill JK, Bonsall MB, Thomas JA (2012) Seasonal migration to high latitudes results in major reproductive benefits in an insect. Proc Natl Acad Sci USA 109:14924–14929PubMedCentralPubMedCrossRefGoogle Scholar
  9. Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Stat 45:90–96Google Scholar
  10. Dingle H, Drake VA (2007) What is migration? Bioscience 57:113–121CrossRefGoogle Scholar
  11. Diniz-Filho JAF, Rangel TFLVB, Bini LM (2008) Model selection and information theory in geographical ecology. Global Ecol Biogeogr 17:479–488CrossRefGoogle Scholar
  12. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder 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 36:27–46CrossRefGoogle Scholar
  13. Environmental Systems Research Institute Inc. (ESRI) (2001) ArcGIS 8.1. ESRI Inc., RedlandsGoogle Scholar
  14. Farr TG, Rosen PA, Caro E, Crippen R, Duren R, Hensley S, Kobrick M, Paller M, Rodriguez E, Roth L, Seal D, Shaffer S, Shimada J, Umland J, Werner M, Oskin M, Burbank D, Alsdorf D (2007) The shuttle radar topography mission. Rev Geophys 45:RG2004Google Scholar
  15. Flockhart DTT, Wassenaar LI, Martin TG, Hobson KA, Wunder MB, Norris DR (2013) Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America. Proc R Soc B 280:20131087PubMedCrossRefGoogle Scholar
  16. García-Barros E, Munguira ML, Cano JM, Romo H, Garcia-Pereira P, Maravalhas ES (2004) Atlas of the butterflies of the Iberian Peninsula and Balearic Islands (Lepidoptera: Papilionoidea and Hesperioidea). Sociedad Entomológica Aragonesa, ZaragozaGoogle Scholar
  17. García-Barros E, Munguira ML, Stefanescu C, Vives Moreno A (2013) Lepidoptera Papilionoidea. In: Ramos MA et al (eds) Fauna Ibérica, vol 37. Museo Nacional de Ciencias Naturales, CSIC, MadridGoogle Scholar
  18. Gutiérrez Illán J, Gutiérrez D, Wilson RJ (2010) The contributions of topoclimate and land cover to species distributions and abundance: fine resolution tests for a mountain butterfly fauna. Global Ecol Biogeogr 19:159–173CrossRefGoogle Scholar
  19. Gutiérrez D, Thomas CD (2000) Marginal range expansion in a host-limited butterfly species Goneptery rhamni. Ecol Entomol 25:165–170CrossRefGoogle Scholar
  20. Holland RA, Wikelski M, Wilcove DS (2006) How and why do insects migrate? Science 313:794–796PubMedCrossRefGoogle Scholar
  21. Hunt JH, Brodie RJ, Carithers TP, Goldstein PZ, Janzen DH (1999) Dry season migration by Costa Rican lowland paper wasps to high elevation cold dormancy sites. Biotropica 31:192–196Google Scholar
  22. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci USA 97:1630–1633PubMedCentralPubMedCrossRefGoogle Scholar
  23. Larsen TB (1976) The importance of migration to the butterfly faunas of Lebanon, East Jordan, and Egypt (Lepidoptera, Rhopalocera). Notulae Entomol 56:73–83Google Scholar
  24. Larsen TB (1982) The importance of migration to the butterfly fauna of Arabia (Lep., Rhopalocera). Atalanta 13:248–259Google Scholar
  25. Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier, AmsterdamGoogle Scholar
  26. Mac Nally R (1996) Hierarchical partitioning as an interpretative tool in multivariate inference. Aust J Ecol 21:224–228CrossRefGoogle Scholar
  27. Mac Nally R (2002) Multiple regression and inference in ecology and conservation biology: further comment on identifying important predictor variables. Biodiv Conserv 11:1397–1401CrossRefGoogle Scholar
  28. Mac Nally R, Walsh CJ (2004) Hierarchical partitioning public-domain software. Biodiv Conserv 13:659–660CrossRefGoogle Scholar
  29. Marini MA, Barbet-Massin M, Lopes LE, Jiguet F (2013) Geographic and seasonal distribution of the cock-tailed tyrant (Alectrurus tricolor) inferred from niche modelling. J Ornithol 154:393–402CrossRefGoogle Scholar
  30. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall/CRC, Boca RatonCrossRefGoogle Scholar
  31. McGuire LP, Boyle WA (2013) Altitudinal migration in bats: evidence, patterns and drivers. Biol Rev 88:767–786PubMedGoogle Scholar
  32. 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 77:145–155PubMedCrossRefGoogle Scholar
  33. Mikkola K (2003) The red admiral butterfly (Vanessa atalanta, Lepidoptera: Nymphalidae) is a true seasonal migrant: an evolutionary puzzle resolved? Eur J Entomol 100:625–626CrossRefGoogle Scholar
  34. Ministerio de Medio Ambiente (2000) Mapa forestal de España. Escala 1:50000. Provincia de Madrid. Ministerio de Medio Ambiente, MadridGoogle Scholar
  35. Ministerio de Medio Ambiente (2002a) Mapa forestal de España. Escala 1:50000. Provincia de Ávila. Ministerio de Medio Ambiente, MadridGoogle Scholar
  36. Ministerio de Medio Ambiente (2002b) Mapa forestal de España. Escala 1:50000. Provincia de Guadalajara. Ministerio de Medio Ambiente, MadridGoogle Scholar
  37. Ministerio de Medio Ambiente (2003) Mapa forestal de España. Escala 1:50000. Provincia de Segovia. Ministerio de Medio Ambiente, MadridGoogle Scholar
  38. Norbu N, Wikelski MC, Wilcove DS, Partecke J, Ugyen, Tenzin U, Sherub, Tempa T (2013) Partial altitudinal migration of a Himalayan forest pheasant. PLoS One 8(4):e60979PubMedCentralPubMedCrossRefGoogle Scholar
  39. Osborne JL, Loxdale HD, Woiwod IP (2002) Monitoring insect dispersal: methods and approaches. In: Bullock JM, Kenward RE, Hails RS (eds) Dispersal ecology. Blackwell Science Ltd, Malden, pp 24–49Google Scholar
  40. Pollard E, Greatorex-Davies JN (1998) Increased abundance of the red admiral butterfly Vanessa atalanta in Britain: the roles of immigration, overwintering and breeding within the country. Ecol Lett 1:77–81CrossRefGoogle Scholar
  41. Pollard E, Hall ML (1980) Possible movement of Gonepteryx rhamni (L.) (Lepidoptera: Pieridae) between hibernating and breeding areas. Entomol Gaz 31:217–220Google Scholar
  42. Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman and Hall, LondonGoogle Scholar
  43. Pruess KP (1967) Migration of the army cutworm, Chorizagrotis auxiliaris (Lepidoptera: Noctuidae). I. Evidence for a migration. Ann Entomol Soc Am 60:910–920Google Scholar
  44. Ramenofsky M, Wingfield JC (2007) Regulation of migration. Bioscience 57:135–143CrossRefGoogle Scholar
  45. Rankin MA, Burchsted CA (1992) The cost of migration in insects. Annu Rev Entomol 37:533–559CrossRefGoogle Scholar
  46. Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227CrossRefGoogle Scholar
  47. Samraoui B, Bouzid S, Boulahbat R, Corbet PS (1998) Postponed reproductive maturation in upland refuges maintains life-cycle continuity during the hot, dry season in Algerian dragonflies (Anisoptera). Int J Odonatol 1:119–135CrossRefGoogle Scholar
  48. Sawada M (1999) Rookcase: an Excel 97/2000 visual basic (VB) add-in for exploring global and local spatial autocorrelation. Bull Ecol Soc Am 80:231–234CrossRefGoogle Scholar
  49. Shapiro AM (1973) Altitudinal migration of butterflies in the central Sierra Nevada. J Res Lepid 12:231–235Google Scholar
  50. Shapiro AM (1974a) Altitudinal migration of central California butterflies. J Res Lepid 13:157–161Google Scholar
  51. Shapiro AM (1974b) Movements of Nymphalis californica (Nymphalidae) in 1972. J Lepid Soc 28:75–78Google Scholar
  52. Shapiro AM (1975) Why do California tortoiseshells migrate? J Res Lepid 14:93–97Google Scholar
  53. Shapiro AM (1980) Mediterranean climate and butterfly migration: an overview of the California fauna. Atalanta 11:161–188Google Scholar
  54. Southwood TRE (1977) Habitat, the templet for ecological strategies. J Anim Ecol 46:337–365CrossRefGoogle Scholar
  55. Stefanescu C (2001) The nature of migration in the red admiral butterfly Vanessa atalanta: evidence from the population ecology in its southern range. Ecol Entomol 26:525–536CrossRefGoogle Scholar
  56. Stefanescu C, Traveset A (2009) Factors influencing the degree of generalization in flower use by Mediterranean butterflies. Oikos 118:1109–1117CrossRefGoogle Scholar
  57. Stefanescu C, Alarcón M, Ávila A (2007) Migration of the painted lady butterfly, Vanessa cardui, to north-eastern Spain is aided by African wind currents. J Anim Ecol 76:888–898PubMedCrossRefGoogle Scholar
  58. Stefanescu C, Askew RR, Corbera J, Shaw MR (2012) Parasitism and migration in southern Palaearctic populations of the painted lady butterfly, Vanessa cardui (Lepidoptera: Nymphalidae). Eur J Entomol 109:85–94CrossRefGoogle Scholar
  59. Stefanescu C, Páramo F, Åkesson S, Alarcón M, Ávila A, Brereton T, Carnicer J, Cassar LF, Fox R, Heliölä J, Hill JK, Hirneisen N, Kjellén N, Kühn E, Kuussaari M, Leskinen M, Liechti F, Musche M, Regan EC, Reynolds DR, Roy DB, Ryrholm N, Schmaljohann H, Settele J, Thomas CD, van Swaay C, Chapman JW (2013) Multi-generational long-distance migration of insects: studying the painted lady butterfly in the Western Palaearctic. Ecography 36:474–486CrossRefGoogle Scholar
  60. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: Accessed 20 Jan 2012
  61. Tolman T, Lewington R (1997) Butterflies of Britain and Europe. HarperCollins, LondonGoogle Scholar
  62. Urquhart FA, Urquhart NR (1978) Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Can J Zool 56:1759–1764CrossRefGoogle Scholar
  63. Wikelski M, Moskowitz D, Adelman JS, Cochran J, Wilcove DS, May ML (2006) Simple rules guide dragonfly migration. Biol Lett 2:325–329PubMedCentralPubMedCrossRefGoogle Scholar
  64. Wiklund C, Lindfors V, Forsberg J (1996) Early male emergence and reproductive phenology of the adult overwintering butterfly Gonepteryx rhamni in Sweden. Oikos 75:227–240CrossRefGoogle Scholar
  65. Williams CB (1930) The migration of butterflies. Oliver and Boyd, EdinburghGoogle Scholar
  66. Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New YorkGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y TecnologíaUniversidad Rey Juan CarlosMóstolesSpain
  2. 2.College of Life and Environmental SciencesUniversity of ExeterExeterUK

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