Abstract
Climate change has resulted in major changes in the phenology—i.e. the timing of seasonal activities, such as flowering and bird migration—of some species but not others. These differential responses have been shown to result in ecological mismatches that can have negative fitness consequences. However, the ways in which climate change has shaped changes in biodiversity within and across communities are not well understood. Here, we build on our previous results that established a link between plant species' phenological response to climate change and a phylogenetic bias in species' decline in the eastern United States. We extend a similar approach to plant and bird communities in the United States and the UK that further demonstrates that climate change has differentially impacted species based on their phylogenetic relatedness and shared phenological responses. In plants, phenological responses to climate change are often shared among closely related species (i.e. clades), even between geographically disjunct communities. And in some cases, this has resulted in a phylogenetically biased pattern of non-native species success. In birds, the pattern of decline is phylogenetically biased but is not solely explained by phenological response, which suggests that other traits may better explain this pattern. These results illustrate the ways in which phylogenetic thinking can aid in making generalizations of practical importance and enhance efforts to predict species' responses to future climate change.
References
-
Ackerly D. D. . 2004 Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. Am. Nat. 163, 654–671. Crossref, PubMed, Web of Science, Google Scholar -
Amano T.& Yamaura Y. . 2007 Ecological and life-history traits related to range contractions among breeding birds in Japan. Biol. Conserv. 137, 271–282. (doi:10.1016/j.biocon.2007.02.010). Crossref, Web of Science, Google Scholar -
Beatley J. C. . 1974 Phenological events and their environmental triggers in Mojave desert ecosystems. Ecology 55, 856–863. (doi:10.2307/1934421). Crossref, Web of Science, Google Scholar -
Bennett P. M.& Owens I. P. F. . 1997 Variation in extinction risk among birds: chance or evolutionary predisposition? Proc. R. Soc. Lond. B 264, 401–408. (doi:10.1098/rspb.1997.0057). Link, Web of Science, Google Scholar -
Bierzychudek P. . 1981 Pollinator limitation of plant reproductive effort. Am. Nat. 117, 838–840. Crossref, Web of Science, Google Scholar -
Bolker B., 2007 APE: analyses of phylogenetics and evolution. v. 2.1-3. See http://ape.mpl.ird.fr/. Google Scholar -
Both C., Bouwhuis S., Lessells C. M.& Visser M. E. . 2006 Climate change and population declines in a long-distance migratory bird. Nature 441, 81–83. (doi:10.1038/nature04539). Crossref, PubMed, Web of Science, Google Scholar -
Bradley N. L., Leopold A. C., Ross J.& Wellington H. . 1999 Phenological changes reflect climate change in Wisconsin. Proc. Natl Acad. Sci. USA 96, 9701–9704. (doi:10.1073/pnas.96.17.9701). Crossref, PubMed, Web of Science, Google Scholar -
Butler C. J. . 2003 The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America. Ibis 145, 484–495. (doi:10.1046/j.1474-919X.2003.00193.x). Crossref, Web of Science, Google Scholar -
Cadotte M. W., Cardinale B. J.& Oakley T. H. . 2008 Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl Acad. Sci. USA 105, 17 012–17 017. (doi:10.1073/pnas.0805962105). Crossref, Web of Science, Google Scholar -
Cadotte M. W., Hamilton M. A.& Murray B. R. . 2009 Phylogenetic relatedness and plant invader success across two spatial scales. Divers. Distrib. 15, 481–488. (doi:10.1111/j.1472-4642.2009.00560.x). Crossref, Web of Science, Google Scholar -
Cardillo M., Mace G. M., Gittleman J. L., Jones K. E., Bielby J.& Purvis A. . 2008 The predictability of extinction: biological and external correlates of decline in mammals. Proc. R. Soc. B 275, 1441–1448. (doi:10.1098/rspb.2008.0179). Link, Web of Science, Google Scholar -
Cavender-Bares J., Ackerly D. D., Baum D. A.& Bazzaz F. A. . 2004 Phylogenetic overdispersion in Floridian oak communities. Am. Nat. 163, 823–843. Crossref, PubMed, Web of Science, Google Scholar -
Cavender-Bares J., Keen A.& Miles B. . 2006 Phylogenetic structure of floridian plant communities depends on taxonomic and spatial scale. Ecology 87, S109–S122. Crossref, PubMed, Web of Science, Google Scholar -
Cavender-Bares J., Kozak K. H., Fine P. V. A.& Kembel S. W. . 2009 The merging of community ecology and phylogenetic biology. Ecol. Lett. 12, 693–715. (doi:10.1111/j.1461-0248.2009.01314.x). Crossref, PubMed, Web of Science, Google Scholar -
Donoghue M. J. . 2008 A phylogenetic perspective on the distribution of plant diversity. Proc. Natl Acad. Sci. USA 105, 11 549–11 555. (doi:10.1073/pnas.0801962105). Crossref, Web of Science, Google Scholar -
Dukes J. S.& Mooney H. A. . 1999 Does global change increase the success of biological invaders? Trends Ecol. Evol. 14, 135–139. (doi:10.1016/S0169-5347(98)01554-7). Crossref, PubMed, Web of Science, Google Scholar -
Edwards E. J., Still C. J.& Donoghue M. J. . 2007 The relevance of phylogeny to studies of global change. Trends Ecol. Evol. 22, 243–249. (doi:10.1016/j.tree.2007.02.002). Crossref, PubMed, Web of Science, Google Scholar -
Felsenstein J. . 1985 Phylogenies and the comparative method. Am. Nat. 125, 1–15. Crossref, Web of Science, Google Scholar -
Fisher D. O.& Owens I. P. F. . 2004 The comparative method in conservation biology. Trends Ecol. Evol. 19, 391–398. (doi:10.1016/j.tree.2004.05.004). Crossref, PubMed, Web of Science, Google Scholar -
Fitter A. H.& Fitter R. S. R. . 2002 Rapid changes in flowering time in British plants. Science 296, 1689–1691. (doi:10.1126/science.1071617). Crossref, PubMed, Web of Science, Google Scholar -
Gilbert G. S.& Webb C. O. . 2007 Phylogenetic signal in plant pathogen–host range. Proc. Natl Acad. Sci. USA 104, 4979–4983. (doi:10.1073/pnas.0607968104). Crossref, PubMed, Web of Science, Google Scholar -
Harvey P. H.& Pagel M. D. . 1991 The comparative method in evolutionary biology. Oxford, UK: Oxford University Press. Google Scholar -
Johanson U., West J., Lister C., Michaels S., Amasino R.& Dean C. . 2000 Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347. (doi:10.1126/science.290.5490.344). Crossref, PubMed, Web of Science, Google Scholar -
Kang H.& Jang J. . 2004 Flowering patterns among angiosperm species in Korea: diversity and constraints. J. Plant Biol. 47, 348–355. (doi:10.1007/BF03030550). Crossref, Web of Science, Google Scholar -
Knight K. S., Kurylo J. S., Endress A. G., Stewart J. R.& Reich P. B. . 2007 Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol. Invas. 9, 925–937. (doi:10.1007/s10530-007-9091-3). Crossref, Web of Science, Google Scholar -
Lambdon P. W. . 2008 Is invasiveness a legacy of evolution? Phylogenetic patterns in the alien flora of Mediterranean islands. J. Ecol. 96, 46–57. Crossref, Web of Science, Google Scholar -
Lord J., Westoby M.& Leishman M. . 1995 Seed size and phylogeny in six temperate floras: constraints, niche conservatism, and adaptation. Am. Nat. 146, 349–364. Crossref, Web of Science, Google Scholar -
Losos J. B. . 2008 Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 11, 995–1003. (doi:10.1111/j.1461-0248.2008.01229.x). Crossref, PubMed, Web of Science, Google Scholar -
Macmynowski D. P., Root T. L., Ballard G.& Geupel G. R. . 2007 Changes in spring arrival of Nearctic–Neotropical migrants attributed to multiscalar climate. Global Change Biol. 13, 2239–2251. (doi:10.1111/j.1365-2486.2007.01448.x). Crossref, Web of Science, Google Scholar -
Maron J. L., Vila M., Bommarco R., Elmendorf S.& Beardsley P. . 2004 Rapid evolution of an invasive plant. Ecol. Monogr. 74, 261–280. (doi:10.1890/03-4027). Crossref, Web of Science, Google Scholar -
McKinney M. L. . 1997 Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu. Rev. Ecol. Syst. 28, 495–516. (doi:10.1146/annurev.ecolsys.28.1.495). Crossref, Google Scholar -
Mehrhoff L. J., Silander J. A., Leicht S. A., Mosher E. S.& Tabak N. M. . 2003 IPANE: invasive plant atlas of New England. Storrs, CT: Department of Ecology & Evolutionary Biology, University of Connecticut. See http://www.ipane.org. Google Scholar -
Memmott J., Craze P. G., Nickolas M. W.& Price M. V. . 2007 Global warming and the disruption of plant–pollinator interactions. Ecol. Lett. 10, 710–717. (doi:10.1111/j.1461-0248.2007.01061.x). Crossref, PubMed, Web of Science, Google Scholar -
Michaels S. D.& Amasino R. M. . 2001 Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935–941. (doi:10.1105/tpc.13.4.935). Crossref, PubMed, Web of Science, Google Scholar -
Miller-Rushing A. J.& Primack R. B. . 2008 Global warming and flowering times in Thoreau's Concord: a community perspective. Ecology 89, 332–341. (doi:10.1890/07-0068.1). Crossref, PubMed, Web of Science, Google Scholar -
Miller-Rushing A. J., Lloyd-Evans T. L., Primack R. B.& Satzinger P. . 2008 Bird migration times, climate change, and changing population sizes. Glob. Change Biol. 14, 1959–1972. (doi:10.1111/j.1365-2486.2008.01619.x). Crossref, Web of Science, Google Scholar -
Mills A. M. . 2005 Changes in the timing of spring and autumn migration in North American migrant passerines during a period of global warming. Ibis 147, 259–269. (doi:10.1111/j.1474-919X.2005.00380.x). Crossref, Web of Science, Google Scholar -
Møller A. P., Rubolini D.& Lehikoinen E. . 2008 Populations of migratory bird species that did not show a phenological response to climate change are declining. Proc. Natl Acad. Sci. USA 105, 16 195–16 200. (doi:10.1073/pnas.0803825105). Crossref, Web of Science, Google Scholar -
Paradis E.& Claude J. . 2002 Analysis of comparative data using generalized estimating equations. J. Theor. Biol. 218, 175–185. (doi:10.1006/jtbi.2002.3066). Crossref, PubMed, Web of Science, Google Scholar -
Parmesan C. . 2006 Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669. (doi:10.1146/annurev.ecolsys.37.091305.110100). Crossref, Web of Science, Google Scholar -
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). Crossref, Web of Science, Google Scholar -
Parmesan C.& Yohe G. . 2003 A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42. (doi:10.1038/nature01286). Crossref, PubMed, Web of Science, Google Scholar -
Primack R. B., Miller-Rushing A. J.& Dharaneeswaran K. . 2009 Changes in the flora of Thoreau's Concord. Biol. Conserv. 142, 500–508. (doi:10.1016/j.biocon.2008.10.038). Crossref, Web of Science, Google Scholar -
Prinzing A., Durka W., Klotz S.& Brandl R. . 2001 The niche of higher plants: evidence for phylogenetic conservatism. Proc. R. Soc. Lond. B 268, 2383–2389. (doi:10.1098/rspb.2001.1801). Link, Web of Science, Google Scholar -
Proches S., Wilson J. R. U., Richardson D. M.& Rejmánek M. . 2008 Searching for phylogenetic pattern in biological invasions. Global Ecol. Biogeogr. 17, 5–10. Google Scholar -
Purvis A. . 2008 Phylogenetic approaches to the study of extinction. Annu. Rev. Ecol. Evol. Syst. 39, 301–319. (doi:10.1146/annurev.ecolsys.063008.102010). Crossref, Web of Science, Google Scholar -
Reynolds J. D. . 2003 Life histories and extinction risk. Macroecology: concepts and consequences (eds, Blackburn T. M.& Gaston K. J. ), pp. 195–217. Cambridge, UK: Cambridge University Press. Google Scholar -
Root T. L., Price J. T., Hall K. R., Schneider S. H., Rosenzweig C.& Pounds J. A. . 2003 Fingerprints of global warming on wild animals and plants. Nature 421, 57–60. (doi:10.1038/nature01333). Crossref, PubMed, Web of Science, Google Scholar -
Sakai A. K., 2001 The population biology of invasive species. Annu. Rev. Ecol. Syst. 32, 305–332. (doi:10.1146/annurev.ecolsys.32.081501.114037). Crossref, Google Scholar -
Sheldon C. C., Rouse D. T., Finnegan E. J., Peacock W. J.& Dennis E. S. . 2000 The molecular basis of vernalization: the central role of. FLOWERING LOCUS C(FLC). Proc. Natl Acad. Sci. USA 97, 3753–3758. (doi:10.1073/pnas.060023597). Crossref, PubMed, Web of Science, Google Scholar -
Simberloff D. . 2000 Global climate change and introduced species in United States forests. Sci. Total Environ. 262, 253–261. (doi:10.1016/S0048-9697(00)00527-1). Crossref, PubMed, Web of Science, Google Scholar -
Sola A. J.& Ehrlen J. . 2007 Vegetative phenology constrains the onset of flowering in the perennial herb Lathyrus vernus. J. Ecol. 95, 208–216. (doi:10.1111/j.1365-2745.2006.01191.x). Crossref, Web of Science, Google Scholar -
Sparks T. H.& Carey P. D. . 1995 The responses of species to climate over two centuries: an analyses of the Marsham phenological record, 1736–1947. J. Ecol. 83, 321–329. Crossref, Web of Science, Google Scholar -
Sparks T. H., Jeffree E. P.& Jeffree C. E. . 2000 An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int. J. Biometeorol. 44, 82–87. (doi:10.1007/s004840000049). Crossref, PubMed, Web of Science, Google Scholar -
Stenseth N. C.& Mysterud A. . 2002 Climate, changing phenology, and other life history and traits: nonlinearity and match-mismatch to the environment. Proc. Natl Acad. Sci. USA 99, 13 379–13 381. (doi:10.1073/pnas.212519399). Crossref, Web of Science, Google Scholar -
Stenseth N. C., Mysterud A., Ottersen G., Hurrell J. W., Chan K. S.& Lima M. . 2002 Ecological effects of climate fluctuations. Science 297, 1292–1296. (doi:10.1126/science.1071281). Crossref, PubMed, Web of Science, Google Scholar -
Strauss S. Y., Webb C. O.& Salamin N. . 2006 Exotic taxa less related to native species are more invasive. Proc. Natl Acad. Sci. USA 103, 5841–5845. (doi:10.1073/pnas.0508073103). Crossref, PubMed, Web of Science, Google Scholar -
Tadege M., Sheldon C. C., Helliwell C. A., Stoutjesdijk P., Dennis E. S.& Peacock W. J. . 2001 Control of flowering time by FLC orthologues in Brassica napus. Plant J. 28, 545–553. (doi:10.1046/j.1365-313X.2001.01182.x). Crossref, PubMed, Web of Science, Google Scholar -
Thuiller W., Richardson D. M.& Midgley G. F. . 2007 Will climate change promote alien invasions? In Biological invasions (ed.& Nentwig W. ), pp. 197–211. Berlin, Germany: Springer. Google Scholar -
Vamosi S. M., Heard S. B., Vamosi J. C.& Webb C. O. . 2009 Emerging patterns in the comparative analysis of phylogenetic community structure. Mol. Ecol. 18, 572–592. (doi:10.1111/j.1365-294X.2008.04001.x). Crossref, PubMed, Web of Science, Google Scholar -
van Schaik C. P., Terborgh J. W.& Wright S. J. . 1993 The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu. Rev. Ecol. Syst. 24, 353–377. (doi:10.1146/annurev.es.24.110193.002033). Crossref, Google Scholar -
Vilá M., Corbin J. D., Dukes J. S., Pino J.& Smith S. D. . 2007 Linking plant invasions to global environmental change. Terrestrial ecosystems in a changing world (eds, Canadell J., Pataki D.& Pitelka L. ), pp. 93–102. New York, NY: Springer. Crossref, Google Scholar -
Visser M. E. . 2008 Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc. R. Soc. B 275, 649–659. (doi:10.1098/rspb.2007.0997). Link, Web of Science, Google Scholar -
Visser M. E.& Both C. . 2005 Shifts in phenology due to global climate change: the need for a yardstick. Proc. R. Soc. B 272, 2561–2569. (doi:10.1098/rspb.2005.3356). Link, Web of Science, Google Scholar -
Walther G. R. . 2003 Plants in a warmer world. Perspect. Plant Ecol. Evol. Syst. 6, 169–185. (doi:10.1078/1433-8319-00076). Crossref, Web of Science, Google Scholar -
Walther G. R., Post E., Convey P., Menzel A., Parmesan C., Beebee T. J. C., Fromentin J. M., Hoegh-Guldberg O.& Bairlein F. . 2002 Ecological responses to recent climate change. Nature 416, 389–395. (doi:10.1038/416389a). Crossref, PubMed, Web of Science, Google Scholar -
Webb C. O.& Donoghue M. J. . 2005 Phylomatic: tree assembly for applied phylogenetics. Mol. Ecol. Notes 5, 181–183. (doi:10.1111/j.1471-8286.2004.00829.x). Crossref, Google Scholar -
Webb C. O., Ackerly D. D., McPeek M. A.& Donoghue M. J. . 2002 Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505. (doi:10.1146/annurev.ecolsys.33.010802.150448). Crossref, Google Scholar -
Webb C. O., Ackerly D. D.& Kembel S. W. . 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Phylocom. v. 3.41. See http://www.phylodiversity.net/phylocom/. Google Scholar -
Wiens J. J.& Graham C. H. . 2005 Niche conservatism: integrating evolution, ecology, and conservation biology. Annu. Rev. Ecol. Evol. Syst. 36, 519–539. (doi:10.1146/annurev.ecolsys.36.102803.095431). Crossref, Web of Science, Google Scholar -
Wikström N., Savolainen V.& Chase M. W. . 2001 Evolution of the angiosperms: calibrating the family tree. Proc. R. Soc. Lond. B 268, 2211–2220. (doi:10.1098/rspb.2001.1782). Link, Web of Science, Google Scholar -
Willis C. G., Ruhfel B., Primack R. B., Miller-Rushing A. J.& Davis C. C. . 2008 Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17 029–17 033. (doi:10.1073/pnas.0806446105). Crossref, Web of Science, Google Scholar -
Willis C. G., Ruhfel B., Primack R. B., Miller-Rushing A. J.& Davis C. C. . 2009 Reply to McDonald et al.: climate change, not deer herbivory, has shaped species decline in Concord, Massachusetts. Proc. Natl Acad. Sci. USA 106, E29–E29. (doi:10.1073/pnas.0900170106). Crossref, Web of Science, Google Scholar -
Willis C. G., Ruhfel B. R., Primack R. B., Miller-Rushing A. J., Losos J. B.& Davis C. C. . 2010 Favourable climate change response explains non-native species' success in Thoreau's woods. PLoS ONE 5, e8878. (doi:10.1371/journal.pone.0008878). Crossref, PubMed, Web of Science, Google Scholar -
Wright S. J.& Calderon O. . 1995 Phylogenetic patterns among tropical flowering phenologies. J. Ecol. 83, 937–948. Crossref, Web of Science, Google Scholar -
Xu C.-Y., Griffin K. L.& Schuster W. S. F. . 2007 Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154, 11–21. (doi:10.1007/s00442-007-0807-y). Crossref, PubMed, Web of Science, Google Scholar