New
Phytologist
Review
Research review
Studying global change through
investigation of the plastic responses of
xylem anatomy in tree rings
Author for correspondence:
Patrick Fonti
Tel: +41 44 739 22 85
Email: [email protected]
Patrick Fonti1, Georg von Arx2,3, Ignacio Garcı́a-González4, Britta
Eilmann5, Ute Sass-Klaassen6, Holger Gärtner1 and Dieter Eckstein7
Received: 22 July 2009
Accepted: 17 August 2009
dorf, Switzerland; 2Laboratory of Tree-Ring Research, University of Arizona, 105 West Stadium,
1
WSL Swiss Federal Research Institute, Dendro Sciences Unit, Zürcherstr. 111, CH-8903 Birmens-
Tucson, AZ 85721-0058, USA; 3School of Natural Resources, University of Arizona, Biological
Sciences East, Tucson, AZ 85721-0058, USA; 4Departamento de Botánica, Universidade de Santiago
de Compostela, Escola Politécnica Superior, Campus de Lugo, E-27002 Lugo, Spain; 5WSL Swiss
Federal Research Institute, Forest Dynamic Unit, Zürcherstr. 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
Summary
New Phytologist (2010) 185: 42–53
doi: 10.1111/j.1469-8137.2009.03030.x
Key words: cell chronologies,
dendrochronology, efficiency versus safety
trade-off, tree-ring anatomy, wood
anatomy, xylem hydraulic responses.
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 adjustments to changing environmental conditions have mainly been obtained through
structural and functional comparative studies between taxa or within taxa on contrasting sites or along environmental gradients. Yet, a gap exists regarding the
study of hydraulic adjustments in response to environmental changes over the lifetimes 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, subannual intervals. Although the idea of investigating environmental signals through
wood anatomical time series goes back to the 1960s, it is only recently that lowcost 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 promising approach in tree biology and climate change research, particularly if complemented 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 for
evaluating scenarios of climate change and the consequences
for species and plant performance. As instrumental records
42 New Phytologist (2010) 185: 42–53
www.newphytologist.org
are not long enough to provide a complete picture of
dynamics in past climates, they need to be supplemented by
proxy records. Trees, as long-living organisms, record ecologically relevant information in their annual rings and
hence represent important natural archives for the study of
The Authors (2009)
Journal compilation New Phytologist (2009)
New
Phytologist
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 maximum
latewood density have been shown to be strongly influenced
by environmental conditions, especially where temperature
or precipitation limits tree growth. They therefore play a
prominent role in the study and reconstruction of climate
variation (IPCC, 2007, Jones et al., 2009).
There are, however, other less widely studied characteristics of wood, for example its anatomical structure, which
can encode additional and novel ecological information.
Variation in wood-anatomical characteristics represents
adaptive structural solutions adopted by the tree in order to
achieve an optimal balance among the competing needs of
support, storage and transport under changing environmental conditions and phylogenetic constraints (Chave et al.,
2009). Consequently, studies of variations in xylem anatomy have already been an important source of information
in plant sciences (Larson, 1994; Gartner, 1995). Until
recently, wood anatomists have advanced the understanding
of phylogenetic adaptations in plants by analysing and
interpreting variation of wood structures across taxa and climatic zones (e.g. Carlquist, 1988; Wheeler & Baas, 1993;
Wiemann et al., 1998). Intraspecific variation across climatic zones, along environmental gradients, or between
contrasting sites supplied additional information about the
linkage between ecology (habitat) and functioning (derived
from 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-anatomical variability along tree-ring sequences – which is the
focus of this review – which has been less widely studied by
wood anatomists, and which we believe can be used to elucidate how individual trees and species respond to changing
environmental conditions (Schweingruber, 1996, 2006).
The ability of a genotype to adjust the phenotype over the
life of a tree is a result of short-term to long-term physiological responses to environmental variability and can be used
to link environment with xylem structure.
Tree-ring anatomy is a methodological approach based
on dendrochronology and quantitative wood anatomy to
assess cell anatomical characteristics (such as conduit size
and density, cell wall thickness and tissue percentage) along
series of dated tree-rings and to analyse them through time
(at the intra- and ⁄ or inter-annual level) in order to characterize the relationships between tree growth and various
environmental factors. This approach supplements tree-ring
based reconstructions of past environmental conditions
with novel understanding about the range and strategies of
species’ responses and their chances of success, and thus
contributes to the evaluation of the impact of predicted
climate change on future vegetation dynamics.
In this review, we stress the potential of including the
dimension of time in analysing inter- and intra-annual
The Authors (2009)
Journal compilation New Phytologist (2009)
Research review
Review
variation in wood structure, thereby mainly focussing on
the water-conducting tissue. In particular, we review dendrochronology-based wood anatomy to assess the state of
the art in this emerging field and to encourage further
research. We first outline the fundamentals behind the environmental information that can be obtained from the
wood-anatomical characteristics of water-conducting cells
(see ‘Water transport in trees and its constraints’, ‘Ecological relevance of xylem hydraulic architecture’ and ‘Environmental imprinting in wood cell anatomy’), then highlight
how methods applied in tree-ring anatomy can contribute
to the extraction of environmental information (see ‘Principles and challenges for decoding cell-based information’
and ‘Time series of wood-anatomical variables and their
environmental signals’), and finally propose future lines of
research (see ‘Conclusion and perspectives’).
Water transport in trees and its constraints
Because of the importance of water in all physiological
processes, its availability and the efficiency and safety of its
transport are often the factors most limiting plant growth
(Tyree & Zimmerman, 2002; Lambers et al., 2008). Considering that > 90% of the water taken up by plants is lost
by transpiration through the leaf, while CO2 is absorbed
at the same time, the importance of water becomes apparent (Kramer & Boyer, 1995). Consequently, to evolve
into tall and self-supporting land plants, trees had to
develop the ability to easily access and economically transport water and to regulate water loss through their leaves
(Koch et al., 2004). Long-distance water transport in trees
occurs passively through the lumina of nonliving conductive cells in the xylem (Carlquist, 1975) and is transferred
between conduits through bordered pits, that is, through
openings in the cell walls regulated by a pit membrane. In
conifers, water flows from tracheid to tracheid through
bordered pits. In angiosperm trees, water is transported
through longitudinally connected vessel elements that
form pipes up to several metres in length. Vessel elements
are longitudinally connected by dissolved end walls (perforation plates) and adjacent vessels are laterally connected
by pits in the longitudinal cell walls to form a vessel
network.
The major force for water transport in the conducting
xylem is generated by transpiration of water from the leaves,
which creates a negative vapour pressure in the cells surrounding the stomata. This causes a negative hydrostatic
pressure in the conducting cells that literally pulls the water
through the continuous network of conduits. As a result of
the cohesive forces among water molecules, this suction
force is transmitted downwards into the root system, where
water is taken up via the root hairs along the fine roots (see
the cohesion-tension theory of the ascent of sap in vascular
plants; Dixon & Joly, 1895; Tyree & Zimmerman, 2002).
New Phytologist (2010) 185: 42–53
www.newphytologist.org
43
44
Review
Research review
However, the need to supply water to the canopy at a
high rate has to be balanced against mechanical stability
while minimizing the risk of xylem dysfunction by cavitation (Hacke & Sperry, 2001; Sperry, 2003). This places an
important constraint on the architecture of stems and represents an important trade-off in plant function (Baas et al.,
2004).
At the conduit level, according to the Hagen–Poiseuille law, water conductivity approximately corresponds to
the fourth power of the conduit diameter. However,
maximum gain in transport efficiency can only be realized if the end wall conductivity increases in concert
with diameter. On its way through the tracheid network,
water travels not only through the lumina, but also
through the bordered pits connecting adjacent cells. Physiological studies have demonstrated that pit membranes are responsible for at least 50% of the hydraulic
resistance in the xylem (Hacke et al., 2006). Changes in
the thickness and porosity of the pit membranes therefore have the potential to exert significant influences on
the total hydraulic resistance in the plant. The longer
and wider the conduit and the thinner and more porous
the pit membrane, the lower is its resistance to water
flow. Consequently, hydraulic conductivity can be considerably increased by slightly increasing the crosssectional lumen area of the conduits and bordered pits,
but increased conduit diameter greatly decreases the safety
of water transport against cavitations (Tyree & Zimmerman, 2002). Cavitations are caused by nucleation forming
air emboli in conduits that interrupt upwards water movement when the conduits come under high tension. Vulnerability 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). Droughtinduced cavitations propagate by air seeding at interconduit pit membranes (Hacke & Sperry, 2001). Pit morphology may differ widely between tree species; the
correlation between pit membrane size and conduit diameter in different taxa has been found to be weak, but differences in pit structure and total area of pits per conduit
seem to strongly influence embolism resistance (Wheeler
et al., 2005; Hacke & Jansen, 2009). Within a single
stem, however, conduit diameter correlates with
vulnerability to drought-induced cavitation, as wider conduits have a greater surface area of pit membranes and
therefore a higher probability of having a large pit membrane pore (Gartner, 1995). By contrast, frost-induced
cavitations occur when xylem sap freezes and dissolved
gases create air bubbles in the wider conduits. Wider
conduits trap larger bubbles in the ice, which are more
likely to trigger cavitation during thawing (e.g. Lemoine
et al., 1999; Field & Brodribb, 2001). This risk appears
to be dependent also on the sugar content of the sap,
the minimum temperature experienced, and the rate and
New Phytologist (2010) 185: 42–53
www.newphytologist.org
New
Phytologist
number of freeze–thaw cycles (Mayr et al., 2007). In
some cases it was observed that cavitations could be
actively removed. This process of water refilling under
negative pressure is not fully understood, but appears to
involve living cells and to require energy (Cochard et al.,
2001; Holbrook et al., 2001; Salleo et al., 2004).
Ecological relevance of xylem hydraulic
architecture
The characteristics of xylem hydraulic architecture, such as
the arrangement, frequency, length, diameter, wall thickness and pit characteristics of conduits, not only regulate
the efficiency of water transport but also affect the margins
of 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- and
intraspecific differences in xylem hydraulic architecture
reflect not only size- or age-related trends but also differences in the way trees adapt or adjust to environmental variability, and can provide information about the plasticity of
a species under changing environmental conditions. A more
direct approach is to assess temporal plasticity in xylem
hydraulic architecture in a tree-ring sequence of a single
tree. As within the same tree and species resistance to cavitation is related to conduit diameter, the risk of system failure
is higher in tree rings where a large amount of the total
hydraulic conductivity is contributed by a few wide conduits. This holds especially true for ring-porous species
where water transport is assumed to take place in the outermost tree ring only. Figure 1 shows an example of how the
risk of a system failure can vary along the annual rings of
one individual. In this case, because of higher cavitation risk
under similar stress conditions, at least 50% loss of conductivity are more likely to occur in years such as 1988 than as
2002 (see Fig. 1).
The developmental success and the competitiveness of
trees depend on their ability to adjust and optimize their
hydraulic architecture to their specific environment. Major
hydraulically relevant properties, such as ring-porous or diffuse-porous xylem structure, leaf stomatal behaviour or the
kind of root system, generally define the range of a species’
tolerance and competitiveness and thus the ecological setting to which a species is adapted. However, the ecological
amplitude and thus the species distribution within given
ecological settings may be partly limited by the species’ plasticity in relevant traits in response to the environmental variability, not only in spatial terms, but also over the lifetime
of a tree (Sultan, 2000; Valladares et al., 2007). Moving
outside these ranges can have detrimental consequences for
the plant.
Comparative analyses of hydraulic traits of trees have
proved to be a valuable source of information for functional
and ecological wood anatomy. The majority of studies doc-
The Authors (2009)
Journal compilation New Phytologist (2009)
New
Phytologist
Review
Research review
umenting variation in xylem hydraulic structure in relation
to changes in water availability were based on comparisons
along different evolutionary developments (e.g. Sperry,
2003; Rowe & Speck, 2005), among diverse groups of distantly related taxa (e.g. Carlquist, 1975; Maherali et al.,
2004), across ecotypes (e.g. Stout & Sala, 2003; Choat
et al., 2007; Sobrado, 2007; De Micco et al., 2008), phenotypes (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 dynamic
hydraulic adjustments through the lifetimes of individuals
or groups of trees. Coping with temporal environmental
variability is the most critical challenge for the survival of
an individual tree. Because trees undergo a continuous
process of ontogenetic adjustments to respond to stress
situations caused by a changing environment, and
changing size and age, valuable ecological information can
be extracted from the temporal reconstruction of these
responses.
Environmental imprinting in wood cell anatomy
Meristems generate new functional structures during the
entire life-span of an organism. Secondary growth of the
woody stem in particular is a dynamic process and is influenced in a complex way by whole-tree physiology, which in
turn is controlled by environmental conditions. The effect
of factors that strongly influence secondary growth are
permanently registered within the anatomical characteristics
and reflected in the tree-ring structure. During wood
formation, xylem cells differentiate through a complex
process encompassing cell-type determination, cell division,
cell differentiation and programmed cell death (see reviews
in Fukuda, 1996; Plomion et al., 2001; Scarpella & Meijer,
2004). These processes are genetically controlled and depend on the ontogenetic status of the tree, but are also influenced, directly and indirectly, by environmental conditions
(Denne & Dodd, 1981).
On the one hand, an environmental event such as a frost
can directly influence cells undergoing differentiation and
1988
100 000
50%
60 000
10%
0 20 000
Conduit area (µm2)
(a)
2002
1%
1960
1970
1980
1990
2000
Year
(b)
Fig. 1 Fluctuation of the threshold conduit
area defining the remaining hydraulic
conductivity when all the widest vessels are
dysfunctional as a result of cavitation (one
tree of Quercus robur; 1956–2005).
(a) Conduit area contributing to 50% (dark
blue line), 10% (green line) and 1% (light
blue line) of the total conductivity. The
relative conductivity of each single conduit
was calculated according to the
Hagen–Poiseuille equation as the fourth
power of the radius. (b) Microsections of the
annual rings between 1988 and 2002.
Colouration of conduits shows their contributions to the overall conductivity: dark blue,
50%; green, 40%; light blue, 9%; red, 1%.
The Authors (2009)
Journal compilation New Phytologist (2009)
1988
2002
Ring width = 2.3 mm
Ring width = 2.2 mm
Vessel class
Dark blue
Green
Light blue
Red
Size
>95901 m2
60801–95900 µm2
5801–60800 µm2
1000–5800 µm2
Vessel class
Dark blue
Green
Light blue
Red
Size
>69201 m2
45001–69200 µm2
4001–4500 µm2
1000–4000 µm2
New Phytologist (2010) 185: 42–53
www.newphytologist.org
45
46
Review
Research review
thus leave an imprint of weakly lignified and crumpled conduits inside a band of dead cell tissue in the tree ring
(Glerum & Farrar, 1966). Analogously, spring conditions
occurring at the time of early wood vessel formation determine cell size by influencing the rate of cell division and differentiation, as observed for some ring-porous species
(Garcı́a-González & Eckstein, 2003; Fonti & Garcı́aGonzález, 2004, 2008). In these cases, the susceptible period of xylem formation to directly perceive and encode
environmental signals is the time window during which
cells are developing. As the periods of division, expansion
and maturation of xylem cells range from several days to
a few weeks (e.g. Rossi et al., 2006), concurrent weather
conditions are likely to directly leave imprints of their
occurrence in the ring structure.
On the other hand, prevailing environmental conditions
such as persistent drought periods can also indirectly induce
adjustments in the wood structure through tree physiological modifications to adapt to the new environmental
demands. Cambial activity and wood cell development are
strongly dependent on the availability of photoassimilates.
In this case, the photosynthesis rate is reduced and assimilate translocation is adjusted, which ultimately influences
cambial activity and xylogenesis, even in subsequent seasons, as observed for Quercus pubescens and Pinus sylvestris
growing under contrasting water supplies (Eilmann et al.,
2009). The resulting wood-anatomical modifications can
greatly differ depending on tree metabolism and speciesspecific wood structure, but also depending on the timing
of the season when the environmental event occurs. A
drought event early in the growth season can induce
different wood-anatomical modifications from a drought
event at the end of the summer, when trees might merely
respond by ceasing wood formation early (Arend &
Fromm, 2007).
Through the means of wood formation, trees are thus
able to perceive directly and indirectly environmental changes which leave permanent environmental imprints on
xylem cells and wood structures, representing a valuable
archive for environmental scientists.
Principles and challenges for decoding
cell-based information
Reconstruction of past environmental conditions using the
variability of datable tree-ring structures is an important
area in dendrochronology. The study of the variation of
cell-anatomical characteristics across series of annual rings
started in the 1960s and 1970s (Knigge & Schulz, 1961;
Eckstein et al., 1974) but has intensified in the last two
decades as a result of improvements in digital image analysis. Formerly, measurements were made visually on microscope slides, with attendant constraints in terms of the
objectivity of quantification and the sample size that could
New Phytologist (2010) 185: 42–53
www.newphytologist.org
New
Phytologist
be used. At present, if the cells are large enough, for example in the early wood vessels of ring-porous species, digital
images 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 these
cases, specific surface preparation techniques are required
(e.g. Spiecker et al., 2000). In general, cutting is preferred
to sanding as it keeps cell walls clean and cell lumina
open. Another necessity for these procedures is to obtain a
high contrast between target objects and background. This
contrast can be enhanced by darkening the wood surface
with ink or a stain and subsequently filling the cell lumina
with a bright substance such as white chalk, plasticine or
wax. Continuous progress in the development of image
analysis systems involving powerful digital cameras, scanners and sophisticated software, as well as new techniques
for wood surface preparation using specific microtomes
(Gärtner & Nievergelt, in press), suggests that in the
future it will probably be possible to examine smaller cells,
such as the vessels of diffuse-porous wood, tracheids, fibres
and parenchyma cells, and even subcellular features such
as bordered pits.
The extraction of information from series of woodanatomical characteristics of xylem cells has been based
on well-established dendrochronological principles, such
as the existence of similar environmentally driven
responses in individuals growing under similar environmental conditions. This assumes the existence of common
variability in the time series of different individuals (common signal), caused by the influence of a given environmental factor (the signal). Moreover, the processes linking
current environmental conditions with responses must
have been the same as those operating in the past (James
Hutton’s principle of uniformitarianism; Britannica
Concise Encyclopædia, 2009). In order to extract this
information, a widely accepted set of specific sampling
principles (selection of sites, species and trees) and methodological procedures (definition of tree-ring variables,
cross-dating, replication, standardization for noise reduction and detrending of ageing trend) has been established
for which only variables such as ring width and maximum
latewood density were initially considered (Cook &
Kairiukstis, 1990; Fritts, 2001).
The major differences between these traditional and
wood-anatomical variables are the scale (moving from mm
to lm), the larger number of observations for each ring,
and the higher temporal (intra-annual) resolution of the
measurements of the wood-anatomical variables. While
ring-width-based dendrochronology usually extracts one
value per ring, integrating radial growth throughout the
growing season, measurements of wood-anatomical variables yield much more data from different parts of the
tree ring which are highly variable along both the radial
(time) and tangential (spatial) positions within a tree
The Authors (2009)
Journal compilation New Phytologist (2009)
New
Phytologist
(a)
Research review
(b1)
(b2)
(b3)
Review
(b4)
Fig. 2 Example of an automated early wood vessel measurement from a digital image. (a) Cut-out digital image of a Quercus robur core
cross-section captured with a high-resolution and distortion-free digital scanner. The image was scanned at 256 greyscale with a resolution of
1500 dpi. The core surface was sanded using 30 lM grit and cleaned with high-pressure water blasting to remove both tyloses and wood
dust from the vessel lumina. In order to improve the contrast, the surrounding tissue was stained black with printer ink and lumina were filled
with white chalk powder. (b) Procedures for vessel recognition and measurement performed using an image analysis tool developed by the
authors (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 homogenizes image contrast which varies as a result of natural heterogeneity in wood surface quality. After additional edge enhancement, the image is
segmented into a binary image using a fixed threshold value of intensity (b1). Clustered image objects are split and vessels (green objects) identified based on area (‡ 1000 lm2) and morphometric characteristics (b2). Annual ring traces (yellow lines) are recognized based on the position
of the largest (early wood) vessels (in purple; b3). Misidentified ring boundaries and vessels are corrected using a manual editing mode available in ROXAS. Finally, recognized vessels are assigned to the corresponding annual ring (alternatively coloured red and white; b4) anatomical
measurement of each single vessel is exported into a spreadsheet file (cf. Fonti et al., 2009a for further details).
ring (see images in Fig. 1). From these data, meaningful
wood-anatomical variables (mean values, density values,
and tissue proportions) have to be calculated for each tree
ring to build annual time series. As a consequence of the
changing environmental conditions throughout the year
and especially during the growing period, radial files of
consecutive cells produced at different times during the year
encode seasonal information. But even cells formed at the
same time must be measured in sufficient numbers to
account for tangential variability in the xylem. If too few
cells are considered, or cells encoding different environmental information at different times are mixed, the ecological
information can be obscured or reduced. A higher time
resolution of the climate signal can often be achieved by
using features of subgroups of cells that are formed at the
same time (Garcı́a-González & Fonti, 2006). In these cases
The Authors (2009)
Journal compilation New Phytologist (2009)
the signal encoded can reflect climatic conditions that
prevail for short periods of from 1 to 2 months.
Studies on ring-porous early wood vessels have shown
that all vessels along a 12-mm-thick tangential band have to
be measured to stabilize the extractable environmental
signal (Garcı́a-González & Fonti, 2008). Moreover, the
environmental signal can be maximized, reduced, or even
absent depending on the criteria applied to select different
vessel-area categories (Fig. 1) or vessel positions (e.g. early
wood vessels of the first row) within the rings.
In conifers, specific standardization procedures (normalized tracheidogram; Vaganov, 1990; or Gompertz function;
Rossi et al., 2003) have been developed to transform the
absolute radial position of a radial row of consecutive tracheids across a tree ring to a relative position, and thus allow
a comparison among tree rings. In these cases, at least five
New Phytologist (2010) 185: 42–53
www.newphytologist.org
47
48
Review
New
Phytologist
Research review
radial files of tracheids have to be measured to obtain reliable data on the variability of cell sizes across tree rings.
Methods to monitor cambial dynamics, such as repeated
pinning (e.g. Dünisch et al., 2002; Seo et al., 2007) or
micro-coring (Deslauriers et al., 2003; Rossi et al., 2006;
van der Werf et al., 2007), permit the determination of seasonal growth patterns that allow each cell in a radial file of
tracheids to be assigned to the time of the season at which it
was formed.
Time series of wood-anatomical variables and
their environmental signals
Specific environmental events affecting cambial activity
leave wood-anatomical imprints inside the tree ring.
Dendrochronology has often been used to reconstruct the
spatio-temporal distribution of discontinuous events based
on these imprints (Gartner et al., 2002; Wimmer, 2002).
Many studies have described these imprints in relation to
the effect of fire (e.g. Madany et al., 1982; Smith & Sutherland, 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 George
et al., 2002), geomorphic processes (e.g. St George &
Nielsen, 2003; Gärtner, 2007; den Ouden et al., 2007), or
frost (e.g. LaMarche & Hirschboeck, 1984).
Recent studies measuring wood-anatomical variables
across series of rings have demonstrated that there is also
potential to extract palaeo-ecological information from continuous chronologies (Eckstein, 2004; Vaganov et al.,
2006). These chronologies allow the application of statistical models to relate wood-anatomical variables to continuous, highly resolved environmental variables, and through
the use of transfer functions they can be used for reconstructions before instrumental data. Most of the relatively few
studies performed to date (Table 1) have examined the link
between different environmental signals and the area of
water-conducting cells. Variability in wood-anatomical variables was found to be mainly related to seasonal climate conditions, such as temperature or water availability, and the
quality and strength of the signal varied with species, climatic zone, season of the year and the anatomical variable
considered. In conifers, studies mainly focused on tracheid
lumen size and cell wall thickness (Yasue et al., 2000; Wang
et al., 2002; Kirdyanov et al., 2003; Panyushkina et al.,
2003; Eilmann et al., 2006; Vaganov et al., 2006), whereas
in angiosperms, particular attention was given to the early
wood vessels of ring-porous species such as Quercus spp.
(Garcı́a-González & Eckstein, 2003; Eilmann et al., 2006;
Tardif & Conciatori, 2006; Fonti & Garcı́a-González,
2008), Castanea sativa (Fonti & Garcı́a-González, 2004;
Fonti et al., 2007) and Tectona grandis (Pumijumnong &
Park, 1999). Similar explorative analyses were also carried
New Phytologist (2010) 185: 42–53
www.newphytologist.org
out for the diffuse-porous species Fagus sylvatica (Sass &
Eckstein, 1995) and Populus · euroamericana (Schume
et al., 2004).
Most of these studies have highlighted a close relationship
between wood-anatomical variables and seasonal climatic
conditions. In some cases and for some specific variables it
has been demonstrated that the signal in wood-anatomical
variables in comparison to traditional tree-ring variables
(ring width or maximum late wood density) can provide
either higher temporal resolution (Panyushkina et al.,
2003), different information (Garcı́a-González & Eckstein,
2003; Fonti & Garcı́a-González, 2004), or applicability to
other environments (Fonti & Garcı́a-González, 2008).
However, we are convinced that screening for additional
meaningful wood-anatomical variables in different species
(sensu Fonti & Garcı́a-González, 2004; Tardif & Conciatori, 2006) and careful exploration of the signal in subselections of contemporaneously formed cells (Garcı́a-González
& Fonti, 2006; 2008) will further support promising
findings presented in Table 1.
However, time series analysis with wood-anatomical variables has primarily been used to explore the potential to
obtain high-resolution proxies (1) by identifying which
environmental factor mainly influences wood-anatomical
variability 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 physiological
mechanisms that cause the variability in wood anatomy.
However, wood-anatomical variables have rarely been
applied to infer functional adjustments of xylem hydraulic
architecture to temporally changing conditions (e.g. Sterck
et al., 2008). Year-to-year analyses will permit the establishment of a link between climatic conditions and the anatomical characteristics of the forming wood. The attribution of
these results to specific physiological responses and elucidation of the functional costs and benefits of the adjustment
(see example in Fig. 1) would contribute to a better understanding of the plasticity in xylem hydraulic architecture
and the different strategies adopted by trees when they are
exposed to changing environmental conditions.
Conclusion and perspectives
Tree-ring anatomy provides a valuable opportunity to add a
time component to the study of plant responses to changing
environments. As a consequence of the direct relationship
between cell structure (e.g. vessel area and vessel density) and
function and their short period of formation, water-conducting cells can record and permanently encode environmental
information with a high temporal resolution. With respect
to traditional tree-ring variables, chronologies of wood-anatomical variables can thus provide novel information that is
not necessarily limited to trees growing under harsh conditions in marginal habitats. Decoding this information, which
The Authors (2009)
Journal compilation New Phytologist (2009)
The Authors (2009)
Journal compilation New Phytologist (2009)
Quercus ilex
Quercus faginea
Populus · euroamericana
Rhizophora mucronata
Quercus alba, Quercus rubra
Quercus pubescens
Quercus pyrenaica
Corcuera et al. (2004a)
Corcuera et al. (2004b)
Schume et al. (2004)
Verheyden et al. (2004, 2005)
Tardif & Conciatori (2006)
Eilmann et al. (2006, 2009)
Corcuera et al. (2006)
Prosopis flexuosa (semi ring-porous)
Castanea sativa
Fonti & Garcı́a-González (2004)
Giantomasi et al. (2009)
Quercus robur
Garcı́a-González & Eckstein (2003)
Quercus petrea
Quercus macrocarpa
St George et al. (2002)
Fonti et al. (2009b)
Tectona grandis
Pumijumnong & Park (1999)
Quercus petreae, Quercus pubescens
Breonadia salicina
Gillespie et al. (1998)
Fonti and Garcı́a-González (2008)
Fagus sylvatica
Sass & Eckstein (1995)
Rhizophora mucronata
Castanea sativa
Vessel size
Quercus robur, Quercus petreae
Huber (1993)
Schmitz et al. (2006)
Fonti et al. (2007)
Vessel diameter and density
Quercus macrocarpa
Woodcock (1989)
1910–1967
Germany
1960–1984
Southeastern Nebraska, USA
1961–1979
France
1914–1988
Valais, Switzerland
1971–1993
South Africa
1947–1996
Southeast Asia
1884–2000
Floodplain, Manitoba, Canada
1925–1996
Maritime site, Spain
1956–1995
Southern Swiss Alps
1982–1997
Northeast Spain
1980–1997
Northeast Spain
1971–1996
Alluvial basin, Austria
Kenyan mangrove forest
1900–1989
Southwestern Quebec
1970–1985
Valais, Switzerland
1976–1997
Northeast Spain
Kenyan mangrove forest
1966–2004
Southern Swiss Alps
1956–2005
Switzerland
1556–2002
Switzerland
1940–2004
Arid and semiarid
central Argentina
Time period and region
November to December P
Early spring P
Early spring P
Salinity
Early spring T
Drought
Rain seasonality
Different climatic parameters
(T and P and drought index)
Drought
Groundwater regime
Drought
Previous late summer P,
early spring T
Summer drought
P between February and April
Different climatic parameters
(T and P)
Flooding event
Mean annual P (July to June)
Max T from previous September
to December
July P
October to June P
Spring P and winter T
Environmental signal
(P, precipitation; T,
temperature)
Research review
Vessel number and vessel area
Early wood vessel size
Early wood vessel size
Vessel density
Early wood vessel size
Vessel diameter and density
Size and number of vessels
Vessel density
Number and size of vessels
Vessel diameter and density
Early wood vessel size
Early wood vessel size
Mean vessel area and diameter,
conductive area and vessel density
Early wood vessel size
Mean vessel diameter and area
Vessel size
Early wood vessel size
Vessel diameter and density
Vessel area
Quercus robur, Fagus sylvatica
Hardwood
Eckstein & Frisse (1982)
Anatomical features
Species
Paper
Table 1 Overview of papers using chronologies of wood cell anatomical features
New
Phytologist
Review
New Phytologist (2010) 185: 42–53
www.newphytologist.org
49
Review
New
Phytologist
Drought
1970–1985
Valais, Switzerland
Size and number of tracheids
Larix sibirica, Larix
gmelinii, Larix cajanderi
Pinus sylvestris
Larix cajanderi
Tracheid number,
size and wall thickness
Tracheid number,
size and wall thickness
Tracheid size and wall thickness
Picea mariana
Different climatic parameters
(T and P)
Mean June T
July to September T
Summer T
1901–1990
Japan
1940–1992
Northern Quebec
1642–1993
Siberia
1936–1989 Siberia
Tracheid size and wall thickness
Picea glehnii
Summer T and August P
Time period and region
Anatomical features
Species
Environmental signal
(P, precipitation; T,
temperature)
Research review
is strongly related to the characteristics and the position of
the cells within the annual ring, requires specific methodological approaches, including the survey of promising woodanatomical variables, appropriate preparation techniques,
and sophisticated statistical tools to build chronologies and
to analyse the relation with environmental factors.
Although this multidisciplinary approach is still at an
early stage of development and in some cases involves
tedious measuring work, it deserves to be further developed
as it has the potential to provide new information in global
change research. First, relevant relationships between the
physical environment and the physiological response of
trees can be recognized and analysed retrospectively, as this
information is permanently registered within the wood
structure. Secondly, the high time resolution of the environmental influence on wood anatomy can be valuable to identify how and when growth processes are sensitive to the
environment and therefore might contribute to disentangling the processes that control tree growth. This is important for understanding both physiological mechanisms and
the functional meaning of growth responses. This is crucial
for evaluating the range of plasticity and the capacity for
resilience of trees growing under certain environmental conditions and ultimately to predict plant responses under
future climatic scenarios.
For broader application of this approach in global change
research, a concerted effort involving diverse disciplines
(functional ecology, wood anatomy, plant physiology and
dendrochronology) is required to address some methodological and conceptual issues. Methodologically, there is a
need for (1) accurate and efficient measuring along series of
rings to increase sample size, (2) expansion of the range of
possible wood-anatomical variables to be measured (e.g. cell
grouping, pit structure and degree of lignification), (3)
understanding of how physiological processes and ageing
modify wood formation, (4) improvement of the procedures to identify and enhance environmental signals in different frequency domains, and (5) evaluation of the
synergistic effect of combining more tree-ring related proxies. In parallel there is a need for a better understanding of
the processes that regulate the hydraulic responses across
species, space and time and their functional meaning.
New Phytologist (2010) 185: 42–53
www.newphytologist.org
Eilmann et al. (2006, 2009)
Kirdyanov et al. (2003)
Panyushkina et al. (2003)
Wang et al. (2002)
Softwood
Yasue et al. (2000)
Paper
Acknowledgements
Table 1 (Continued)
50
We thank three anonymous reviewers for valuable feedback
on and improvements to an earlier draft of this article.
References
Arend M, Fromm J. 2007. Seasonal change in the drought response of
wood cell development in poplar. Tree Physiology 27: 985–992.
Asshoff R, Schweingruber FH, Wermelinger B. 1999. Influence of a gypsy
moth (Lymantria dispar L.) outbreak on radial growth and wood-
The Authors (2009)
Journal compilation New Phytologist (2009)
New
Phytologist
anatomy of Spanish chestnut (Castanea sativa Mill.) in Ticino (Switzerland). Dendrochronologia 16–17: 133–145.
Baas P. 1986. Ecological patterns of xylem anatomy. In: Givnish TD, ed.
On the economy of plant form and function. Cambridge, UK: Cambridge
University Press, 327–352.
Baas P, Ewers FW, Davis SD, Wheeler EA. 2004. Evolution of xylem
physiology. In: Hemsley AR, Poole I, eds. The evolution of plant physiology. London, UK: Elsevier Academic Press, 273–295.
Beikircher B, Mayr S. 2008. The hydraulic architecture of Juniperus communis L. ssp. communis: shrubs and trees compared. Plant, Cell & Environment 31: 1545–1556.
Britannica Concise Encyclopædia. 2009. ‘Uniformitarianism’. In: Encyclopædia Britannica, Premium Service. http://www.britannica.com
(accessed 14 August 2009).
Carlquist S 1975. Ecological strategies of xylem evolution. Berkeley, CA,
USA: University of California Press.
Carlquist S. 1988. Comparative wood anatomy: systematic, ecological and
evolutionary aspects of dicotyledon wood. Berlin Heidelberg, New York,
NY, USA: Springer-Verlag.
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. 2009.
Towards a worldwide wood economics spectrum. Ecology Letters 12:
351–366.
Choat B, Sack L, Holbrook M. 2007. Diversity of hydraulic traits in nine
Cordia species growing in tropical forests with contrasting precipitation.
New Phytologist 175: 686–698.
Choat B, Cobb AR, Jansen S. 2008. Structure and function of bordered
pits: new discoveries and impacts on whole-plant hydraulic function.
New Phytologist 177: 608–626.
Cochard H. 2006. Cavitation in trees. Comptes Rendus Académie des Sciences Physique 7: 1018–1026.
Cochard H, Lemoine D, Ameglio T, Granier A. 2001. Mechanisms of
xylem recovery from winter embolism in Fagus sylvatica. Tree Physiology
21: 1–27.
Comstock JP, Sperry JS. 2000. Theoretical consideration of optimal conduit length for water transport in vascular plants. New Phytologist 148:
195–218.
Cook ER, Kairiukstis LA. 1990. Methods of dendrochronology:
applications in the environmental sciences. International Institute for
Applied Systems Analysis. Boston, MA, USA: Kluwer Academic
Publishers.
Cook ER, Woodhouse CA, Eakin CM, Meko DM, Stahle DW. 2004.
Long-term aridity changes in the western United States. Science 306:
1015–1018.
Corcuera L, Camarero JJ, Gil-Pelegrin E. 2004a. Effects of a severe
drought on Quercus ilex radial growth and xylem anatomy. Trees –
Structure and Function 16: 83–92.
Corcuera L, Camarero JJ, Gil-Pelegrin E. 2004b. Effects of a severe
drought on growth and wood anatomical properties of Quercus faginea.
IAWA Journal 25: 185–204.
Corcuera L, Camarero JJ, Siso S, Gil-Pelegrin E. 2006. Radial-growth
and wood-anatomical changes in overaged Quercus pyrenaica coppice
stands: functional responses in a new Mediterranean landscape. Trees –
Structure and Function 20: 91–98.
De Micco V, Aronne G. 2009. Seasonal dimorphism in wood anatomy of
the Mediterranean Cistus incanus L. subsp. incanus. Trees – Structure and
Function 23: 981–989.
De Micco V, Aronne G, B7aas P. 2008. Wood anatomy and hydraulic
architecture of stems and twigs of some Mediterranean trees and shrubs
along a mesic–xeric gradient. Trees – Structure and Function 22: 643–
655.
Denne MP, Dodd RS. 1981. The environmental control of xylem differentiation. In: Barnett JR, ed. Xylem cell development. Kent, UK: Castle
House, 236–255.
The Authors (2009)
Journal compilation New Phytologist (2009)
Research review
Review
Deslauriers A, Morin H, Bégin Y. 2003. Cellular phenology of annual
ring formation of Abies balsamea in the Quebec boreal forest (Canada).
Canadian Journal of Forest Research 33: 190–200.
Dixon HH, Joly J. 1895. On the ascent of sap. Philosophical Transaction of
the Royal Society of London 186: 563–576.
Dünisch O, Bauch J, Gasparotto L. 2002. Formation of increment zones
and intra-annual growth dynamics in the xylem of Swietenia macrophylla, Carapa guianensis, and Cedrela odorata (Meliaceae). IAWA Journal 23: 101–119.
Eckstein D. 2004. Change in past environments – secrets of the tree hydrosystem. New Phytologist 163: 1–4.
Eckstein D, Frisse E. 1982. The influence of temperature and precipitation
on vessel area and ring width of oak and beech. In: Hughes MK, Kelly
PM, Pilcher JR, LaMarche VC, eds. Climate from tree rings. Cambridge,
UK: Cambridge University Press, 12.
Eckstein D, Frisse E, Liese W. 1974. Holzanatomische Untersuchungen
an umweltgeschädigten Strassenbäumen der Hamburger Innenstadt.
European Journal of Forest Pathology 4: 232–244.
Eilmann B, Weber P, Rigling A, Eckstein D. 2006. Growth reactions of
Pinus sylvestris L. and Quercus pubescens Willd. to drought years at a xeric
site in Valais, Switzerland. Dendrochronologia 23: 121–132.
Eilmann B, Zweifel R, Buchmann N, Fonti P, Rigling A. 2009. Droughtinduced adaptation of xylem in Scots pine and pubescent oak. Tree
Physiology 29: 1011–1020.
Esper J, Cook ER, Schweingruber FH. 2002. Low-frequency signals in
long tree-ring chronologies and the reconstruction of past temperature
variability. Science 295: 2250–2253.
Esper J, Büntgen U, Frank DC, Nievergelt D, Liebhold A. 2007.
1200 years of regular outbreaks in alpine insect. Proceedings of the Royal
Society B 274: 671–679.
Field TS, Brodribb T. 2001. Stem water transport and freeze–thaw xylem
embolism in conifers and angiosperm in a Tasmanian treeline heath.
Oecologia 127: 314–320.
Fonti P, Garcı́a-González I. 2004. Suitability of chestnut earlywood vessel
chronologies for ecological studies. New Phytologist 163: 77–86.
Fonti P, Garcı́a-González I. 2008. Earlywood vessel size of oak as potential
proxy for spring precipitation in mesic sites. Journal of Biogeography 35:
2249–2257.
Fonti P, Solomonoff N, Garcı́a-González I. 2007. Earlywood vessels of
Castanea sativa record temperature before their formation. New Phytologist 173: 562–570.
Fonti P., Eilmann B, Garcı́a-González I, von Arx G. 2009a. Expeditious
building of ring-porous earlywood vessel chronologies without loosing
signal information. Trees – Structure and Function 23: 665–671.
Fonti P, Treydte K, Osenstetter S, Frank DC, Esper J. 2009b. Frequencydependent signals in multi-centennial oak vessel data. Palaeogeography,
Palaeoclimatology, Palaeoecology 275: 92–99.
Fritts HC. 2001. Tree rings and climate. Caldwell, USA: Blackburn Press.
Fukuda H. 1996. Xylogenesis: initiation, progression, and cell death.
Annual Review of Plant Physiology and Plant Molecular Biology 47: 299–
325.
Garcı́a-González I, Eckstein D. 2003. Climatic signal of earlywood vessels
of oak on a maritime site. Tree Physiology 23: 497–504.
Garcı́a-González I, Fonti P. 2006. Selecting earlywood vessels to maximize
their environmental signal. Tree Physiology 26: 1289–1296.
Garcı́a-González I., Fonti P. 2008. Ensuring a representative sample of
earlywood vessels for dendroecological studies: an example from two
ring-porous species. Trees – Structure and Function 22: 237–244.
Gartner BL. 1995. Plant stems: physiological and functional morphology.
New York, NY, USA: Academic Press.
Gärtner H. 2007. Tree roots: methodological review and new development
in dating and quantifying erosive processes. Geomorphology 86: 243–251.
New Phytologist (2010) 185: 42–53
www.newphytologist.org
51
52
Review
Research review
Gärtner H, Nievergelt D. (in press). The core-microtome. A new tool for
surface preparation on cores and time series analysis of varying cell
parameters. Dendrochronologia.
Gartner B, Aloni R, Funada R, Lichtfuss-Gautier AN, Roig FA. 2002.
Clues for dendrochronology from studies of wood structure and function. Dendrochronologia 20: 53–61.
Giantomasi MA, Roig Juñent FI, Villagra PE, Srur AM. 2009. Annual
variation and influence of climate on the ring width and wood hydrosystem of Prosopis flexuosa DC trees using image analysis. Trees – Structure
and Function 23: 117–126.
Gillespie RD, Sym SD, Rogers KH. 1998. A preliminary investigation
of the potential to determine the age of individual trees of Breonadia
salicina (Rubiaceae) by relating xylem vessel diameter and area to
rainfall and temperature data. South African Journal of Botany 64:
316–321.
Glerum C, Farrar JL. 1966. Frost ring formation in the stems of some
coniferous species. Canadian Journal of Botany 44: 879–886.
Hacke UG, Jansen S. 2009. Embolism resistance of three boreal conifer
species varies with pith structure. New Phytologist 182: 675–686.
Hacke UG, Sperry JS. 2001. Functional and ecological xylem
anatomy. Perspectives in Plant Ecology, Evolution and Systematic 4:
97–115.
Hacke UG, Sperry JS, Pockman WP, Davis SD, McCullock KA. 2001.
Trends in wood density and structure are linked to prevention of xylem
implosion by negative pressure. Oecologia 126: 457–461.
Hacke UG, Sperry JS, Wheeler JK, Castro L. 2006. Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26:
689–701.
Holbrook NM, Ahrens ET, Burns MJ, Zwieniecki MA. 2001. In vivo
observation of cavitation and embolism repair using magnetic resonance
imaging. Plant Physiology 126: 27–31.
Huber F. 1993. Determination of the area of vessels in the earlywood of
indigenous oaks in France (Quercus robur L., Quercus petraea Liebl.):
effects related to individual trees, foliar cover, climatic conditions and
cambial age. Annals of Forest Sciences 50: 509–524.
IPCC 2007. Climate change 2007: the physical science basis. Contribution
of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University
Press.
Jansen S, Baas P, Gasson P, Smets E. 2003. Vestured pits: do they promote safer water transport? International Journal of Plant Sciences 164:
405–413.
Jones PD, Briffa KR, Osborn TJ, Lough JM, van Ommen TD, Vinther
BM, Luterbacher J, Wahl ER, Zwiers FW, Mann ME et al. 2009.
High-resolution palaeoclimatology of the last millennium: a review of
current status and future prospects. The Holocene 19: 3–49.
Kirdyanov A, Hughes M, Vaganov E, Schweingruber F, Silkin P. 2003.
The importance of early summer temperature and date of snow melt for
tree growth in the Siberian Subartic. Trees – Structure and Function 17:
61–69.
Knigge W, Schulz H. 1961. Einfluss der Jahreswitterung 1959 auf Zellartverteilung, Faserlänge und Gefässweite verschiedener Holzarten. Holz als
Roh- und Werkstoff 19: 293–303.
Koch GW, Sillett SC, Jennings GM, Davis SD. 2004. The limits to tree
height. Nature 428: 851–854.
Kramer PJ, Boyer JS. 1995. Water relations of plants and soils. San Diego,
CA, USA: Academic Press.
LaMarche VC Jr, Hirschboeck KK. 1984. Frost rings in trees as records of
major volcanic eruptions. Nature 307: 121–128.
Lambers H, Chapin FS, Pons TL. 2008. Plant physiological ecology. New
York, NY, USA: Springer Verlag.
Larson PR. 1994. The vascular cambium: development and structure. Berlin
Heidelberg New York: Springer Verlag.
New Phytologist (2010) 185: 42–53
www.newphytologist.org
New
Phytologist
Lemoine D, Granier A, Cochard H. 1999. Mechanism of freeze-induced
embolism in Fagus sylvatica L. Trees – Structure and Function 13: 206–
210.
Liang EY, Eckstein D. 2006. Light rings in Chinese pine (Pinus tabulaeformis) in semiarid areas of north China and their palaeo-climatological
potential. New Phytologist 171: 783–791.
Madany MH, Swetnam TW, West N. 1982. Comparison of two
approaches for determining fire dates from tree scars. Forest Science 28:
856–861.
Maherali H, Pockman WT, Jackson RB. 2004. Adaptive variation in the
vulnerability of woody plants to xylem cavitation. Ecology 83: 2184–
2199.
Mayr S, Cochard H, Ameglio T, Kikuta SB. 2007. Embolism formation
during freezing in the wood of Picea abies. Plant Physiology 143: 60–67.
Munro MAR, Brown PM, Hughes MK, Garcia EMR. 1996. Image analysis of tracheid dimensions for dendrochronological use. In: Dean JS,
Meko DM, Swetnam TW, eds. Tree rings, environment, and humanity.
Proceedings of the International Conference, Tucson, Arizona, 17–21
May 1994. Radiocarbon, Dept. of Geosciences University of Arizona,
843–851.
den Ouden J, Sass-Klaassen U, Copini P. 2007. Dendrogeomorphology –
a new tool to study drift-sand dynamics. Netherlands Journal of Geosciences 86: 355–363.
Panyushkina P, Hughes M, Vaganov E, Munro M. 2003. Summer temperature in northeastern Siberia since 1642 reconstructed from tracheid
dimensions and cell numbers of Larix cajanderi. Canadian Journal of
Forest Research 33: 1905–1914.
Pittermann J, Sperry JS, Wheeler J, Hacke U, Sikkema E. 2006. Mechanical reinforcement of tracheids compromises the hydraulic efficiency of
conifer xylem. Plant, Cell & Environment 29: 1618–1628.
Plomion C, Leprovost G, Stokes A. 2001. Wood formation in trees. Plant
Physiology 127: 1513–1523.
Poyatos R, Martı́nez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine
J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N et al. 2007.
Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia
153: 245–259.
Pumijumnong N, Park WK. 1999. Vessel chronologies from teak in
northern Thailand and their climatic signal. IAWA Journal 20: 285–
294.
Rossi S, Deslauriers A, Morin H. 2003. Application of the Gompertz
equation for the study of xylem cell development. Dendrochronologia 21:
33–39.
Rossi S, Deslauriers A, Anfodillo T. 2006. Assessment of cambial activity
and xylogenesis by microsampling tree species: an example at the Alpine
timberline. IAWA Journal 27: 383–394.
Rowe N, Speck T. 2005. Plant growth forms: an ecological and evolutionary perspective. New Phytologist 166: 61–72.
Salleo S, Lo Gullo MA, Trifilò P, Cardini A. 2004. New evidence for a role
of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell & Environment 27: 1065–1076.
Sass U, Eckstein D. 1995. The variability of vessel size in beech (Fagus
sylvatica L.) and its ecophysiological interpretation. Trees – Structure and
Function 9: 247–252.
Scarpella E, Meijer AH. 2004. Pattern formation in the vascular system of
monocot and dicot plant species. New Phytologist 164: 209–245.
Schmitz N, Verheyden A, Beeckman H, Kairo JG, Koedam N. 2006.
Influence of a salinity gradient on the vessel characters of the mangrove
species Rhizophora mucronata. Annals of Botany 98: 1321–1330.
Schume H, Grabner M, Eckmullner O. 2004. The influence of an altered
groundwater regime on vessel properties of hybrid poplar. Trees – Structure and Function 18: 184–194.
Schweingruber FH. 1996. Tree rings and environment – dendroecology.
Bern, Switzerland: Paul Haupt.
The Authors (2009)
Journal compilation New Phytologist (2009)
New
Phytologist
Schweingruber FH. 2006. Wood structure and environment. Berlin
Heidelberg, New York, NY, USA: Springer-Verlag.
Seo J-W, Eckstein D, Schmitt U. 2007. The pinning method: from pinning to data preparation. Dendrochronologia 25: 79–86.
Smith KT, Sutherland EK. 1999. Fire-scar formation and compartmentalization in oak. Canadian Journal of Forest Research 29: 166–171.
Sobrado MA. 2007. Relationship of water transport to anatomical features
in the mangrove Laguncularia racemosa grown under contrasting salinities. New Phytologist 173: 584–591.
Sperry JS. 2003. Evolution of water transport and xylem structure. International Journal of Plant Sciences 164: S115–S127.
Sperry JS, Hacke UG, Pittermann J. 2006. Size and function in conifer
tracheids and angiosperm vessels. American Journal of Botany 93: 1490–
1500.
Spicer R, Gartner BL. 1998. Hydraulic properties of Douglas-fir (Pseudotsuga menziesii) branches and halves with reference to compression wood.
Tree Physiology 18: 777–784.
Spiecker H, Schinker MG, Hansen J, Park YI, Ebding T, Doll W. 2000.
Cell structure in tree rings: Novel methods for preparation and image
analysis of large cross sections. IAWA Journal 21: 361–373.
St George S, Nielsen E. 2003. Palaeoflood records for the Red River, Manitoba, Canada, derived from anatomical tree-ring signatures. Holocene
13: 547–555.
St George S, Nielsen E, Conciatori F, Tardif J. 2002. Trends in Quercus
macrocarpa vessel areas and their implications for tree-ring paleoflood
studies. Tree-Ring Research 58: 3–10.
Sterck FJ, Zweifel R, Sass-Klaassen U, Qumruzzaman C. 2008. Persisting
soil drought reduces leaf specific conductivity in Scots pine (Pinus sylvestris) and pubescent oak (Quercus pubescens). Tree Physiology 28: 529–
536.
Stout DL, Sala A. 2003. Xylem vulnerability to cavitation in Pseudotsuga
menziesii and Pinus ponderosa from contrasting habitas. Tree Physiology
23: 43–50.
Sultan SE. 2000. Phenotypic plasticity for plant development, function
and life history. Trends in Plant Science 5: 537–542.
Tardif JC, Conciatori F. 2006. Influence of climate on tree ring and vessel
features in red oak and white oak growing near their northern distribution limit, southwestern Quebec, Canada. Canadian Journal of Forest
Research 36: 2317–2330.
Treydte K, Schleser GH, Helle G, Frank DC, Winiger M, Haug GH,
Esper J. 2006. The twentieth century was the wettest period in northern
Pakistan over the past millennium. Nature 440: 1179–1182.
Trouet V, Esper J, Graham NE, Baker A, Scourse JD, Frank DC. 2009.
Persistent positive North Atlantic Oscillation mode dominated the
Medieval Climate Anomaly. Science 324: 78–80.
Tyree MT, Zimmerman MH. 2002. Xylem structure and the ascent of sap.
2nd edn. New York, NY, USA: Springer-Verlag.
Vaganov EA. 1990. The tracheidogram method in tree-ring analysis and
its application. In: Cook ER, Kairiukstis LA, eds. Methods of
The Authors (2009)
Journal compilation New Phytologist (2009)
Research review
Review
dendrochronology. Applications in the environmental science. International
Institute for Applied Systems Analysis. Boston, MA, USA: Kluwer Academic Publishers, 63–75.
Vaganov EA, Hughes MK, Shashkin AV. 2006. Growth dynamics of conifer
tree rings: images of past and future environments. Berlin Heidelberg, New
York, USA: Springer-Verlag.
Valladares F, Gianoli E, Gómez JM. 2007. Ecological limits to plant
phenotypic plasticity. New Phytologist 176: 749–763.
Verheyden A, Kairo JG, Beeckman H, Koedam N. 2004. Growth rings,
growth ring formation and age determination in the mangrove Rhizophora mucronata. Annals of Botany 94: 59–66.
Verheyden A, De Ridder F, Schmitz N, Beeckman H, Koedam N. 2005.
High-resolution time series of vessel density in Kenyan mangrove trees
reveal a link with climate. New Phytologist 167: 425–435.
Villar-Salvador P, Castro-Dı́ez P, Pérez-Rontomé C, Montserrat-Martı́
G. 1997. Stem xylem features in three Quercus (Fagaceae) species along
a climatic gradient in NE Spain. Trees – Structure and Function 12:
90–96.
Von Arx G, Dietz H. 2005. Automated image analysis of annual rings in
the roots of perennial forbs. International Journal of Plant Science 166:
723–732.
Wang L, Payette S, Bégin Y. 2002. Relationships between anatomical and
densitometric characteristics of black spruce and summer temperature at
tree line in northern Quebec. Canadian Journal of Forest Research 32:
477–486.
van der Werf GW, Sass-Klaassen U, Mohren GMJ. 2007. The impact of
the 2003 summer drought on the intra-annual growth pattern of beech
(Fagus sylvatica L.) and oak (Quercus robur L.) on a dry site in the Netherlands. Dendrochronologia 25: 103–112.
Wheeler EA, Baas P. 1993. The potential and limitation of dicotyledonous
wood anatomy for climate reconstructions. Paleobiology 19: 487–498.
Wheeler EA, Sperry JS, Hacke UG, Hoang N. 2005. Inter-vessel pitting
and cavitation in woody Rosaceae and other vesselled plants: a basis for a
safety versus efficiency trade-off in xylem transport. Plant, Cell & Environment 28: 800–812.
Wheeler EA, Baas P, Rodgers S. 2007. Variations in dicot anatomy: a global analysis based on the Insidewood database. IAWA Journal 28: 229–
258.
Wiemann MC, Wheeler EA, Manchester SR, Portier KM. 1998.
Dicotyledonous wood anatomical characters as predictors of climate.
Palaeogeography, Palaeoclimatology, Palaeoecology 139: 83–100.
Wimmer R. 2002. Wood anatomical features in tree-rings as indicators of
environmental change. Dendrochronologia 20: 21–36.
Woodcock DW. 1989. Climate sensitivity of wood-anatomical features in
a ring-porous oak (Quercus macrocarpa). Canadian Journal of Forest
Research 19: 639–644.
Yasue K, Funada R, Kobayashi O, Ohtani J. 2000. The effects of tracheid
dimensions on variations in maximum density of Picea glehnii and relationships to climatic factors. Trees – Structure and Function 14: 223–229.
New Phytologist (2010) 185: 42–53
www.newphytologist.org
53