Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier.

In a temperate climate, understory trees leaf out earlier than canopy trees, but the cause of this discrepancy remains unclear. This study aims to investigate whether this discrepancy results from ontogenic changes or from microclimatic differences. Seedlings of five deciduous tree species were grown in spring 2012 in the understory and at canopy height using a 45-m-high construction crane built into a mature mixed forest in the foothills of the Swiss Jura Mountains. The leaf development of these seedlings, as well as conspecific adults, was compared, taking into account the corresponding microclimate. The date of leaf unfolding occurred 10-40 d earlier in seedlings grown at canopy level than in conspecific adults. Seedlings grown in the understory flushed c. 6 d later than those grown at canopy height, which can be attributed to the warmer temperatures recorded at canopy height (c. 1°C warmer). This study demonstrates that later leaf emergence of canopy trees compared with understory trees results from ontogenic changes and not from the vertical thermal profile that exists within forests. This study warns against the assumption that phenological data obtained in warming and photoperiod experiments on juvenile trees can be used for the prediction of forest response to climate warming.

[1]  Ivan A. Janssens,et al.  The Impact of Winter and Spring Temperatures on Temperate Tree Budburst Dates: Results from an Experimental Climate Manipulation , 2012, PloS one.

[2]  M. North,et al.  Canopy microclimate response to pattern and density of thinning in a Sierra Nevada forest , 2009 .

[3]  Andrew D. Richardson,et al.  Phenological Differences Between Understory and Overstory: A Case Study Using the Long-Term Harvard Forest Records , 2009 .

[4]  C. Augspurger.  Early spring leaf out enhances growth and survival of saplings in a temperate deciduous forest , 2008, Oecologia.

[5]  Jacques Roy,et al.  Changes in leaf phenology of three European oak species in response to experimental climate change. , 2010, The New phytologist.

[6]  W. Winner,et al.  Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. , 2002, Tree physiology.

[7]  C. Augspurger,et al.  Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. , 2003, Tree physiology.

[8]  Richard B Primack,et al.  Leaf-out phenology of temperate woody plants: from trees to ecosystems. , 2011, The New phytologist.

[9]  C. Jackson,et al.  The Climate near the Ground , 1966 .

[10]  A. Donnelly,et al.  Modelling the timing of Betula pubescens budburst. I. Temperature and photoperiod: a conceptual model , 2011 .

[11]  K. Seiwa,et al.  Changes in Leaf Phenology are Dependent on Tree Height inAcer mono, a Deciduous Broad-leaved Tree , 1999 .

[12]  Asko Noormets,et al.  Phenology of Ecosystem Processes , 2009 .

[13]  C. Körner,et al.  Web-FACE: a new canopy free-air CO2 enrichment system for tall trees in mature forests , 2002, Oecologia.

[14]  Sylvain Delzon,et al.  Quantifying phenological plasticity to temperature in two temperate tree species , 2010 .

[15]  S. Thomas.  Photosynthetic capacity peaks at intermediate size in temperate deciduous trees. , 2010, Tree physiology.

[16]  A. Escudero,et al.  Ontogenetic changes in leaf phenology of two co-occurring Mediterranean oaks differing in leaf life span , 2009, Ecological Research.

[17]  C. Augspurger.  Developmental versus environmental control of early leaf phenology in juvenile Ohio buckeye (Aesculus glabra) , 2004 .

[18]  M. Cannell.  Spring phenology of trees and frost avoidance * , 1997 .

[19]  R. Calamassi,et al.  Geographic variation and bud dormancy in beech seedlings (Fagus sylvatica L) , 1996 .

[20]  Christian Körner,et al.  Photoperiod sensitivity of bud burst in 14 temperate forest tree species , 2012 .

[21]  F. A. Bazzaz,et al.  Changes in drought response strategies with ontogeny in Quercus rubra: implications for scaling from seedlings to mature trees , 2000, Oecologia.

[22]  M. Day,et al.  Age- and size-related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. , 2002, Tree physiology.

[23]  Carl F. Salk,et al.  Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade , 2005 .

[24]  M. Tomita,et al.  Influence of canopy tree phenology on understorey populations of Fagus crenata , 2004 .

[25]  D. Goldblum,et al.  Sugar maple seedling carbon assimilation at the northern limit of its range: the importance of seasonal light , 2010 .

[26]  O. Keene,et al.  The log transformation is special. , 1995, Statistics in medicine.

[27]  David Basler,et al.  What role for photoperiod in the bud burst phenology of European beech , 2012, European Journal of Forest Research.

[28]  Maria E. Eriksson,et al.  The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. , 2012, Plant, cell & environment.

[29]  C. Körner,et al.  Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species , 2013, Oecologia.

[30]  Christian Körner,et al.  Phenology Under Global Warming , 2010, Science.

[31]  K. Yazaki,et al.  Ontogenetic transition of leaf physiology and anatomy from seedlings to mature trees of a rain forest pioneer tree, Macaranga gigantea. , 2005, Tree physiology.

[32]  Rebecca A Montgomery,et al.  Leaf phenology in relation to canopy closure in southern Appalachian trees. , 2008, American journal of botany.

[33]  Andrew D. Richardson,et al.  Phenological Differences Between Understory and Overstory , 2009 .

[34]  H. Hänninen,et al.  Dormancy release of Norway spruce under climatic warming: testing ecophysiological models of bud burst with a whole-tree chamber experiment. , 2007, Tree physiology.

[35]  Seiwa.  Ontogenetic changes in leaf phenology of Ulmus davidiana var. japonica, a deciduous broad-leaved tree. , 1999, Tree physiology.

[36]  Isabelle Chuine,et al.  Modelling the timing of Betula pubescens budburst. II. Integrating complex effects of photoperiod into process-based models , 2011 .

[37]  F. Herbert Bormann,et al.  Leaf phenology, photosynthesis, and the persistence of saplings and shrubs in a mature northern hardwood forest. , 1998, Tree physiology.

[38]  M. Cannell,et al.  Date of budburst of fifteen tree species in Britain following climatic warming , 1989 .

[39]  Constance A. Harrington,et al.  Modeling the effects of winter environment on dormancy release of Douglas-fir , 2010 .