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Beyond tree-ring widths: stable isotopes sharpen the focus on climate responses of temperate forest trees

Beyond tree-ring widths: stable isotopes sharpen the focus on climate responses of temperate forest trees
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  © The Author 2015. Published by Oxford University Press. All rights reserved. For Permissions, please email: Tree Physiology 35, 1–3doi:10.1093/treephys/tpu115 Beyond tree-ring widths: stable isotopes sharpen the focus on climate responses of temperate forest trees Lucas A. Cernusak 1,3  and Nathan B. English 2 1 College of Marine and Environmental Sciences, James Cook University, Queensland, Australia; 2 College of Science, Technology and Engineering, James Cook University, Queensland, Australia; 3 Corresponding author ( Received November 8, 2014; accepted December 4, 2014; handling Editor Danielle Way Tree rings provide an indispensable tool for assessing a tree's response to variability in its environment, oftentimes also pro-viding a means of reconstructing that variability beyond instru-mental records. The wood that trees produce is laid down sequentially, creating an archive of temporally ordered material that is rich in physiological and environmental information. This is made all the more useful because trees are globally distrib-uted, can live for thousands of years and in some cases remain intact long after they die. Tree-ring archives are used in a wide variety of studies, including, but not limited to, climate recon-structions (Cook et al. 2010), archaeological dating of ruins (C ˇ ufar 2007 ), reconstructions of re history and recurrence intervals (Swetnam et al. 1999), and assessments of tree physiological responses to drought (McDowell et al. 2010). The number of applications for tree rings has grown steadily in recent decades, and the variety of measurements that can be made on tree rings has grown as well (Speer 2010). The simplest measurement that can be made is in-series whole-ring widths. From this starting point, additional information can be gained from measuring early-wood and late-wood widths, wood density, elemental abundances, microbril angles, radial diameters of xylem conduits and stable-isotope ratios of the organic material in tree rings. A tree-ring record based on a single sample from a tree is referred to as a series, whereas a composite of many series is referred to as a chronology.To be useful, a measured tree-ring record must be both date-able and responsive. Being dateable means the rings must be shown to represent specic years at annual increments, with as few missing or false rings as possible. Being responsive means the rings or their characteristics must yield signicant variations in response to physiological or climatic drivers, and these variations must be strong enough to stand out from the background noise. Tree-ring series can be described as ‘sensi-tive’ or ‘complacent’, depending on whether or not the mea-sured parameter is responsive to the physiological or climatic drivers of interest (Stokes and Smiley 1968). Recent work has progressed towards more accurately dating tree rings (Hua 2009), including dating rings with non-annual increments (Loader et al. 2011), and in a new paper published in this issue, Hartl-Meier et al. (2015)  have expanded the denition of  just what constitutes a sensitive tree-ring series and the type of forest in which one can expect to nd such a series. As the science of dendrochronology advanced from the early 20th century, it became evident that there were geo-graphic sweet spots for developing ring-width chronologies. The trick is to sample trees that are growing away from their optimal climatic conditions. Individuals that are growing near the edge of the species' geographical range, either horizon-tally or elevationally, are more likely to be sensitive to a limit-ing environmental factor, for example, rainfall or temperature (Figure 1). At the same time, however, the target trees must not be so far towards the edge of the species' range that miss-ing rings resulting from multiple poor growth years prevent the development of an accurate and reliable chronology (Figure 1). This sampling paradigm mostly restricts ring-width based chro-nologies to the inward portion of the periphery of most large temperate forests. With careful site selection, or by substitut-ing elevation for horizontal distance, many interior forests can be used to develop useful chronologies. This includes stable-isotope series (e.g., Marshall and Monserud 1996, Duquesnay  et al. 1998, Tognetti et al. 2014), but these have seldom been recognized as useful from a climate reconstruction perspective. Commentary   a  t   J   a m e  s  C  o ok  Uni   v e r  s i   t   y on J   a n u a r  y2  9  ,2  0 1  5 h  t   t   p :  /   /   t  r  e  e  ph  y s  . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om   Tree Physiology Volume 35, 2015 In general, regions or sites within the optimal growth habitat of a species will just not yield ring-width chronologies that are both dateable and sensitive. Stable-isotope studies have tended to follow the inner periphery sampling paradigm in sub-polar, temperate and semi-arid forests (e.g., Breshears et al. 2009, Loader et al. 2013 a , Heres et al. 2014), due to accessi-bility of existing samples and sites, and to a continued empha-sis on picking sites on the basis that they are the most likely to harbour climate-sensitive ring-width chronologies, in addition to, one hopes, stable-isotope chronologies.Hartl-Meier et al. (2015) constructed tree-ring chronologies for ring widths and for the stable-isotope ratios of carbon and oxygen for three mid-latitude tree species: Norway spruce, European larch and beech. Stable-isotope ratios of carbon and oxygen have previously been measured in tree rings and are a commonly applied tool in dendrochronology (McCarroll and Loader 2004). The real novelty in the Hartl-Meier et al. (2015)  analysis lies not so much in what they did, but rather in where they did it. The climatic conditions at their study site in the Austrian pre-Alps are characterized by relatively high annual precipitation (1370 mm year − 1 ) and by relatively optimal grow-ing conditions for the three focal tree species. Three different topographic positions were sampled at the site, with European larch not present on the driest, south-exposed position. The plateau position, in particular, had deep soils and productiv-ity high enough that it was judged appropriate for establish-ment of a plantation early in the 20th century. Thus, this does not represent the periphery of the geographical range of these three tree species; rather, it is more characteristic of the inte-rior of the climatic space over which these temperate forest trees are distributed.Based purely on the ring-width chronologies, one would indeed be forced to agree that the site is not ideal, as the ring widths were only weakly correlated with climatic indices, and there was little coherence among species in ring-width responses to climate. Unlike the ring widths, however, stable-isotope ratios in tree-ring cellulose showed a strong coherence among species and strong correlations with climatic indices, including growing season cloud cover, temperature and mois-ture. These strong correlations were maintained across the positions within the site, from the dry, south-facing slope to the productive plateau. These results of Hartl-Meier et al. (2015) suggest that there is a strong potential for developing stable-isotope based tree-ring chronologies throughout the geo-graphical ranges of temperate tree species, rather than just on the periphery of their distributions. Recent results also suggest that the same may be true for tree-ring chronologies based on tracheid radial diameter and microbril angle ( Allen et al. 2013, Drew et al. 2013). The ability to sample a single spe- cies of tree, or multiple species of different functional types, across the full range of their geographical distributions could provide a signicant advantage for understanding species-level responses to climate change.In addition to providing a tool for climate reconstructions based on tree-ring chronologies, stable isotopes also provide insights into the physiological responses of trees to extreme climate events. For example, Hartl-Meier et al. (2015) con-ducted a superposed epoch analysis (SEA) on the responses of the three tree species to drought events that occurred in 1983, 1992, 1994 and 2003. The SEA technique creates a composite response by overlaying multiple events, thereby allowing a signal to emerge from noise associated with other drivers that work on similar time scales. By applying SEA, Hartl-Meier et al. (2015) resolved intriguing differences among their three study species on how they responded to drought. Norway spruce, which has been shown to employ an isohy-dric strategy with respect to its stomatal regulation (McDowell et al. 2008), suffered the largest growth reductions during and following drought. This species also had the highest δ 18 O in its wood, consistent with having shallower roots and not having access to deep soil moisture; and it also had the highest δ 13 C 2  Cernusak and English Figure 1. A schematic of ring-width (RW) and stable-isotope ( δ  ) char-acteristics in tree-ring series across the climatic range of a hypotheti-cal forest. The top panel shows mean ring widths (black), correlations (red) of ring width and isotope series among trees and with climate, the variability (dark blue) of the ring width and isotope series as mea-sured by mean sensitivity and standard deviation, the percentage of absent or partial rings (grey), and the dominance of the canopy (green). The bottom diagram illustrates where ring-width and stable-isotope-based chronologies are best able to act as proxies for climatic or physiological variability. Figure modied from Fritts (1976).   a  t   J   a m e  s  C  o ok  Uni   v e r  s i   t   y on J   a n u a r  y2  9  ,2  0 1  5 h  t   t   p :  /   /   t  r  e  e  ph  y s  . oxf   or  d  j   o ur n a l   s  . or  g /  D o wnl   o a  d  e  d f  r  om   Tree Physiology Online at in its wood, consistent with a greater stomatal limitation on photosynthesis than in European larch or beech.We do not mean to suggest that there is not real value in obtaining ring-width chronologies; the ring widths are, after all, a whole-tree integration of the tree's growth response. And developing isotopic chronologies is not without its drawbacks, requiring a great deal more money, effort and equipment than ring-width chronologies (Gaudinski et al. 2005), and recent work suggests that greater sample numbers are required than have been used in past studies (Loader et al. 2013 b ). However, it is clear that much complementary information can be gained by analysing stable-isotope ratios, and other wood properties, in addition to ring widths. Hartl-Meier et al. (2015) have demonstrated this nicely. The combination of ring width and stable-isotope analyses appears especially well suited to providing information on how forest tree species are likely to respond to climate stress (Allen et al. 2010). This information could be of critical importance as we seek to manage forest ecosystems in the current era of rapid global climate change. Conict of interest None declared. Funding L.A.C. was supported by an Australian Research Council Future Fellowship (FT100100329). N.B.E. was supported by an Australian Research Council Discovery Early Career Research Award (DE130100295). References Allen CD, Macalady AK, Chenchouni H et al. (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684.Allen KJ, Drew DM, Downes GM, Evans R, Cook ER, Battaglia M, Baker PJ (2013) A strong regional temperature signal in low-elevation Huon pine. J Quat Sci 28:433–438.Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT (2009) Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ 7: 185–189.Cook ER, Anchukaitis KJ, Buckley BM, D'Arrigo RD, Jacoby GC, Wright WE (2010) Asian monsoon failure and megadrought during the last millennium. Science 328:486–489.C ˇ ufar K (2007) Dendrochronology and past human activity. A review of advances since 2000. Tree Ring Res 63:47–60.Drew DM, Allen K, Downes GM, Evans R, Battaglia M, Baker P (2013) Wood properties in a long-lived conifer reveal strong climate signals where ring-width series do not. Tree Physiol 33:37–47.Duquesnay A, Bréda N, Stievenard M, Dupouey JL (1998) Changes of tree-ring δ 13 C and water-use efciency of beech ( Fagus sylvatica  L.) in north-eastern France during the past century. Plant Cell Environ 21:565–572.Fritts HC (1976) Tree rings and climate. The Blackburn Press, NJ, USA. 367 p.Gaudinski JB, Dawson TE, Quideau S, Schuur EAG, Roden JS, Trumbore SE, Sandquist DR, Oh SW, Wasylishen RE (2005) Comparative analysis of cellulose preparation techniques for use with 13 C, 14 C, and 18 O isotopic measurements. Anal Chem 77:7212–7224.Hartl-Meier C, Zang C, Büntgen U, Esper J, Rothe A, Göttlein A, Dirnböck T, Treydte K (2015) Uniform climate sensitivity in tree-ring stable isotopes across species and sites in a mid-latitude temperate forest. 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