Studying global change through investigation of the plastic responses of xylem anatomy in tree rings

Research review

Studying global change throughinvestigation of the plastic responses ofxylem anatomy in tree rings

Author for correspondence:Patrick FontiTel: +41 44 739 22 85

Email: [email protected]

Received: 22 July 2009

Accepted: 17 August 2009

Patrick Fonti1, Georg von Arx2,3, Ignacio Garcıa-Gonzalez4, Britta

Eilmann5, Ute Sass-Klaassen6, Holger Gartner1 and Dieter Eckstein7

1WSL Swiss Federal Research Institute, Dendro Sciences Unit, Zurcherstr. 111, CH-8903 Birmens-

dorf, Switzerland; 2Laboratory of Tree-Ring Research, University of Arizona, 105 West Stadium,

Tucson, AZ 85721-0058, USA; 3School of Natural Resources, University of Arizona, Biological

Sciences East, Tucson, AZ 85721-0058, USA; 4Departamento de Botanica, Universidade de Santiago

de Compostela, Escola Politecnica Superior, Campus de Lugo, E-27002 Lugo, Spain; 5WSL Swiss

Federal Research Institute, Forest Dynamic Unit, Zurcherstr. 111, CH-8903 Birmensdorf,

Switzerland; 6Forest Ecology and Forest Management Group, Center for Ecosystem Studies,

Wageningen University, PO Box 47, 6700 AA Wageningen, The Netherlands; 7Department of Wood

Science, University of Hamburg, Leuschnerstr. 91, D-21031 Hamburg, Germany

New Phytologist (2010) 185: 42–53doi: 10.1111/j.1469-8137.2009.03030.x

Key words: cell chronologies,dendrochronology, efficiency versus safetytrade-off, tree-ring anatomy, woodanatomy, xylem hydraulic responses.

Summary

Variability in xylem anatomy is of interest to plant scientists because of the role

water transport plays in plant performance and survival. Insights into plant adjust-

ments to changing environmental conditions have mainly been obtained through

structural and functional comparative studies between taxa or within taxa on con-

trasting sites or along environmental gradients. Yet, a gap exists regarding the

study of hydraulic adjustments in response to environmental changes over the life-

times of plants. In trees, dated tree-ring series are often exploited to reconstruct

dynamics in ecological conditions, and recent work in which wood-anatomical

variables have been used in dendrochronology has produced promising results.

Environmental signals identified in water-conducting cells carry novel information

reflecting changes in regional conditions and are mostly related to short, sub-

annual intervals. Although the idea of investigating environmental signals through

wood anatomical time series goes back to the 1960s, it is only recently that low-

cost computerized image-analysis systems have enabled increased scientific output

in this field. We believe that the study of tree-ring anatomy is emerging as a prom-

ising approach in tree biology and climate change research, particularly if comple-

mented by physiological and ecological studies. This contribution presents the

rationale, the potential, and the methodological challenges of this innovative

approach.

Introduction

Long records of environmental conditions are essential forevaluating scenarios of climate change and the consequencesfor species and plant performance. As instrumental records

are not long enough to provide a complete picture ofdynamics in past climates, they need to be supplemented byproxy records. Trees, as long-living organisms, record eco-logically relevant information in their annual rings andhence represent important natural archives for the study of

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Journal compilation � New Phytologist (2009)

global changes throughout the last millennium (Esper et al.,2002; Cook et al., 2004; Treydte et al., 2006; Trouet et al.,2009). Tree-ring variables such as ring width or maximumlatewood density have been shown to be strongly influencedby environmental conditions, especially where temperatureor precipitation limits tree growth. They therefore play aprominent role in the study and reconstruction of climatevariation (IPCC, 2007, Jones et al., 2009).

There are, however, other less widely studied characteris-tics of wood, for example its anatomical structure, whichcan encode additional and novel ecological information.Variation in wood-anatomical characteristics representsadaptive structural solutions adopted by the tree in order toachieve an optimal balance among the competing needs ofsupport, storage and transport under changing environmen-tal conditions and phylogenetic constraints (Chave et al.,2009). Consequently, studies of variations in xylem anat-omy have already been an important source of informationin plant sciences (Larson, 1994; Gartner, 1995). Untilrecently, wood anatomists have advanced the understandingof phylogenetic adaptations in plants by analysing andinterpreting variation of wood structures across taxa and cli-matic zones (e.g. Carlquist, 1988; Wheeler & Baas, 1993;Wiemann et al., 1998). Intraspecific variation across cli-matic zones, along environmental gradients, or betweencontrasting sites supplied additional information about thelinkage between ecology (habitat) and functioning (derivedfrom xylem anatomy) (e.g. Carlquist, 1975; Baas, 1986;Villar-Salvador et al., 1997; Wheeler et al., 2007). There is,however, another source of variation, that is, the wood-ana-tomical variability along tree-ring sequences – which is thefocus of this review – which has been less widely studied bywood anatomists, and which we believe can be used to elu-cidate how individual trees and species respond to changingenvironmental conditions (Schweingruber, 1996, 2006).The ability of a genotype to adjust the phenotype over thelife of a tree is a result of short-term to long-term physiolog-ical responses to environmental variability and can be usedto link environment with xylem structure.

Tree-ring anatomy is a methodological approach basedon dendrochronology and quantitative wood anatomy toassess cell anatomical characteristics (such as conduit sizeand density, cell wall thickness and tissue percentage) alongseries of dated tree-rings and to analyse them through time(at the intra- and ⁄ or inter-annual level) in order to charac-terize the relationships between tree growth and variousenvironmental factors. This approach supplements tree-ringbased reconstructions of past environmental conditionswith novel understanding about the range and strategies ofspecies’ responses and their chances of success, and thuscontributes to the evaluation of the impact of predictedclimate change on future vegetation dynamics.

In this review, we stress the potential of including thedimension of time in analysing inter- and intra-annual

variation in wood structure, thereby mainly focussing onthe water-conducting tissue. In particular, we review den-drochronology-based wood anatomy to assess the state ofthe art in this emerging field and to encourage furtherresearch. We first outline the fundamentals behind the envi-ronmental information that can be obtained from thewood-anatomical characteristics of water-conducting cells(see ‘Water transport in trees and its constraints’, ‘Ecologi-cal relevance of xylem hydraulic architecture’ and ‘Environ-mental imprinting in wood cell anatomy’), then highlighthow methods applied in tree-ring anatomy can contributeto the extraction of environmental information (see ‘Princi-ples and challenges for decoding cell-based information’and ‘Time series of wood-anatomical variables and theirenvironmental signals’), and finally propose future lines ofresearch (see ‘Conclusion and perspectives’).

Water transport in trees and its constraints

Because of the importance of water in all physiologicalprocesses, its availability and the efficiency and safety of itstransport are often the factors most limiting plant growth(Tyree & Zimmerman, 2002; Lambers et al., 2008). Con-sidering that > 90% of the water taken up by plants is lostby transpiration through the leaf, while CO2 is absorbedat the same time, the importance of water becomes appar-ent (Kramer & Boyer, 1995). Consequently, to evolveinto tall and self-supporting land plants, trees had todevelop the ability to easily access and economically trans-port water and to regulate water loss through their leaves(Koch et al., 2004). Long-distance water transport in treesoccurs passively through the lumina of nonliving conduc-tive cells in the xylem (Carlquist, 1975) and is transferredbetween conduits through bordered pits, that is, throughopenings in the cell walls regulated by a pit membrane. Inconifers, water flows from tracheid to tracheid throughbordered pits. In angiosperm trees, water is transportedthrough longitudinally connected vessel elements thatform pipes up to several metres in length. Vessel elementsare longitudinally connected by dissolved end walls (perfo-ration plates) and adjacent vessels are laterally connectedby pits in the longitudinal cell walls to form a vesselnetwork.

The major force for water transport in the conductingxylem is generated by transpiration of water from the leaves,which creates a negative vapour pressure in the cells sur-rounding the stomata. This causes a negative hydrostaticpressure in the conducting cells that literally pulls the waterthrough the continuous network of conduits. As a result ofthe cohesive forces among water molecules, this suctionforce is transmitted downwards into the root system, wherewater is taken up via the root hairs along the fine roots (seethe cohesion-tension theory of the ascent of sap in vascularplants; Dixon & Joly, 1895; Tyree & Zimmerman, 2002).

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However, the need to supply water to the canopy at ahigh rate has to be balanced against mechanical stabilitywhile minimizing the risk of xylem dysfunction by cavita-tion (Hacke & Sperry, 2001; Sperry, 2003). This places animportant constraint on the architecture of stems and repre-sents an important trade-off in plant function (Baas et al.,2004).

At the conduit level, according to the Hagen–Poiseu-ille law, water conductivity approximately corresponds tothe fourth power of the conduit diameter. However,maximum gain in transport efficiency can only be real-ized if the end wall conductivity increases in concertwith diameter. On its way through the tracheid network,water travels not only through the lumina, but alsothrough the bordered pits connecting adjacent cells. Physio-logical studies have demonstrated that pit mem-branes are responsible for at least 50% of the hydraulicresistance in the xylem (Hacke et al., 2006). Changes inthe thickness and porosity of the pit membranes there-fore have the potential to exert significant influences onthe total hydraulic resistance in the plant. The longerand wider the conduit and the thinner and more porousthe pit membrane, the lower is its resistance to waterflow. Consequently, hydraulic conductivity can be consid-erably increased by slightly increasing the cross-sectional lumen area of the conduits and bordered pits,but increased conduit diameter greatly decreases the safetyof water transport against cavitations (Tyree & Zimmer-man, 2002). Cavitations are caused by nucleation formingair emboli in conduits that interrupt upwards water move-ment when the conduits come under high tension. Vulner-ability to cavitation is increased by greater conduit size(see reviews by Hacke & Sperry, 2001; Cochard, 2006)and by weak pit structures (Jansen et al., 2003). Drought-induced cavitations propagate by air seeding at intercon-duit pit membranes (Hacke & Sperry, 2001). Pit mor-phology may differ widely between tree species; thecorrelation between pit membrane size and conduit diame-ter in different taxa has been found to be weak, but differ-ences in pit structure and total area of pits per conduitseem to strongly influence embolism resistance (Wheeleret al., 2005; Hacke & Jansen, 2009). Within a singlestem, however, conduit diameter correlates withvulnerability to drought-induced cavitation, as wider con-duits have a greater surface area of pit membranes andtherefore a higher probability of having a large pit mem-brane pore (Gartner, 1995). By contrast, frost-inducedcavitations occur when xylem sap freezes and dissolvedgases create air bubbles in the wider conduits. Widerconduits trap larger bubbles in the ice, which are morelikely to trigger cavitation during thawing (e.g. Lemoineet al., 1999; Field & Brodribb, 2001). This risk appearsto be dependent also on the sugar content of the sap,the minimum temperature experienced, and the rate and

number of freeze–thaw cycles (Mayr et al., 2007). Insome cases it was observed that cavitations could beactively removed. This process of water refilling undernegative pressure is not fully understood, but appears toinvolve living cells and to require energy (Cochard et al.,2001; Holbrook et al., 2001; Salleo et al., 2004).

Ecological relevance of xylem hydraulicarchitecture

The characteristics of xylem hydraulic architecture, such asthe arrangement, frequency, length, diameter, wall thick-ness and pit characteristics of conduits, not only regulatethe efficiency of water transport but also affect the marginsof safety against hydraulic system failures (Comstock &Sperry, 2000; Hacke et al., 2001, 2006; Pittermann et al.,2006; Sperry et al., 2006; Choat et al., 2008). Inter- andintraspecific differences in xylem hydraulic architecturereflect not only size- or age-related trends but also differ-ences in the way trees adapt or adjust to environmental vari-ability, and can provide information about the plasticity ofa species under changing environmental conditions. A moredirect approach is to assess temporal plasticity in xylemhydraulic architecture in a tree-ring sequence of a singletree. As within the same tree and species resistance to cavita-tion is related to conduit diameter, the risk of system failureis higher in tree rings where a large amount of the totalhydraulic conductivity is contributed by a few wide con-duits. This holds especially true for ring-porous specieswhere water transport is assumed to take place in the outer-most tree ring only. Figure 1 shows an example of how therisk of a system failure can vary along the annual rings ofone individual. In this case, because of higher cavitation riskunder similar stress conditions, at least 50% loss of conduc-tivity are more likely to occur in years such as 1988 than as2002 (see Fig. 1).

The developmental success and the competitiveness oftrees depend on their ability to adjust and optimize theirhydraulic architecture to their specific environment. Majorhydraulically relevant properties, such as ring-porous or dif-fuse-porous xylem structure, leaf stomatal behaviour or thekind of root system, generally define the range of a species’tolerance and competitiveness and thus the ecological set-ting to which a species is adapted. However, the ecologicalamplitude and thus the species distribution within givenecological settings may be partly limited by the species’ plas-ticity in relevant traits in response to the environmental var-iability, not only in spatial terms, but also over the lifetimeof a tree (Sultan, 2000; Valladares et al., 2007). Movingoutside these ranges can have detrimental consequences forthe plant.

Comparative analyses of hydraulic traits of trees haveproved to be a valuable source of information for functionaland ecological wood anatomy. The majority of studies doc-

44 Review Research reviewNewPhytologist





umenting variation in xylem hydraulic structure in relationto changes in water availability were based on comparisonsalong different evolutionary developments (e.g. Sperry,2003; Rowe & Speck, 2005), among diverse groups of dis-tantly related taxa (e.g. Carlquist, 1975; Maherali et al.,2004), across ecotypes (e.g. Stout & Sala, 2003; Choatet al., 2007; Sobrado, 2007; De Micco et al., 2008), pheno-types (e.g. Poyatos et al., 2007; Beikircher & Mayr, 2008)or among diverse plant organs (e.g. Spicer & Gartner,1998; De Micco & Aronne, 2009).

However, a gap exists regarding the study of dynamichydraulic adjustments through the lifetimes of individualsor groups of trees. Coping with temporal environmentalvariability is the most critical challenge for the survival ofan individual tree. Because trees undergo a continuousprocess of ontogenetic adjustments to respond to stresssituations caused by a changing environment, andchanging size and age, valuable ecological information canbe extracted from the temporal reconstruction of theseresponses.

Environmental imprinting in wood cell anatomy

Meristems generate new functional structures during theentire life-span of an organism. Secondary growth of thewoody stem in particular is a dynamic process and is influ-enced in a complex way by whole-tree physiology, which inturn is controlled by environmental conditions. The effectof factors that strongly influence secondary growth arepermanently registered within the anatomical characteristicsand reflected in the tree-ring structure. During woodformation, xylem cells differentiate through a complexprocess encompassing cell-type determination, cell division,cell differentiation and programmed cell death (see reviewsin Fukuda, 1996; Plomion et al., 2001; Scarpella & Meijer,2004). These processes are genetically controlled and de-pend on the ontogenetic status of the tree, but are also influ-enced, directly and indirectly, by environmental conditions(Denne & Dodd, 1981).

On the one hand, an environmental event such as a frostcan directly influence cells undergoing differentiation and

Year

Con

duit

area

(µm

2 )

1960 1970 1980 1990 2000

0 20

000

60

000

10

0 00

0

50%

10%

1%

2002 Ring width = 2.2 mm

1988 Ring width = 2.3 mm

1988 2002

Vessel class SizeDark blue >95901 m2

Green 60801–95900 µm2

Light blue 5801–60800 µm2

Red 1000–5800 µm2

Vessel class Dark blue

Green Light blue

Red

Size>69201 m2

45001–69200 µm2

4001–4500 µm2

1000–4000 µm2

(a)

(b)

Fig. 1 Fluctuation of the threshold conduitarea defining the remaining hydraulicconductivity when all the widest vessels aredysfunctional as a result of cavitation (onetree of Quercus robur; 1956–2005).(a) Conduit area contributing to 50% (darkblue line), 10% (green line) and 1% (lightblue line) of the total conductivity. Therelative conductivity of each single conduitwas calculated according to theHagen–Poiseuille equation as the fourthpower of the radius. (b) Microsections of theannual rings between 1988 and 2002.Colouration of conduits shows their contri-butions to the overall conductivity: dark blue,50%; green, 40%; light blue, 9%; red, 1%.






thus leave an imprint of weakly lignified and crumpled con-duits inside a band of dead cell tissue in the tree ring(Glerum & Farrar, 1966). Analogously, spring conditionsoccurring at the time of early wood vessel formation deter-mine cell size by influencing the rate of cell division and dif-ferentiation, as observed for some ring-porous species(Garcıa-Gonzalez & Eckstein, 2003; Fonti & Garcıa-Gonzalez, 2004, 2008). In these cases, the susceptible per-iod of xylem formation to directly perceive and encodeenvironmental signals is the time window during whichcells are developing. As the periods of division, expansionand maturation of xylem cells range from several days toa few weeks (e.g. Rossi et al., 2006), concurrent weatherconditions are likely to directly leave imprints of theiroccurrence in the ring structure.

On the other hand, prevailing environmental conditionssuch as persistent drought periods can also indirectly induceadjustments in the wood structure through tree physiologi-cal modifications to adapt to the new environmentaldemands. Cambial activity and wood cell development arestrongly dependent on the availability of photoassimilates.In this case, the photosynthesis rate is reduced and assimi-late translocation is adjusted, which ultimately influencescambial activity and xylogenesis, even in subsequent sea-sons, as observed for Quercus pubescens and Pinus sylvestrisgrowing under contrasting water supplies (Eilmann et al.,2009). The resulting wood-anatomical modifications cangreatly differ depending on tree metabolism and species-specific wood structure, but also depending on the timingof the season when the environmental event occurs. Adrought event early in the growth season can inducedifferent wood-anatomical modifications from a droughtevent at the end of the summer, when trees might merelyrespond by ceasing wood formation early (Arend &Fromm, 2007).

Through the means of wood formation, trees are thusable to perceive directly and indirectly environmental chan-ges which leave permanent environmental imprints onxylem cells and wood structures, representing a valuablearchive for environmental scientists.

Principles and challenges for decodingcell-based information

Reconstruction of past environmental conditions using thevariability of datable tree-ring structures is an importantarea in dendrochronology. The study of the variation ofcell-anatomical characteristics across series of annual ringsstarted in the 1960s and 1970s (Knigge & Schulz, 1961;Eckstein et al., 1974) but has intensified in the last twodecades as a result of improvements in digital image analy-sis. Formerly, measurements were made visually on micro-scope slides, with attendant constraints in terms of theobjectivity of quantification and the sample size that could

be used. At present, if the cells are large enough, for exam-ple in the early wood vessels of ring-porous species, digitalimages can be directly captured from the wood surface,allowing a more efficient survey to be performed (e.g.Munro et al., 1996; Fonti et al., 2009a; Fig. 2). In thesecases, specific surface preparation techniques are required(e.g. Spiecker et al., 2000). In general, cutting is preferredto sanding as it keeps cell walls clean and cell luminaopen. Another necessity for these procedures is to obtain ahigh contrast between target objects and background. Thiscontrast can be enhanced by darkening the wood surfacewith ink or a stain and subsequently filling the cell luminawith a bright substance such as white chalk, plasticine orwax. Continuous progress in the development of imageanalysis systems involving powerful digital cameras, scan-ners and sophisticated software, as well as new techniquesfor wood surface preparation using specific microtomes(Gartner & Nievergelt, in press), suggests that in thefuture it will probably be possible to examine smaller cells,such as the vessels of diffuse-porous wood, tracheids, fibresand parenchyma cells, and even subcellular features suchas bordered pits.

The extraction of information from series of wood-anatomical characteristics of xylem cells has been basedon well-established dendrochronological principles, suchas the existence of similar environmentally drivenresponses in individuals growing under similar environ-mental conditions. This assumes the existence of commonvariability in the time series of different individuals (com-mon signal), caused by the influence of a given environ-mental factor (the signal). Moreover, the processes linkingcurrent environmental conditions with responses musthave been the same as those operating in the past (JamesHutton’s principle of uniformitarianism; BritannicaConcise Encyclopædia, 2009). In order to extract thisinformation, a widely accepted set of specific samplingprinciples (selection of sites, species and trees) and meth-odological procedures (definition of tree-ring variables,cross-dating, replication, standardization for noise reduc-tion and detrending of ageing trend) has been establishedfor which only variables such as ring width and maximumlatewood density were initially considered (Cook &Kairiukstis, 1990; Fritts, 2001).

The major differences between these traditional andwood-anatomical variables are the scale (moving from mmto lm), the larger number of observations for each ring,and the higher temporal (intra-annual) resolution of themeasurements of the wood-anatomical variables. Whilering-width-based dendrochronology usually extracts onevalue per ring, integrating radial growth throughout thegrowing season, measurements of wood-anatomical vari-ables yield much more data from different parts of thetree ring which are highly variable along both the radial(time) and tangential (spatial) positions within a tree






ring (see images in Fig. 1). From these data, meaningfulwood-anatomical variables (mean values, density values,and tissue proportions) have to be calculated for each treering to build annual time series. As a consequence of thechanging environmental conditions throughout the yearand especially during the growing period, radial files ofconsecutive cells produced at different times during the yearencode seasonal information. But even cells formed at thesame time must be measured in sufficient numbers toaccount for tangential variability in the xylem. If too fewcells are considered, or cells encoding different environmen-tal information at different times are mixed, the ecologicalinformation can be obscured or reduced. A higher timeresolution of the climate signal can often be achieved byusing features of subgroups of cells that are formed at thesame time (Garcıa-Gonzalez & Fonti, 2006). In these cases

the signal encoded can reflect climatic conditions thatprevail for short periods of from 1 to 2 months.

Studies on ring-porous early wood vessels have shownthat all vessels along a 12-mm-thick tangential band have tobe measured to stabilize the extractable environmentalsignal (Garcıa-Gonzalez & Fonti, 2008). Moreover, theenvironmental signal can be maximized, reduced, or evenabsent depending on the criteria applied to select differentvessel-area categories (Fig. 1) or vessel positions (e.g. earlywood vessels of the first row) within the rings.

In conifers, specific standardization procedures (normal-ized tracheidogram; Vaganov, 1990; or Gompertz function;Rossi et al., 2003) have been developed to transform theabsolute radial position of a radial row of consecutive trac-heids across a tree ring to a relative position, and thus allowa comparison among tree rings. In these cases, at least five

(a) (b1) (b2) (b3) (b4)

Fig. 2 Example of an automated early wood vessel measurement from a digital image. (a) Cut-out digital image of a Quercus robur corecross-section captured with a high-resolution and distortion-free digital scanner. The image was scanned at 256 greyscale with a resolution of1500 dpi. The core surface was sanded using 30 lM grit and cleaned with high-pressure water blasting to remove both tyloses and wooddust from the vessel lumina. In order to improve the contrast, the surrounding tissue was stained black with printer ink and lumina were filledwith white chalk powder. (b) Procedures for vessel recognition and measurement performed using an image analysis tool developed by theauthors (ROXAS; cf. Von Arx & Dietz, 2005) that combines the functionality of IMAGE PRO PLUS (v4.5; Media Cybernetics, Bethesda, MD, USA)with the authors’ own code for automated detection of vessels and tree-ring boundaries. During analysis, ROXAS locally improves and homoge-nizes image contrast which varies as a result of natural heterogeneity in wood surface quality. After additional edge enhancement, the image issegmented into a binary image using a fixed threshold value of intensity (b1). Clustered image objects are split and vessels (green objects) iden-tified based on area (‡ 1000 lm2) and morphometric characteristics (b2). Annual ring traces (yellow lines) are recognized based on the positionof the largest (early wood) vessels (in purple; b3). Misidentified ring boundaries and vessels are corrected using a manual editing mode avail-able in ROXAS. Finally, recognized vessels are assigned to the corresponding annual ring (alternatively coloured red and white; b4) anatomicalmeasurement of each single vessel is exported into a spreadsheet file (cf. Fonti et al., 2009a for further details).






radial files of tracheids have to be measured to obtain reli-able data on the variability of cell sizes across tree rings.Methods to monitor cambial dynamics, such as repeatedpinning (e.g. Dunisch et al., 2002; Seo et al., 2007) ormicro-coring (Deslauriers et al., 2003; Rossi et al., 2006;van der Werf et al., 2007), permit the determination of sea-sonal growth patterns that allow each cell in a radial file oftracheids to be assigned to the time of the season at which itwas formed.

Time series of wood-anatomical variables andtheir environmental signals

Specific environmental events affecting cambial activityleave wood-anatomical imprints inside the tree ring.Dendrochronology has often been used to reconstruct thespatio-temporal distribution of discontinuous events basedon these imprints (Gartner et al., 2002; Wimmer, 2002).Many studies have described these imprints in relation tothe effect of fire (e.g. Madany et al., 1982; Smith & Suther-land, 1999), defoliation (e.g. Huber, 1993; Asshoff et al.,1999; Esper et al., 2007), drought (e.g. Corcuera et al.,2004a,b; Liang & Eckstein, 2006; Eilmann et al., 2009),intensity and frequency of flooding events (e.g. St Georgeet al., 2002), geomorphic processes (e.g. St George &Nielsen, 2003; Gartner, 2007; den Ouden et al., 2007), orfrost (e.g. LaMarche & Hirschboeck, 1984).

Recent studies measuring wood-anatomical variablesacross series of rings have demonstrated that there is alsopotential to extract palaeo-ecological information from con-tinuous chronologies (Eckstein, 2004; Vaganov et al.,2006). These chronologies allow the application of statisti-cal models to relate wood-anatomical variables to continu-ous, highly resolved environmental variables, and throughthe use of transfer functions they can be used for reconstruc-tions before instrumental data. Most of the relatively fewstudies performed to date (Table 1) have examined the linkbetween different environmental signals and the area ofwater-conducting cells. Variability in wood-anatomical vari-ables was found to be mainly related to seasonal climate con-ditions, such as temperature or water availability, and thequality and strength of the signal varied with species, cli-matic zone, season of the year and the anatomical variableconsidered. In conifers, studies mainly focused on tracheidlumen size and cell wall thickness (Yasue et al., 2000; Wanget al., 2002; Kirdyanov et al., 2003; Panyushkina et al.,2003; Eilmann et al., 2006; Vaganov et al., 2006), whereasin angiosperms, particular attention was given to the earlywood vessels of ring-porous species such as Quercus spp.(Garcıa-Gonzalez & Eckstein, 2003; Eilmann et al., 2006;Tardif & Conciatori, 2006; Fonti & Garcıa-Gonzalez,2008), Castanea sativa (Fonti & Garcıa-Gonzalez, 2004;Fonti et al., 2007) and Tectona grandis (Pumijumnong &Park, 1999). Similar explorative analyses were also carried

out for the diffuse-porous species Fagus sylvatica (Sass &Eckstein, 1995) and Populus · euroamericana (Schumeet al., 2004).

Most of these studies have highlighted a close relationshipbetween wood-anatomical variables and seasonal climaticconditions. In some cases and for some specific variables ithas been demonstrated that the signal in wood-anatomicalvariables in comparison to traditional tree-ring variables(ring width or maximum late wood density) can provideeither higher temporal resolution (Panyushkina et al.,2003), different information (Garcıa-Gonzalez & Eckstein,2003; Fonti & Garcıa-Gonzalez, 2004), or applicability toother environments (Fonti & Garcıa-Gonzalez, 2008).However, we are convinced that screening for additionalmeaningful wood-anatomical variables in different species(sensu Fonti & Garcıa-Gonzalez, 2004; Tardif & Conciato-ri, 2006) and careful exploration of the signal in subselec-tions of contemporaneously formed cells (Garcıa-Gonzalez& Fonti, 2006; 2008) will further support promisingfindings presented in Table 1.

However, time series analysis with wood-anatomical vari-ables has primarily been used to explore the potential toobtain high-resolution proxies (1) by identifying whichenvironmental factor mainly influences wood-anatomicalvariability in a certain species and environmental setting,(2) by defining when in the season the signal is registered,and – to a lesser extent – (3) to determine the physiologicalmechanisms that cause the variability in wood anatomy.However, wood-anatomical variables have rarely beenapplied to infer functional adjustments of xylem hydraulicarchitecture to temporally changing conditions (e.g. Stercket al., 2008). Year-to-year analyses will permit the establish-ment of a link between climatic conditions and the anatom-ical characteristics of the forming wood. The attribution ofthese results to specific physiological responses and elucida-tion of the functional costs and benefits of the adjustment(see example in Fig. 1) would contribute to a better under-standing of the plasticity in xylem hydraulic architectureand the different strategies adopted by trees when they areexposed to changing environmental conditions.

Conclusion and perspectives

Tree-ring anatomy provides a valuable opportunity to add atime component to the study of plant responses to changingenvironments. As a consequence of the direct relationshipbetween cell structure (e.g. vessel area and vessel density) andfunction and their short period of formation, water-conduct-ing cells can record and permanently encode environmentalinformation with a high temporal resolution. With respectto traditional tree-ring variables, chronologies of wood-ana-tomical variables can thus provide novel information that isnot necessarily limited to trees growing under harsh condi-tions in marginal habitats. Decoding this information, which






Tab

le1

Ove

rvie

wof

pap

ers

usi

ng

chro

nolo

gie

sof

wood

cell

anat

om

ical

feat

ure

s

Pap

erSp

ecie

sA

nat

om

ical

feat

ure

sTim

eper

iod

and

regio

n

Envi

ronm

enta

lsig

nal

(P,pre

cipitat

ion;T,

tem

per

ature

)

Har

dw

ood

Ecks

tein

&Fr

isse

(1982)

Querc

us

robur,

Fagus

sylv

ati

caV

esse

lare

a1910–1

967

Ger

man

ySp

ring

Pan

dw

inte

rT

Woodco

ck(1

989)

Querc

us

macr

oca

rpa

Ves

seld

iam

eter

and

den

sity

1960–1

984

South

east

ern

Neb

rask

a,U

SAO

ctober

toJu

ne

P

Huber

(1993)

Querc

us

robur,

Querc

us

petr

eae

Early

wood

vess

elsi

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is strongly related to the characteristics and the position ofthe cells within the annual ring, requires specific methodo-logical approaches, including the survey of promising wood-anatomical variables, appropriate preparation techniques,and sophisticated statistical tools to build chronologies andto analyse the relation with environmental factors.

Although this multidisciplinary approach is still at anearly stage of development and in some cases involvestedious measuring work, it deserves to be further developedas it has the potential to provide new information in globalchange research. First, relevant relationships between thephysical environment and the physiological response oftrees can be recognized and analysed retrospectively, as thisinformation is permanently registered within the woodstructure. Secondly, the high time resolution of the environ-mental influence on wood anatomy can be valuable to iden-tify how and when growth processes are sensitive to theenvironment and therefore might contribute to disentan-gling the processes that control tree growth. This is impor-tant for understanding both physiological mechanisms andthe functional meaning of growth responses. This is crucialfor evaluating the range of plasticity and the capacity forresilience of trees growing under certain environmental con-ditions and ultimately to predict plant responses underfuture climatic scenarios.

For broader application of this approach in global changeresearch, a concerted effort involving diverse disciplines(functional ecology, wood anatomy, plant physiology anddendrochronology) is required to address some methodo-logical and conceptual issues. Methodologically, there is aneed for (1) accurate and efficient measuring along series ofrings to increase sample size, (2) expansion of the range ofpossible wood-anatomical variables to be measured (e.g. cellgrouping, pit structure and degree of lignification), (3)understanding of how physiological processes and ageingmodify wood formation, (4) improvement of the proce-dures to identify and enhance environmental signals in dif-ferent frequency domains, and (5) evaluation of thesynergistic effect of combining more tree-ring related prox-ies. In parallel there is a need for a better understanding ofthe processes that regulate the hydraulic responses acrossspecies, space and time and their functional meaning.

Acknowledgements

We thank three anonymous reviewers for valuable feedbackon and improvements to an earlier draft of this article.

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Studying global change through investigation of the plastic responses of xylem anatomy in tree rings

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