Abstract
In plant ecophysiology, functional leaf traits are generally not assessed in relation to phenological phase of the canopy. Leaf traits measured in deciduous perennial species are known to vary between spring and summer seasons, but there is a knowledge gap relating to the late-summer phase marked by growth cessation and bud set occurring well before fall leaf senescence. The effects of phenology on canopy physiology were tested using a common garden of over 2,000 black cottonwood (Populus trichocarpa) individuals originating from a wide geographical range (44–60ºN). Annual phenological events and 12 leaf-based functional trait measurements were collected spanning the entire summer season prior to, and following, bud set. Patterns of seasonal trait change emerged by synchronizing trees using their date of bud set. In particular, photosynthetic, mass, and N-based traits increased substantially following bud set. Most traits were significantly different between pre-bud set and post-bud set phase trees, with many traits showing at least 25 % alteration in mean value. Post-bud set, both the significance and direction of trait–trait relationships could be modified, with many relating directly to changes in leaf mass. In Populus, these dynamics in leaf traits throughout the summer season reflected a shift in whole plant physiology, but occurred long before the onset of leaf senescence. The marked shifts in measured trait values following bud set underscores the necessity to include phenology in trait-based ecological studies or large-scale phenotyping efforts, both at the local level and larger geographical scale.
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References
Ackerly DD (2004) Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. Am Nat 163:654–671
Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and relative importance of intra- vs. interspecific variability in plant traits. Funct Ecol 24:1192–1201
Ceulemans R, Isebrands JG (1996) Carbon acquisition and allocation. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, National Research Council of Canada, Ottawa, pp 355–399
Chen B, Chen JM (2007) Diurnal, seasonal and interannual variability of carbon isotope discrimination at the canopy level in response to environmental factors in a boreal forest ecosystem. Plant Cell Environ 30:1223–1239
Chuine I, Cour P (1999) Climatic determinants of budburst seasonality in four temperate-zone tree species. New Phytol 143:339–349
Cornelissen HC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380
Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126
Delagrange S (2011) Light- and seasonal-induced plasticity in leaf morphology, N partitioning and photosynthetic capacity of two temperate deciduous species. Environ Exp Bot 70:1–10
Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304
Farmer RE Jr (1994) The genecology of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, National Research Council of Canada, Ottawa, pp 33–55
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
Gornall JL, Guy RD (2007) Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa). Can J Bot 85:1202–1213
Grassi G, Vicinelli E, Ponti F, Cantoni L, Magnani F (2005) Seasonal and interannual variability of photosynthetic capacity in relation to leaf nitrogen in a deciduous forest plantation in northern Italy. Tree Physiol 25:349–360
Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. J Veg Sci 17:255–260
Herbst M, Rosier PT, Morecroft MD, Gowing DJ (2008) Comparative measurements of transpiration and canopy conductance in two mixed deciduous woodlands differing in structure and species composition. Tree Physiol 28:959–970
Ingvarsson PK, Garcia MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2 a candidate gene for day-length-induced growth cessation and bud set across a latitudinal gradient in European aspen (Populus tremula). Genetics 172:1845–1853
Kalcsits L, Silim S, Tanino K (2009) Warm temperature accelerates short photoperiod induced growth cessation and dormancy induction in hybrid poplar (Populus × spp.). Trees 23:971–979
Keir KR, Bemmels JB, Aitken SN (2011) Low genetic diversity moderate local adaptation and phylogeographic insights in Cornus nuttallii (Cornaceae). Am J Bot 98:1327–1336
Keller SR, Soolanayakanahally RY, Guy RD, Silim SN, Olson MS, Tiffin P (2011) Climate-driven local adaptation of ecophysiology and phenology in balsam poplar Populus balsamifera L. (Salicaceae). Am J Bot 98:99–108
Kuptz D, Fleischmann F, Matyssek R, Grams TEE (2011) Seasonal patterns of carbon allocation to respiratory pools in 60-yr-old deciduous (Fagus sylvatica) and evergreen (Picea abies) trees assessed via whole-tree stable carbon isotope labeling. New Phytol 191:160–172
Luquez V, Hall D, Albrechtsen BR, Karlsson J, Ingvarsson P, Jansson P (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet Genomes 4:279–292
Ma S, Baldocchi DD, Mambelli S, Dawson TE (2011) Are temporal variations of leaf traits responsible for seasonal and inter-annual variability in ecosystem CO2 exchange? Funct Ecol 25:258–270
Maseyk KS, Lin T, Rotenberg E, Grünzweig JM, Schwartz A, Yakir D (2008) Physiology-phenology interactions in a productive semi-arid pine forest. New Phytol 178:603–616
Morecroft MD, Roberts JM (1999) Photosynthesis and stomatal conductance of mature canopy oak (Quercus robur) and sycamore (Acer pseudoplatanus) trees throughout the growing season. Funct Ecol 13:332–342
Pau S, Wolkovich EM, Cook BJ, Davies TJ, Kraft NJB, Bolmgren K, Betancourt JL, Cleland EE (2011) Predicting phenology by integrating ecology evolution and climate science. Glob Change Biol 17:3633–3643
Polgar CA, Primack RB (2011) Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191:926–941
Reich PB (1995) Phenology of tropical forests: patterns causes and consequences. Can J Bot 73:164–174
Rohde A, Storme V, Jorge V, Gaudet M, Vitacolonna N, Fabbrini F, Ruttink T, Zaina G, Marron N, Dillen S, Steenackers M, Sabatti M, Morgante M, Boerjan W, Bastien C (2011) Bud set in poplar—genetic dissection of a complex trait in natural and hybrid populations. New Phytol 189:106–121
Sang Y, Chuankuan W, Huo H (2011) Inter-specific and seasonal variations in photosynthetic capacity and water use efficiency of five temperate tree species in Northeastern China. Scand J For Res 26:21–29
Shipley B, Lechowicz MJ, Wright I, Reich PB (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–541
Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera). Plant Cell Environ 32:1821–1832
Soolanayakanahally RY, Guy RD, Silim SN, Song M (2012) Timing of photoperiodic competency causes phenological mismatch in balsam poplar (Populus balsamifera L.). Plant Cell Environ. doi:10.1111/j.1365-3040.2012.02560.x
Stokes VJ, Morecroft MD, Morison JIL (2010) Comparison of leaf water use efficiency of oak and sycamore in the canopy over two growing seasons. Trees 24:297–306
Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892
Wilson KB, Baldocchi DD, Hanson PJ (2001) Leaf age affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant Cell Environ 24:571–583
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of the global leaf trait relationships. New Phytol 166:485–496
Xie C-Y, Ying CC, Yanchuk AD, Holowachuk DL (2009) Ecotypic model of regional differentiation caused by restricted gene migration: a case in black cottonwood (Populus trichocarpa) along the Pacific Northwest coast. Can J For Res 39:519–525
Acknowledgments
The authors are thankful for assistance from L. Muenter, E. Moreno, L. Liao, and for helpful discussion from L. Kalcsits and R. Soolanayakanahally. This work was supported by Applied Genomics Innovation Program of Genome BC and NSERC Discovery grant to R. D. G.
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Communicated by Todd Dawson.
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McKown, A.D., Guy, R.D., Azam, M.S. et al. Seasonality and phenology alter functional leaf traits. Oecologia 172, 653–665 (2013). https://doi.org/10.1007/s00442-012-2531-5
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DOI: https://doi.org/10.1007/s00442-012-2531-5