Abstract
Changing global climate, particularly rising temperatures, has been linked through observations with advanced spring phenology in temperate regions. We experimentally tested if regional climate change predictions of increased temperature and precipitation alter the spring phenology of eastern US tree seedlings. This study reports the results of a 3-year-field experiment designed to study the responses of eastern deciduous tree species planted in a post-harvest environment to a 2 °C increase in temperature and a 20 % increase in precipitation. Species were monitored for timing of germination and leaf out in four treatment combinations (ambient, warmed, irrigated, and warmed + irrigated) on 16 plots located in a recently harvested central Pennsylvania forest. The 2 °C warming advanced day of seed germination by an average of 2 weeks and seedling leaf out by 10 days among all species (both p < 0.001). However, increased precipitation did not result in a significant change in spring phenology. Species responded uniquely to treatments, with germination advancing in three of five species in response to warming and leaf out advancing in six of six species. Southern species projected to expand northward into the study region with rising temperatures did not show responses to warming treatments that would provide them an advantage over current resident species. Timing of germination and leaf out varied among years of the experiment, most likely driven by year-to-year variability in spring temperatures. The climate change experiment highlighted the potential of a moderate 2 °C temperature increase to advance spring phenology of deciduous tree seedlings by up to 2 weeks, with a lack of a phenological response to a 20 % increase in precipitation.
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References
Alison FH, Lechowicz MJ (1992) Predicting the Timing of Budburst in Temperate Trees. J Appl Ecol 29:597–604
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jónsdóttir IS, Laine K, Lévesque E, Marion GM, Molau U, Mølgaard P, Nordenhäll U, Raszhivin V, Robinson CH, Starr G, Stenström A, Stenström M, Totland Ø, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511
Augspurger CK (2008) Early spring leaf out enhances growth and survival of saplings in a temperate deciduous forest. Oecologia 156:281–286
Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525
Augspurger C, Cheeseman JM, Salk CF (2005) Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct Ecol 19:537–546
Badeck F-W, Bondeau A, Böttcher K, Doktor D, Lucht W, Schaber J, Sitch S (2004) Responses of spring phenology to climate change. New Phytol 162:295–309
Burns RM, Honkala BH (1990) Silvics of North America: 1. Conifers; 2. Hardwoods. Agricultural Handbook 654, vol 2. US Dept of Ag For Serv, Washington, DC, p 877
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci 105:4495–4500
Chmielewski FM, Rötzer (2001) Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–112
Chuine I (2010) Why does phenology drive species distribution? Philos Trans R Soc B 365:3149–3160
Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510
Chuine I, Cour P, Rousseau DD (1999) Selecting models to predict the timing of flowering of temperate trees: implications for tree phenology modelling. Plant Cell Environ 22:1–13
Cleland E, Chuine I, Menzel A, Mooney H, Schwartz M (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365
Cramer W, Bondeau A, Woodward FI, Prentice IC, Betts RA, Brovkin V, Cox PM, Fisher V, Foley JA, Friend AD, Kucharik C, Lomas MR, Ramankutty N, Sitch S, Smith B, White A, Young-Molling C (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models. Glob Change Biol 7:357–373
Gill DS, Amthor JS, Bormann FH (1998) Leaf phenology, photosynthesis, and the persistence of saplings and shrubs in a mature northern hardwood forest. Tree Physiol 18:281–289
Gunderson CA, O’Hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Change Biol 16:2272–2286
Hakkinen R, Linkosalo T, Hari P (1998) Effects of dormancy and environmental factors on timing of bud burst in Betula pendula. Tree Physiol 18:707–712
Hänninen H (1991) Does climatic warming increase the risk of frost damage in northern trees? Plant Cell Environ 14:449–454
Heide OM (1993) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540
Heyhoe K, Wake CP, Huntington TG, Luo L, Schwartz MD, Sheffied J, Wood E, Anderson B, Bradbury J, DeGaetano A, Troy TJ, Wolfe D (2007) Past and future changes in climate and hydrological indicators in the US Northeast. Clim Dyn 28:381–407
Higgins SI, Clark JS, Nathan R, Hovestadt T, Schurr F, Fragoso JMV, Aguiar MR, Ribbens E, Lavorel S (2003) Forecasting plant migration rates: managing uncertainty for risk assessment. J Ecol 91:341–347
Hovenden MJ, Wills KE, Vander Schoor JK, Williams AL, Newton PCD (2008) Flowering phenology in a species-rich temperate grassland is sensitive to warming but not elevated CO2. New Phytol 178:815–822
Iverson LR, Prasad AM (1998) Predicting abundance of 80 tree species following climate change in the eastern United States. Ecol Monogr 68:465–485
Iverson LR, Schwartz MW, Prasad AM (2004) How fast and far might tree species migrate in the eastern United States due to climate change? Glob Ecol Biogeogr 13:209–219
Jackson ST, Betancourt JL, Booth RK, Gray ST (2010) Ecology and the rachet of events: climate variability, niche dimensions, and species distributions. PNAS 106:19685–19692
Kardol P, Campany CE, Souza L, Norby RJ, Weltzin JF, Classen AT (2010) Climate change effects on plant biomass alter dominance patterns and community evenness in an experimental old-field ecosystem. Glob Change Biol 16:2676–2687
Kimball BA (2005) Theory and performance of an infrared heater for ecosystem warming. Glob Change Biol 11:2041–2056
King JS, Kubiske ME, Pregitzer KS, Hendrey GR, McDonald EP, Giardina CP, Quinn VS, Karnosky DF (2005) Tropospheric O3 compromises net primary production in young stands of trembling aspen, paper birch and sugar maple in response to elevated atmospheric CO2. New Phytol 168:623–636
Kramer K (1994) A modelling analysis of the effects of climatic warming on the probability of spring frost damage to tree species in The Netherlands and Germany. Plant Cell Environ 17:367–377
Kwit MC, Rigg LS, Goldblum D (2010) Sugar maple seedling carbon assimilation at the northern limit of its range: the importance of seasonal light. Can J For Res 40:385–393
Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13:571–577
Leithead MD, Anand M, Silva LCR (2010) Northward migrating trees establish in treefall gaps at the northern limit of the temperature-boreal ecotone, Ontario, Canada. Oecologia 164:1095–1106
Linderholm H (2006) Growing season changes in the last century. Agric For Meteorol 137:1–14
Linkosalo T, Häkkinen R, Terhivuo J, Tuomenvirta H, Hari P (2009) The time series of flowering and leaf bud burst of boreal trees (1846–2005) support the direct temperature observations of climatic warming. Agric For Meteorol 149:453–461
McDaniel MD, Wagner RJ, Rollinson CR, Kimball BA, Kaye MW, Kaye JP (2013) Microclimate and ecological threshold responses in a warming and wetting experiment following whole-tree harvest. Theoret Appl Climatol. doi:10.1007/s00704-013-0942-9
McMaster G, Wilhelm W (1997) Growing degree-days: one equation, two interpretations. Agric For Meteorol 87:291–300
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissolli P, Braslavská OG, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, Remišvá V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F-E, Zach S, Zust ANA (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976
Milbau A, Graae BJ, Shevtsova A, Nijs I (2009) Effects of a warmer climate on seed germination in the subarctic. Ann Bot 104:287–296
Morin X, Lechowicz MJ, Augspurger CK, O’Keefe J, Viner D, Chuine I (2009) Leaf phenology in 22 North American tree species during the 21st century. Glob Change Biol 15:961–975
Myking T, Heide OM (1995) Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiol 15:697–704
Neilson RP, Pitelka LF, Solomon AM, Nathan RAN, Midgley GF, Fragoso JMV, Lischke H, Thompson KEN (2005) Forecasting regional to global plant migration in response to climate change. Bioscience 55:749–759
Oliver CD, Larson BC (1996) Forest stand dynamics. McGraw-Hill, Inc, New York
Ollinger SV, Goodale CL, Hayhoe K, Jenkins JP (2007) Potential effects of climate change and rising CO2 on ecosystem processes in northeastern U.S. forests. Mitig Adapt Strat Glob Change 13:467–485
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Pearson RG (2006) Climate change and the migration capacity of species. Trends Ecol Evol 21:111–113
Peñuelas J, Gordon C, Llorens L, Nielsen T, Tietema A, Beier C, Bruna P, Emmett B, Estiarte M, Gorissen A (2004) Nonintrusive field experiments show different plant responses to warming and drought among sites, seasons, and species in a north–south European gradient. Ecosystems 7:598–612
Polgar CA, Primack RB (2011) Leaf-out phenology of temperature woody plants: from trees to ecosystems. New Phytol 191:926–941
Polgar CA, Primack RB, Dukes JS, Schaaf C, Wang Z, Hoeppner SS (2013) Tree leaf out response to temperature: comparing field observations, remote sensing, and a warming experiment. Int J Biometeorol. doi:10.1007/s00484-013-0718-z
Post ES, Pedersen C, Wilmers CC, Forchhammer MC (2008) Phenological sequences reveal aggregate life history response to climatic warming. Ecology 89:363–370
Prasad AM, Iverson LR, Matthews S, Peters M (2007–ongoing) A climate change atlas for 134 forest tree species of the eastern United States [database]. http://www.nrs.fs.fed.us/atlas/tree. Northern Research Station, USDA Forest Service, Delaware, OH
Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S, Migiliavacca 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 365:3227–3246
Rollinson CR, Kaye MW (2012) Experimental warming alters spring phenology of certain plant functional groups in an early successional forest community. Glob Change Biol 18:1108–1116
Rollinson CR, Kaye MW, Leites LP (2012) Community assembly and plant cover responses to experimental warming and increased precipitation of an early successional forest. Ecosphere 3:122. doi:10.1890/ES12-00321.1
Royo AA, Carson WP (2006) On the formation of dense understory layers in forests worldwide: consequences and implications for forest dynamics, biodiversity, and succession. Can J For Res 36:1345–1362
Schwartz M (1998) Green-wave phenology. Nature 394:839–840
Swanson ME, Franklin JF, Beschta RL et al (2010) The forgotten stage of forest succession: early-successional ecosystems on forest sites. Front Ecol Environ 9:117–125
Thuiller W, Albert C et al (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspect Plant Ecol Evol Syst 9:137–152
Walker MD, Walker DA, Welker JM, Arft AM, Bardsley T, Brooks PD, Fahnestock JT, Jones MH, Losleben M, Parsons AN, Seastedt TR, Turner PL (1999) Long-term experimental manipulation of winter snow regime and summer temperature in arctic and alpine tundra. Hydrol Process 13:2315–2330
Walther G-R, Berger S et al (2005) An ecological ‘footprint’ of climate change. Proc R Soc B 272:1427–1432
Wan S, Lou Y, Wallace L (2002) Changes in microclimate induced by experimental warming and clipping in a tallgrass prairie. Glob Change Biol 8:754–768
Zhou L, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res 106:20069–20083
Acknowledgments
J. P. Kaye, M. Abrams, and B. A. Kimball contributed to the development of this project and the experimental design. M. D.McDaniel, C. Rollinson, B. Frasier, and C. Hone assisted in data collection at the research site. Two anonymous reviewers provided helpful comments on the manuscript. This research was funded by the Northeastern Region of the U.S. Department of Energy’s National Institute of Climate Change Research and the College of Agricultural Sciences, The Pennsylvania State University.
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Communicated by Lesley Rigg.
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Kaye, M.W., Wagner, R.J. Eastern deciduous tree seedlings advance spring phenology in response to experimental warming, but not wetting, treatments. Plant Ecol 215, 543–554 (2014). https://doi.org/10.1007/s11258-014-0322-2
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DOI: https://doi.org/10.1007/s11258-014-0322-2