Abstract
Climate change is affecting high-altitude and high-latitude communities in significant ways. In the short growing season of subarctic habitats, it is essential that the timing and duration of phenological phases match favorable environmental conditions. We explored the time of the first appearance of flowers (first flowering day, FFD) and flowering duration across subarctic species composing different communities, from boreal forest to tundra, along an elevational gradient (600–800 m). The study was conducted on Mount Irony (856 m), North-East Canada (54°90′N, 67°16′W) during summer 2012. First, we quantified phylogenetic signal in FFD at different spatial scales. Second, we used phylogenetic comparative methods to explore the relationship between FFD, flowering duration, and elevation. We found that the phylogenetic signal for FFD was stronger at finer spatial scales and at lower elevations, indicating that closely related species tend to flower at similar times when the local environment is less harsh. The comparatively weaker phylogenetic signal at higher elevation may be indicative of convergent evolution for FFD. Flowering duration was correlated significantly with mean FFD, with later-flowering species having a longer flowering duration, but only at the lowest elevation. Our results indicate significant evolutionary conservatism in responses to phenological cues, but high phenotypic plasticity in flowering times. We suggest that phylogenetic relationships should be considered in the search for predictions and drivers of flowering time in comparative analyses, because species cannot be considered as statistically independent. Further, phenological drivers should be measured at spatial scales such that variation in flowering matches variation in environment.
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References
Arft AM, Walker MD, Gurevitch JEA, Alatalo JM, Bret-Harte MS, Dale M, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511
Blionis GJ, Halley JM, Vokou D (2008) Flowering phenology of Campanula on Mt Olympos, Greece. Ecography 24:696–706
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Bolmgren K (1998) The use of synchronization measures in studies of plant reproductive phenology. Oikos 82:411–415
Bolmgren K, Cowan DP (2008) Time - size tradeoffs: a phylogenetic comparative study of flowering time, plant height and seed mass in a north-temperate flora. Oikos 117:424–429
Bolmgren K, Lönnberg K (2005) Herbarium data reveal an association between fleshy fruit type and earlier flowering time. Int J Plant Sci 166:663–670
Bolmgren K, Eriksson O, Linder HP (2003) Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms. Evolution 57:2001–2011
Cavender–Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715
Davis CC, Willis CG, Primack RB, Miller-Rushing AJ (2010) The importance of phylogeny to the study of phenological response to global climate change. Philos Trans R Soc B: Biol Sci 365:3201–3213
Debussche M, Garnier E, Thompson JD (2004) Exploring the causes of variation in phenology and morphology in Mediterranean geophytes: a genus-wide study of Cyclamen. Bot J Linn Soc 145:469–484
Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73:69–86
Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 783–791
Fenner M (1998) The phenology of growth and reproduction in plants. Perspect Plant Ecol Evol Syst 1:78–91
Fitter AH, Fitter RSR, Harris ITB, Williamson MH (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 55–60
Forrest J, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440
Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726
Gordo O, Sanz JJ (2009) Long-term temporal changes of plant phenology in the Western Mediterranean. Glob Chang Biol 15:1930–1948
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology, vol 239. Oxford University Press, Oxford
Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3:457–463
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362
Jia P, Twenke B, Xiangqian L, Guozhen D (2011) Relationships between flowering phenology and functional traits in eastern Tibet alpine meadow. Arct Antarct Alp Res 43:585–592
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 11:569–574
Kramer K (1995) Phenotypic plasticity of the phenology of seven European tree species in relation to climatic warming. Plant Cell Environ 18:93–104
Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113
Kudo G, Suzuki S (2002) Relationships between flowering phenology and fruit-set of dwarf shrubs in alpine fellfields in northern Japan: a comparison with a subarctic heathland in northern Sweden. Arct Antarct Alp Res 185–190
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 20. Bioinformatics 23:2947–2948
Mazer SM, Travers SE, Cook BI, Davies TJ., Bolmgren K, Kraft NJ, Salomin N and Inouye DI (2013) Flowering date of taxonomic families predicts phenological sensitivity to temperature: implications for forecasting the effects of climate change on unstudied taxa. Am J Bot (in press)
Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57:243–263
Oberrath R, Böhning-Gaese K (2002) Phenological adaptation of ant-dispersed plants to seasonal variation in ant activity. Ecology 83:1412–1420
Orme CDL, Freckleton R, Thomas G, Petzoldt T, Fritz S and Isaac NC (2011) Comparative analysis of phylogenetics and evolution in R. R package version 0.4. URL: http://CRAN.R-project.org/package=caper
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13:1860–1872
Pau S, Wolkovich EM, Cook BI, Davies TJ, Kraft NJB, Bolmgren K, Betancourt JL, Cleland EE (2011) Predicting phenology by integrating ecology, evolution and climate science. Glob Chang Biol 17:3633–3643
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79:1261–1271
Primack RB (1985) Patterns of flowering phenology in communities, populations, individuals and single flowers. In: White J (ed) The population structure of vegetation. Junk, Dordrecht, pp 571–593
R Core Team (2012) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, URL http://www.R-projectorg/
Ranjitkar S, Luedeling E, Shrestha KK, Guan K, Xu J (2012) Flowering phenology of tree rhododendron along an elevation gradient in two sites in the Eastern Himalayas. Int J Biometeorol 57:225–240
Ratnasingham S, Hebert PD (2007). BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes 7:355–364
Sandel B, Arge L, Dalsgaard B, Davies RG, Gaston KJ, Sutherland WJ, Svenning J-C (2011) The influence of late quaternary climate-change velocity on species endemism. Science 334:660–664
Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198–202
Stevens PF (2012) Angiosperm Phylogeny Website Version 12. http://www.mobot.org/MOBOT/research/APweb/. Accessed 27 November 2012
Sundqvist MK, Giesler R, Wardle DA (2011) Within- and across-species responses of plant traits and litter decomposition to elevation across contrasting vegetation types in subarctic tundra. PLoS ONE, 6, e27056
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237
Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC (2008) Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proc Natl Acad Sci USA 105:17029–17033
Acknowledgments
We are grateful to Łukasz Grewling and Jan F. Gogarten who made valuable comments on the manuscript. The study was supported by the Natural Sciences and Engineering Research Council, the Northern Scientific Training Program and the Quebec Centre for Biodiversity Science. We also thank McGill Subarctic Research Station and Hardy B. Granberg for providing infrastructure and Claudel Fournier for his help with field work.
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Lessard-Therrien, M., Davies, T.J. & Bolmgren, K. A phylogenetic comparative study of flowering phenology along an elevational gradient in the Canadian subarctic. Int J Biometeorol 58, 455–462 (2014). https://doi.org/10.1007/s00484-013-0672-9
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DOI: https://doi.org/10.1007/s00484-013-0672-9