International Journal of Biometeorology

, Volume 58, Issue 4, pp 579–589 | Cite as

Phenology research for natural resource management in the United States

  • Carolyn A. F. EnquistEmail author
  • Jherime L. Kellermann
  • Katharine L. Gerst
  • Abraham J. Miller-Rushing
Phenology – Milwaukee 2012


Natural resource professionals in the United States recognize that climate-induced changes in phenology can substantially affect resource management. This is reflected in national climate change response plans recently released by major resource agencies. However, managers on-the-ground are often unclear about how to use phenological information to inform their management practices. Until recently, this was at least partially due to the lack of broad-based, standardized phenology data collection across taxa and geographic regions. Such efforts are now underway, albeit in very early stages. Nonetheless, a major hurdle still exists: phenology-linked climate change research has focused more on describing broad ecological changes rather than making direct connections to local to regional management concerns. To help researchers better design relevant research for use in conservation and management decision-making processes, we describe phenology-related research topics that facilitate “actionable” science. Examples include research on evolution and phenotypic plasticity related to vulnerability, the demographic consequences of trophic mismatch, the role of invasive species, and building robust ecological forecast models. Such efforts will increase phenology literacy among on-the-ground resource managers and provide information relevant for short- and long-term decision-making, particularly as related to climate response planning and implementing climate-informed monitoring in the context of adaptive management. In sum, we argue that phenological information is a crucial component of the resource management toolbox that facilitates identification and evaluation of strategies that will reduce the vulnerability of natural systems to climate change. Management-savvy researchers can play an important role in reaching this goal.


Climate change Species interactions Forecasting Vulnerability assessment Phenology literacy 



We thank Jake Weltzin, David Inouye, Alyssa Rosemartin, David Moore, and two anonymous reviewers for insightful comments on an earlier version of this manuscript. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of their respective funding agencies and organizations.


  1. Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980CrossRefGoogle Scholar
  2. Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302CrossRefGoogle Scholar
  3. Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc B-Biological Sci 279:3843–3852CrossRefGoogle Scholar
  4. Ault TR, Henebry GM, de Beurs KM, Schwartz MD, Betancourt JL, Moore D (2013) Lessons from the false spring of 2012, earliest on record in North America. EOS, Trans Am Geophys Union 94:181–182CrossRefGoogle Scholar
  5. Austen DJ (2011) Landscape Conservation Cooperatives: a science-based network in support of conservation. The Wildlife Professional, Fall, 2011Google Scholar
  6. Aono Y, Kazui K (2008) Phenological data series of cherry tree flowering in Kyoto, Japan, and its application to reconstruction of springtime temperatures since the 9th century. Int J Climatol 28:905–914CrossRefGoogle Scholar
  7. Bagne KE, Friggens MM, Finch DM (2011). A system for assessing vulnerability of species (SAVS) to climate change. US Department of Agriculture, Forest Service, Rocky Mountain Research StationGoogle Scholar
  8. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377CrossRefGoogle Scholar
  9. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83CrossRefGoogle Scholar
  10. Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83CrossRefGoogle Scholar
  11. Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Wisconsin. Proc Natl Acad Sci U S A 96:9701–9704CrossRefGoogle Scholar
  12. Carpenter SR, Bennett EM, Peterson GD (2006) Scenarios for ecosystem services: an overview. Ecol Soc 11(1):29Google Scholar
  13. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Yeong Ryu H, Sbeglia GC, Spagnolo F, Waldron JB, Warsi O, Wiens JJ (2012) How does climate change cause extinction? Proceedings of the Royal Society B: Biological Sciences 280 online early doi:  10.1098/rspb.2012.1890.
  14. Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026CrossRefGoogle Scholar
  15. Chuine I, Yiou P, Viovy N, Seguin B, Daux V, Ladurie EL (2004) Grape ripening as a past climate indicator. Nature 432:289–290CrossRefGoogle Scholar
  16. Chuine I (2010) Why does phenology drive species distribution? Phil Trans R Soc B-Biolog Sci 365:3149–3160CrossRefGoogle Scholar
  17. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol, Evol 22:357–365CrossRefGoogle Scholar
  18. Cleland EE, Allen JM, Crimmins TM, Dunne JA, Pau S, Travers S, Zavaleta ES, Wolkovich EM (2012) Phenological tracking enables positive species responses to climate change. Ecology 93:1765–1771CrossRefGoogle Scholar
  19. Cook BI, Terando A, Steiner A (2010) Ecological forecasting under climatic data uncertainty: a case study in phenological modeling. Environ Res Lett 5:044014. doi: 10.1088/1748-9326/5/4/044014 CrossRefGoogle Scholar
  20. Denny EG, Gerst KL, Miller-Rushing AJ, Tierney GL, Crimmins TM, Enquist CAF, Guertin P, Rosemartin AH, Schwartz MD, Thomas KA, Weltzin JF (2013) Standardized phenology monitoring methods to track plants and animal activity for science and resource management applications. Int J Biometeorol. (in press) Google Scholar
  21. Diez JM, Ibáñez I, Miller-Rushing AJ, Mazer SJ, Crimmins TM, Crimmins MA, Bertelsen, CD, Inouye DW (2012) Forecasting phenology: from species variability to community patterns. Ecol lett 15:545–553Google Scholar
  22. Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817CrossRefGoogle Scholar
  23. Durant JM, Hjermann DO, Anker-Nilssen T, Beaugrand G, Mysterud A, Pettorelli N, Stenseth NC (2005) Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol Lett 8:952–958CrossRefGoogle Scholar
  24. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefGoogle Scholar
  25. Ellwood ER, Temple SA, Primack RB, Bradley NL, Davis CC (2013) Record-breaking early flowering in the eastern United States. PloS ONE 8:e53788CrossRefGoogle Scholar
  26. Enquist CAF, Miller-Rushing AJ (2011) Standards and tools for using phenology in science, management, and education. Park Sci 28(2):70Google Scholar
  27. Enquist CAF, Rosemartin A, Schwartz MD (2012) Identifying and prioritizing phenological data products and tools. Eos, Transactions American Geophysical Union 93 (37):356.Google Scholar
  28. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–U105CrossRefGoogle Scholar
  29. Ghersa CM, Holt JS (1995) Using phenology prediction in weed management: a review. Weed Res 35:461–470CrossRefGoogle Scholar
  30. Glick P, Stein BA, Edelson NA (eds) (2011) Scanning the conservation horizon: a guide to climate change vulnerability assessment. National Wildlife Federation, Washington, DC, USAGoogle Scholar
  31. Gu L, Hanson PJ, Mac Post W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freezes: increased cold damage in a warming world? Bioscience 58:253–262CrossRefGoogle Scholar
  32. Haggerty BP, Matthews ER, Gerst KL, Evenden AG, Mazer SJ (2013) The California Phenology Project: tracking plant responses to climate change. Madroño 60:1–3CrossRefGoogle Scholar
  33. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Ecology—climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162CrossRefGoogle Scholar
  34. Hegland SJ, Nielsen A, Lazaro A, Bjerknes A-L, Totland O (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195CrossRefGoogle Scholar
  35. Herms DA (2004) Using degree-days and plant phenology to predict pest activity. In: V. Krischik and J. Davidson, Eds. IPM (Integrated Pest Management) of Midwest Landscapes, pp. 49–59. Minnesota Experiment Station Publication SB-07645, 316 pp.Google Scholar
  36. Holzkamper A, Calanca P, Fuhrer J (2013) Identifying climatic limitations to grain maize yield potentials using a suitability evaluation approach. Agric Forest Meteorol 168:149–159CrossRefGoogle Scholar
  37. Ibáñez I, Primack RB, Miller-Rushing AJ, Ellwood E, Higuchi H, Lee SD, Kobori H, Silander JA (2010) Forecasting phenology under global warming. Philos Trans R Soc, B 365:3247–3260CrossRefGoogle Scholar
  38. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362CrossRefGoogle Scholar
  39. IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri, R.K and Reisinger, A.(eds.)]. IPCC, Geneva, Switzerland, 104 pp.Google Scholar
  40. Jolly WM, Nemani R, Running SW (2005) A generalized, bioclimatic index to predict foliar phenology in response to climate. Glob Chang Biol 11(4):619–632CrossRefGoogle Scholar
  41. Jones BK, Bogen H, Verrecken H, Weltzin JF (2010) Design and importance of multi-tiered ecological monitoring networks. In: Müller F, Baessler C, Schubert H, Klotz S (eds) Long-term ecological research. Springer Science + Business Media B.V, New York, pp 355–374CrossRefGoogle Scholar
  42. Knudsen E, Lindén A, Both C, Jonzén N, Pulido F, Saino N, Sutherland WJ, Bach LA, Coppack T, Ergon T, Gienapp P, Gill JA, Gordo O, Hedenström A, Lehikoinen E, Marra PP, Møller AP, Nilsson ALK, Péron G, Ranta E, Rubolini D, Sparks TH, Spina F, Studds CE, Sæther SA, Tryjanowski P, Stenseth NC (2011) Challenging claims in the study of migratory birds and climate change. Biol Rev 86:928–946CrossRefGoogle Scholar
  43. Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston TA, Steffan-Dewenter I, Vazquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A-M, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314CrossRefGoogle Scholar
  44. Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119:561–601CrossRefGoogle Scholar
  45. Lavalle C, Micale F, Houston TD, Camia A, Hiederer R, Lazar C, Conte C, Amatulli G, Genovese G (2009) Climate change in Europe. 3. Impact on agriculture and forestry. A review (Reprinted). Agron Sustain Dev 29:433–446CrossRefGoogle Scholar
  46. Lawler JJ, Tear TH, Pyke C, Shaw MR, Gonzalez P, Kareiva P, Pearsall S (2010) Resource management in a changing and uncertain climate. Front Ecol Environ 8(1):35–43CrossRefGoogle Scholar
  47. Levin DA (2006) Flowering phenology in relation to adaptive radiation. Syst Bot 31:239–246CrossRefGoogle Scholar
  48. Lovett GM, Burns DA, Driscoll CT, Jenkins JC, Mitchell MJ, Rustad L, Shanley JB, Likens GE, Haeuber R (2007) Who needs environmental monitoring? Front Ecol Environ 5:253–260CrossRefGoogle Scholar
  49. Marino GP, Kaiser DP, Gu L, Ricciuto DM (2011) Reconstruction of false spring occurrences over the southeastern United States, 1901–2007: an increasing risk of spring freeze damage? Environ Res Lett 6:024015. doi: 10.1088/1748-9326/6/2/024015 CrossRefGoogle Scholar
  50. McKinney AM, Goodell K (2011) Plant–pollinator interactions between an invasive and native plant vary between sites with different flowering phenology. Plant Ecol 212:1025–1035CrossRefGoogle Scholar
  51. McKinney AM, CaraDonna PJ, Inouye DW, Barr B, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources. Ecology 93:1987–1993CrossRefGoogle Scholar
  52. Melaas EK, Friedl MA, Zhu Z (2013) Detecting interannual variation in deciduous broadleaf forest phenology using Landsat TM/ETM + data. Remote Sens Environ 132:176–185CrossRefGoogle Scholar
  53. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecol Lett 10:710–717CrossRefGoogle Scholar
  54. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kuebler K, Bissolli P, Braslavska OG, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F-E, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976CrossRefGoogle Scholar
  55. Miller-Rushing AJ, Primack RB, Primack D, Mukunda S (2006) Photographs and herbarium specimens as tools to document phenological changes in response to global warming. Am J Bot 93:1667–1674CrossRefGoogle Scholar
  56. Miller-Rushing AJ, Hoye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Phil Trans R Soc B-Biological Sci 365:3177–3186CrossRefGoogle Scholar
  57. Miller-Rushing AJ, Evenden A, Gross J, Mitchell B, Sachs S (2011) Parks use phenology to improve management and communicate climate change. Park Sci 28:61–67Google Scholar
  58. Milly PCD, Julio B, Malin F, Robert MH, Zbigniew WK, Dennis PL, Ronald JS (2008) Stationarity is dead. Science 319:573–574CrossRefGoogle Scholar
  59. Møller AP, 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 U S A 105:16195–16200CrossRefGoogle Scholar
  60. Morecroft MD, Bealey CE, Beaumont DA, Benham S, Brooks DR, Burt TP, Critchley CNR, Dick J, Littlewood NA, Monteith DT, Scott WA, Smith RI, Walmsey C, Watson H (2009) The UK Environmental Change Network: emerging trends in the composition of plant and animal communities and the physical environment. Biol Conserv 142:2814–2832CrossRefGoogle Scholar
  61. Morin X, Augspurger C, Chuine I (2007) Process-based modeling of species’ distributions: what limits temperate tree species’ range boundaries? Ecology 88:2280–2291CrossRefGoogle Scholar
  62. Morisette JT, Richardson AD, Knapp AK, Fisher JI, Graham EA, Abatzoglou J, Wilson BE, Breshears DD, Henebry GM, Hanes JM, Liang L (2009) Tracking the rhythm of the seasons in the face of global change: phenological research in the 21st century. Front Ecol Environ 7(5):253–260CrossRefGoogle Scholar
  63. National Ecological Observatory Network (NEON) (2011) Science strategy: enabling continental-scale ecological forecasting, pp. 55Google Scholar
  64. Nichols JD, Williams BK (2006) Monitoring for conservation. Trends Ecol, Evol 21:668–673CrossRefGoogle Scholar
  65. Nolan VP, Weltzin JF (2011) Phenology for science, resource management, decision making, and education. Eos, Transactions American Geophysical Union 92 (2):15.Google Scholar
  66. Ollerton J, Lack AJ (1992) Flowering phenology: an example of relaxation of natural selection? Trends Ecol Evol 7:274–276CrossRefGoogle Scholar
  67. Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466(7305):482–485Google Scholar
  68. Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583CrossRefGoogle Scholar
  69. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefGoogle Scholar
  70. 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 Biology 17:3633–3643CrossRefGoogle Scholar
  71. Pereira HM, Ferrier S, Walters M, Geller GN, Jongman RHG, Scholes RJ, Bruford MW, Brummitt N, Butchart SHM, Cardoso AC, Coops NC, Dulloo E, Faith DP, Freyhof J, Gregory RD, Heip C, Höft R, Hurtt G, Jetz W, Karp DS, McGeoch MA, Obura D, Onoda Y, Pettorelli N, Reyers B, Sayre R, Scharlemann JPW, Stuart SN, Turak E, Walpole M, Wegmann M (2013) Essential biodiversity variables. Science 339(6117):277–278CrossRefGoogle Scholar
  72. Perlut NG, Strong AM, Alexander TJ (2011) A model for integrating wildlife science and agri‐environmental policy in the conservation of declining species. J Wildl Manag 75(7):1657–1663CrossRefGoogle Scholar
  73. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefGoogle Scholar
  74. Peterson GD, Cumming GS, Carpenter SR (2003) Scenario planning: a tool for conservation in an uncertain world. Conserv Biol 17(2):358–366CrossRefGoogle Scholar
  75. Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Phil Trans R SocB-Biol Sci 363(1501):2369–2375Google Scholar
  76. Primack RB (1980) Variation in the phenology of natural populations of montane shrubs in New Zealand. J Ecol 68:849–862CrossRefGoogle Scholar
  77. Primack RB, Miller-Rushing AJ (2012) Uncovering, collecting, and analyzing records to investigate the ecological impacts of climate change: a template from Thoreau’s Concord. Bioscience 62:170–181CrossRefGoogle Scholar
  78. Pulido F (2007) Phenotypic changes in spring arrival: evolution, phenotypic plasticity, effects of weather and condition. Clim Res 35:5–23CrossRefGoogle Scholar
  79. Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S, Migliavacca M, Montagnani L, Munger JW, Moors E, Piao S, Rebmann C, Reichstein M, Saigusa N, Tomelleri E, Vargas R, Varlagin A (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos Trans R Soc, B 365:3227–3246CrossRefGoogle Scholar
  80. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefGoogle Scholar
  81. Rosemartin AH, Crimmins TM, Enquist CAF, Gerst KL, Kellermann JL, Posthumus EE, Denny EG, Guertin P, Marsh LM, Weltzin JW (2013) Organizing phenological data resources to inform natural resource conservation. Biological Conservation doi: 10.1016/j.biocon.2013.07.003
  82. Ruckman EM, Schwinning S, Lyons KG (2012) Effects of phenology at burn time on post-fire recovery in an invasive C-4 grass. Restor Ecol 20:756–763CrossRefGoogle Scholar
  83. Schwartz MD, Ault TR, Betancourt JL (2012a) Spring onset variations and trends in the continental United States: past and regional assessment using temperature-based indices. Int J Climatol. doi: 10.1002/joc.3400 Google Scholar
  84. Schwartz MD, Betancourt JL, Weltzin JF (2012b) From Caprio’s lilacs to the USA National Phenology Network. Front Ecol Environ 10(6):324–327CrossRefGoogle Scholar
  85. Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos Trans R Soc, B 365:3161–3176CrossRefGoogle Scholar
  86. Souriau A, Yiou P (2001) Grape harvest dates for checking NAO paleoreconstructions. Geophys Res Lett 28:3895–3898CrossRefGoogle Scholar
  87. Sparks TH, Carey PD (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. J Ecol 83:321–329CrossRefGoogle Scholar
  88. Thuiller W (2007) Biodiversity—climate change and the ecologist. Nature 448:550–552CrossRefGoogle Scholar
  89. USDA Forest Service (USFS) (2009) Forest Service Global Change Research Strategy, 2009–2019. Accessed 29 November 2012.
  90. US Environmental Protection Agency (EPA) (2012) Climate Change Indicators in the United States. Accessed 29 November 2012.
  91. US Fish and Wildlife Service (USFWS) (2010) Rising to the Urgent Challenge: Strategic Plan for Responding to Accelerating Climate Change. September 2010. Accessed 29 November 2012.
  92. US National Park Service (NPS) (2010) National Park Service Climate Change Response Strategy. September 2010. Fort Collins, Colorado. Accessed 29 November 2012.
  93. Van Buskirk J, Mulvihill RS, Leberman RC (2012) Phenotypic plasticity alone cannot explain climate-induced change in avian migration timing. Ecol Evol 2:2430–2437CrossRefGoogle Scholar
  94. Ventrella D, Charfeddine M, Moriondo M, Rinaldi M, Bindi M (2012) Agronomic adaptation strategies under climate change for winter durum wheat and tomato in southern Italy: irrigation and nitrogen fertilization. Reg Environ Chang 12:407–419CrossRefGoogle Scholar
  95. Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B 272:2561–2569CrossRefGoogle Scholar
  96. Walters CJ (1986) Adaptive management of renewable resources. McMillan, New YorkGoogle Scholar
  97. Walther GR (2010) Community and ecosystem responses to recent climate change. Phil Trans R Soc B-Biological Sci 365:2019–2024CrossRefGoogle Scholar
  98. White MA, Beurs D, Kirsten M, Didan K, Inouye DW, Richardson AD, Lauenroth WK (2009) Intercomparison, interpretation, and assessment of spring phenology in North America estimated from remote sensing for 1982–2006. Glob Chang Biol 15(10):2335–2359CrossRefGoogle Scholar
  99. Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6(12):e325CrossRefGoogle Scholar
  100. Williams BK, Brown ED (2012) Adaptive Management: The U.S. Department of the Interior Applications Guide. Adaptive Management Working Group, U.S. Department of the Interior, Washington, DC.Google Scholar
  101. 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 U S A 105:17029–17033CrossRefGoogle Scholar
  102. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Losos JB, Davis CC (2010) Favorable climate change response explains non-native species’ success in Thoreau’s woods. PloS ONE 5:e8878CrossRefGoogle Scholar
  103. Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Glob Chang Biol 10:1844–1856CrossRefGoogle Scholar
  104. Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology. Front Ecol Environ 9:287–294CrossRefGoogle Scholar
  105. Wolkovich EM, Davies TJ, Schaefer H, Cleland EE, Cook BI, Travers SE, Willis CG, Davis CC (2013) Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change. Am J Bot 100:1407–1421. doi: 10.3732/ajb.1200478 CrossRefGoogle Scholar
  106. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10CrossRefGoogle Scholar
  107. Young B, Byers E, Gravuer K, Hammerson G, Redder A (2010) Guidelines for using the NatureServe Climate Change Vulnerability Index. NatureServe, ArlingtonGoogle Scholar

Copyright information

© ISB 2014

Authors and Affiliations

  • Carolyn A. F. Enquist
    • 1
    • 2
    • 3
    Email author
  • Jherime L. Kellermann
    • 1
    • 3
    • 5
  • Katharine L. Gerst
    • 1
    • 3
  • Abraham J. Miller-Rushing
    • 4
  1. 1.National Coordinating OfficeUSA National Phenology NetworkTucsonUSA
  2. 2.The Wildlife SocietyBethesdaUSA
  3. 3.School of Natural Resources and the EnvironmentUniversity of ArizonaTucsonUSA
  4. 4.Schoodic Education and Research Center and Acadia National ParkNational Park ServiceWinter HarborUSA
  5. 5.Natural Sciences DepartmentOregon Institute of Technology and Science and Learning CenterKlamath FallsUSA

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