Abstract
The timing of many biological events, including butterfly imago emergence, has advanced under climate change, with the rate of these phenological changes often differing among taxonomic groups. Such inter-taxa variability can lead to phenological mismatches. For example, the timing of a butterfly’s flight period may become misaligned with a key nectar resource, potentially increasing the extinction risk to both species. Here we fit statistical models to field data to determine how the phenology of the marbled white butterfly, Melanargia galathea, and its main nectar source, greater knapweed, Centaurea scabiosa, have changed over recent years at three sites across the UK. We also consider whether topographical diversity affects C. scabiosa’s flowering period. At our focal site, on the species’ northern range limit, we find that over a 13-year period the onset of C. scabiosa’s flowering period has become later whilst there is no obvious trend over time in the onset of M. galathea’s flight period. In recent years, butterflies have started to emerge before their key nectar source was available across most of the site. This raises the intriguing possibility that phenological mismatch could be an unrecognised determinant of range limits for some species. However, the presence of topographical diversity within the site decreased the chance of a mismatch occurring by increasing the length of the flowering period by up to 14 days. We suggest that topographical diversity could be an important component in minimising phenological mismatches under future climate change.
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References
Altermatt F (2010) Tell me what you eat and I’ll tell you when you fly: diet can predict phenological changes in response to climate change. Ecol Lett 13:1475–1484. doi:10.1111/j.1461-0248.2010.01534.x
Altermatt F (2012) Temperature-related shifts in butterfly phenology depend on the habitat. Glob Change Biol 18:2429–2438. doi:10.1111/j.1365-2486.2012.02727.x
Amano T, Smithers RJ, Sparks TH, Sutherland WJ (2010) A 250-year index of first flowering dates and its response to temperature changes. Proc R Soc B-Biol Sci 277:2451–2457. doi:10.1098/rspb.2010.0291
Araujo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753. doi:10.1111/j.1466-8238.2007.00359.x
Asher J, Warren M, Fox R, Harding P, Jeffcoate G, Jeffcoate S (2001) Millenium atlas of butterflies in Britain and Ireland. Oxford University Press, Oxford
Audusseau H, Nylin S, Janz N (2013) Implications of a temperature increase for host plant range: predictions for a butterfly. Ecol Evol 3:3021–3029. doi:10.1002/ece3.696
Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci USA 108:20645–20649. doi:10.1073/pnas.1115559108
Bartomeus I, Park MG, Gibbs J, Danforth BN, Lakso AN, Winfree R (2013) Biodiversity ensures plant–pollinator phenological synchrony against climate change. Ecol Lett 16:1331–1338. doi:10.1111/ele.12170
Bergman KO (2001) Population dynamics and the importance of habitat management for conservation of the butterfly Lopinga achine. J Appl Ecol 38:1303–1313. doi:10.1046/j.0021-8901.2001.00672.x
Bryant SR, Thomas CD, Bale JS (2002) The influence of thermal ecology on the distribution of three nymphalid butterflies. J Appl Ecol 39:43–55. doi:10.1046/j.1365-2664.2002.00688.x
Bulmer MG (1983) Models for the evolution of protandry in insects. Theor Popul Biol 23:314–322. doi:10.1016/0040-5809(83)90021-7
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Calinger KM, Queenborough S, Curtis PS (2013) Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America. Ecol Lett 16:1037–1044. doi:10.1111/ele.12135
Cherry SG, Derocher AE, Thiemann GW, Lunn NJ (2013) Migration phenology and seasonal fidelity of an Arctic marine predator in relation to sea ice dynamics. J Anim Ecol 82:912–921. doi:10.1111/1365-2656.12050
Cormont A, Wamelink GWW, Jochem R, WallisDeVries MF, Wegman RMA (2013) Host plant-mediated effects of climate change on the occurrence of the Alcon blue butterfly (Phengaris alcon). Ecol Model 250:329–337. doi:10.1016/j.ecolmodel.2012.11.022
Crick HQP, Sparks TH (1999) Climate change related to egg-laying trends. Nature 399:423–424. doi:10.1038/20839
Crick HQP, Dudley C, Glue DE, Thomson DL (1997) UK birds are laying eggs earlier. Nature 388:526–526. doi:10.1038/41453
Devictor V et al (2012) Differences in the climatic debts of birds and butterflies at a continental scale. Nat Clim Change 2:121–124. doi:10.1038/nclimate1347
Diamond SE, Frame AM, Martin RA, Buckley LB (2011) Species’ traits predict phenological responses to climate change in butterflies. Ecology 92:1005–1012
Doi H, Gordo O, Katano I (2008) Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Clim Res 36:181–190. doi:10.3354/cr00741
Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074. doi:10.1126/science.289.5487.2068
Fabina NS, Abbott KC, Gilman RT (2010) Sensitivity of plant–pollinator-herbivore communities to changes in phenology. Ecol Model 221:453–458. doi:10.1016/j.ecolmodel.2009.10.020
Fitter AH, Fitter RSR (2002) Rapid Changes in Flowering Time in British plants. Science 296:1689–1691. doi:10.1126/science.1071617
Fox R, Asher J, Brereton T, Roy D, Warren M (2006) The state of butterflies in Britain and Ireland. NatureBureau i–viii, 1–112
Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495. doi:10.1007/s00442-005-0240-z
Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD (2008) Assisted colonization and rapid climate change. Science 321:345–346. doi:10.1126/science.1157897
Hopkins JJ, Allison HM, Walmsley CA, Gaywood M, Thurgate G (2007) Conserving biodiversity in a changing climate: guidance on building capacity to adapt. Defra, London
Kraemer 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
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320. doi:10.1890/12-2003.1
Lenda M, Skorka P (2010) Patch occupancy, number of individuals and population density of the Marbled White in a changing agricultural landscape. Acta Oecol-Int J Ecol 36:497–506. doi:10.1016/j.actao.2010.07.002
Loertscher M, Erhardt A, Zettel J (1995) Microdistribution of butterflies in a mosaic-like habitat—the role of nectar sources. Ecography 18:15–26. doi:10.1111/j.1600-0587.1995.tb00115.x
Loss SR, Terwilliger LA, Peterson AC (2011) Assisted colonization: integrating conservation strategies in the face of climate change. Biol Conserv 144:92–100. doi:10.1016/j.biocon.2010.11.016
Lunt ID et al (2013) Using assisted colonisation to conserve biodiversity and restore ecosystem function under climate change. Biol Conserv 157:172–177. doi:10.1016/j.biocon.2012.08.034
Marra PP, Francis CM, Mulvihill RS, Moore FR (2005) The influence of climate on the timing and rate of spring bird migration. Oecologia 142:307–315. doi:10.1007/s00442-004-1725-x
Mason THE, Stephens PA, Apollonio M, Willis SG (2014) Predicting potential responses to future climate in an alpine ungulate: interspecific interactions exceed climate effects. Glob Change Biol. doi:10.1111/gcb.12641
McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21:297–302. doi:10.1111/j.1523-1739.2007.00676.x
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717. doi:10.1111/j.1461-0248.2007.01061.x
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659–659. doi:10.1038/17709
Murphy JM et al (2009) UK climate projections science report: climate change projections. Met Office Hadley Centre, Exeter
Nakazawa T, Doi H (2012) A perspective on match/mismatch of phenology in community contexts. Oikos 121:489–495. doi:10.1111/j.1600-0706.2011.20171.x
Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Change Biol 13:1860–1872. doi:10.1111/j.1365-2486.2007.01404.x
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286
Pellerin M, Delestrade A, Mathieu G, Rigault O, Yoccoz NG (2012) Spring tree phenology in the Alps: effects of air temperature, altitude and local topography. Eur J For Res 131:1957–1965. doi:10.1007/s10342-012-0646-1
Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman & Hall, London
Primack D, Imbres C, Primack RB, Miller-Rushing AJ, Del Tredici P (2004) Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Am J Bot 91:1260–1264. doi:10.3732/ajb.91.8.1260
Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant–pollinator interactions. Ecol Lett 14:69–74. doi:10.1111/j.1461-0248.2010.01557.x
Ricciardi A, Simberloff D (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24:248–253. doi:10.1016/j.tree.2008.12.006
Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227. doi:10.1111/j.1365-2664.2007.01377.x
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
Roy DB, Rothery P, Moss D, Pollard E, Thomas JA (2001) Butterfly numbers and weather: predicting historical trends in abundance and the future effects of climate change. J Anim Ecol 70:201–217. doi:10.1046/j.1365-2656.2001.00480.x
Sparks TH, Yates TJ (1997) The effect of spring temperature on the appearance dates of British butterflies 1883–1993. Ecography 20:368–374
Stace C (1991) New flora of the British Isles. Cambridge University Press, Cambridge
Stefanescu C, Penuelas J, Filella I (2003) Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Glob Change Biol 9:1494–1506. doi:10.1046/j.1365-2486.2003.00682.x
Thackeray SJ et al (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313. doi:10.1111/j.1365-2486.2010.02165.x
Thomas CD (2011) Translocation of species, climate change, and the end of trying to recreate past ecological communities. Trends Ecol Evol 26:216–221. doi:10.1016/j.tree.2011.02.006
Thomas JA, Simcox DJ, Hovestadt T (2011) Evidence based conservation of butterflies. J Insect Conserv 15:241–258. doi:10.1007/s10841-010-9341-z
Turlure C, Van Dyck H (2009) On the consequences of aggressive male mate-locating behaviour and micro-climate for female host plant use in the butterfly Lycaena hippothoe. Behav Ecol Sociobiol 63:1581–1591. doi:10.1007/s00265-009-0753-2
van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: The importance of synchrony. In: Annual Review of Entomology, vol 52. Annual Review of Entomology. Annual Reviews, Palo Alto, pp 37–55. doi:10.1146/annurev.ento.52.110405.091418
van Halder I, Barbaro L, Jactel H (2011) Conserving butterflies in fragmented plantation forests: are edge and interior habitats equally important? J Insect Conserv 15:591–601. doi:10.1007/s10841-010-9360-9
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B Biol Sci 272:2561–2569. doi:10.1098/rspb.2005.3356
Vitt P, Havens K, Hoegh-Guldberg O (2009) Assisted migration: part of an integrated conservation strategy. Trends Ecol Evol 24:473–474. doi:10.1016/j.tree.2009.05.007
Wallisdevries MF, Van Swaay CAM, Plate CL (2012) Changes in nectar supply: a possible cause of widespread butterfly decline. Curr Zool 58:384–391
Warren MS et al (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65–69. doi:10.1038/35102054
Weiss SB, Murphy DD, White RR (1988) Sun, slope and butterflies—topographic determinants of habitat quality for Euphydryas-editha. Ecology 69:1486–1496. doi:10.2307/1941646
Wiklund C, Solbreck C (1982) Adaptive versus incidental explanations for the occurrence of protandry in a butterfly, Leptidea-sinapis L. Evolution 36:56–62. doi:10.2307/2407966
Willis SG, Hill JK, Thomas CD, Roy DB, Fox R, Blakeley DS, Huntley B (2009) Assisted colonization in a changing climate: a test-study using two U.K. butterflies. Conserv Lett 2:46–51. doi:10.1111/j.1755-263X.2008.00043.x
Wilson A (1985) Flavonoid pigments in marbled white butterfly (Melanargia-galathea) are dependent on flavonoid content of larval diet. J Chem Ecol 11:1161–1179. doi:10.1007/bf01024106
Acknowledgments
Funding was provided by Grevillea Trust studentships to B.J.H. and C.L.K., both supervised by S.G.W. and cosupervised by S.A.R. and Dr Robert Baxter respectively. Data were supplied by the UK Butterfly Monitoring Scheme (UKBMS) and Yorkshire Wildlife Trust. The UKBMS is operated by the Centre for Ecology & Hydrology and Butterfly Conservation and funded by a multi-agency consortium including the Countryside Council for Wales, Defra, the Joint Nature Conservation Committee, Forestry Commission, Natural England, the Natural Environment Research Council, and Scottish Natural Heritage. The UKBMS is indebted to all volunteers who contribute data to the scheme. We thank Yorkshire Wildlife Trust, Durham City Council and the Wildlife Trust for Bedfordshire, Cambridgeshire and Northamptonshire for access to their land and numerous field assistants for their help in collecting data. We are grateful to two anonymous reviewers for helpful comments on an earlier draft.
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Hindle, B.J., Kerr, C.L., Richards, S.A. et al. Topographical variation reduces phenological mismatch between a butterfly and its nectar source. J Insect Conserv 19, 227–236 (2015). https://doi.org/10.1007/s10841-014-9713-x
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DOI: https://doi.org/10.1007/s10841-014-9713-x