Dendrochronologia 32 (2014) 1–6
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Dendrochronologia
journal homepage: www.elsevier.com/locate/dendro
Original article
Comparing methods to analyse anatomical features of tree rings with
and without intra-annual density fluctuations (IADFs)
Veronica De Micco a,∗ , Giovanna Battipaglia b,c , Paolo Cherubini d , Giovanna Aronne a
a
Dip. Agraria, Università degli Studi di Napoli Federico II, via Università, 100, I-80055 Portici, NA, Italy
Dip. Scienze e Tecnologie Ambientali, Biologiche e Farmaceutiche, Seconda Università di Napoli, via Vivaldi 43, 81100 Caserta, Italy
c
Centre for Bio-Archeology and Ecology, Ecole Pratique des Hautes Etudes (PALECO EPHE), Institut de Botanique, University of Montpellier 2, F-34090
Montpellier, France
d
WSL Swiss Federal Institute for Forest, Snow and Landscape Research, CH-8903 Birmensdorf, Switzerland
b
a r t i c l e
i n f o
Article history:
Received 30 July 2012
Accepted 1 June 2013
Keywords:
Dendroecology
Intra-annual density fluctuations (IADFs)
False rings
Mediterranean tree-rings
Quantitative wood anatomy
Vessel size
a b s t r a c t
Different methods to analyse variations in vessel size in tree rings with and without intra-annual density fluctuations (IADFs) in Erica arborea L. are presented. These methods are based on the in continuum
collection of vessel size data within the ring using digital images. In the analysis of rings from the early(EW) to late-wood (LW), the following vessel parameters were determined: (a) progressive number, (b)
lumen area, and (c) lumen centre of gravity (i.e. distance between lumen centre and EW beginning). To
make rings of different width or number of vessels comparable, progressive number and centre of gravity
variables were standardised. Different graphical representations and data interpolation techniques were
compared. Our results indicate that the most consistent procedure to measure the position and width of
IADFs along tree rings should include the following steps: (a) plotting vessel lumen area in relation to
standardised progressive number, (b) interpolation of vessel area series using simple moving average, (c)
superimposition of curves from series of tree rings with and without IADFs, and (d) the establishment of
the points where the two series intercept. Our results show that, in diffuse-porous woods, vessel position
can be represented by a simpler automatically detected parameter, thus simplifying the procedure for
data collection and analysis. The proposed graphical representation also facilitates the establishment of
links between IADFs and ecological processes.
© 2013 Elsevier GmbH. All rights reserved.
Introduction
Wood is the long-term memory of the history of a tree, because
tree rings record the signs of plant growth reactions behind biotic
and environmental influence. Both gradual variability in environmental factors and extreme events can be recognised in specific
traits of tree rings at anatomical and chemical levels. As summarised by Rossi and Deslauriers (2007), “wood is not just the simple
addition of unaltered elements like bricks on a pre-existing wall”.
Indeed, xylem formation is the result of cambial cell division and
processes of cell growth and differentiation. These phenomena are
regulated by several intrinsic factors (e.g. gene expression, hormonal signals and interaction between cell wall components), as
well as environmental factors (e.g. temperature and precipitation)
(Grozdits and Ifju, 1984; Wardrop, 1965; Deslauriers and Morin,
2005; De Micco et al., 2010; Lupi et al., 2010).
∗ Corresponding author. Tel.: +39 081 2532026/2539443; fax: +39 081 7755114.
E-mail address: demicco@unina.it (V. De Micco).
1125-7865/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.dendro.2013.06.001
Dendrochronology has emerged as a discipline studying tree
growth during long-time scales, to link tree-ring features and
climatic information in order to estimate retrospectively past
environmental dynamics. In the last decades, dendrochronology
has been supported more and more by other disciplines mainly
focusing on the study of cambial activity, quantification of wood
anatomical features and analysis of stable isotopes (De Micco et al.,
2007; Battipaglia et al., 2009; Rossi et al., 2012). Such a multidisciplinary approach helps extracting ecophysiological information
from tree rings (Fonti and García-González, 2004; Battipaglia et al.,
2007, 2010; Fonti et al., 2010; Moreno-Gutiérrez et al., 2012).
In dendroecology, the traditional weakness of using a minimum
time resolution of 1 year has been solved by introducing analytical approaches at shorter time scales (Rossi and Deslauriers, 2007).
Intra-annual analyses of tree rings allow a finer understanding of
plant growth responses to environmental variability. Moreover,
they help the interpretation of Intra-Annual-Density-Fluctuations
(IADFs), also known as false- or double-rings, which are generally
detected as abrupt changes in the wood density of tree rings. Initially investigated to solve problems of cross-dating due to false
rings consequent to frost events (Glock, 1951), IADFs have been
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V. De Micco et al. / Dendrochronologia 32 (2014) 1–6
more and more used to relate specific wood regions along a tree
ring to precise climatic anomalies, thus allowing reconstructing
detailed environmental information at a seasonal level. Such an
approach enhances that, apart the three spatial dimensions, wood
is characterised by a fourth dimension, namely time (Glock and
Reeds, 1940; Wimmer, 2002; Edmondson, 2010). The use of IADFs
as intra-annual pointers of climatic abrupt variations is particularly
interesting in shrub species of the Mediterranean area, where the
high frequency of IADFs hampers tree-ring dating (Cherubini et al.,
2003). Indeed, IADFs proved to be a valuable tool helping the interpretation of the main climatic factors driving wood formation in
Arbutus unedo L. and Pinus halepensis (Battipaglia et al., 2010; de
Luis et al., 2011).
As recently reported by Eckstein and Schweingruber (2009),
the quantification of specific wood anatomical features in treering series is expanding in tree-ring research, because the response
of trees to environmental changes is stored not only in tree-ring
width, wood density and isotope composition, but also in many
other anatomical features. However, different anatomical traits
are often highly correlated and can be considered interchangeable
indicators of changing environmental conditions during tree-ring
formation (Wimmer, 2002). It goes without saying that there might
be a natural tendency to consider anatomical traits easy to measure
and free from the operator subjectivity as much as possible. Definitely, the amount of time and labour needed for the collection
of wood structural data has discouraged thorough studies based
on large sampling (Gartner et al., 2002). The introduction of new
techniques for automatic assessment of wood anatomical features
has been a drive versus the development of quantitative wood
anatomy as a discipline strictly related to dendrochronology (Fonti
et al., 2010). However, the presence of tools for rapid assessment of
anatomical features can still not completely solve the problems of
subjectivity if correct standardisation of measurement and internal
controls are not established (Gartner et al., 2002; De Micco et al.,
2012).
In this paper, we present a comparison between different methods used to analyse vessel size variation in tree rings with and
without IADFs. Such methods are based on the collection of vessel
size data in continuum, along tree rings, in standardised transects
on digital images. Our aim was to verify whether, in the analysis of
vessel size variation along tree rings, data of vessel size need to be
coupled with data about the exact position of each vessel relative to
the ring boundary as done in Battipaglia et al. (2010). We hypothesise that, in a diffuse-porous wood, vessel position can be replaced
by a more easily detectable parameter: the progressive number
at which each vessel is automatically detected when scanning the
image for the analysis from the beginning of tree-ring (earlywood)
towards its ending (latewood). The investigation was focused on
Erica arborea L., a species common in the Mediterranean maquis,
whose wood has a tendency to form frequent IADFs.
data are from the Portoferraio meteorological station located at
10 km from the sampling site (42◦ 49 N, 10◦ 20 E, 25 m a.s.l.).
Tree-ring dating, selection of tree rings with and without IADFs in
microsections
Twenty plants (2–3 m height, 4–8 cm diameter), not multistemmed, were sampled. Three disks from the base of each shrub
were cut and air dried. In all samples, tree-ring width was measured
using a LINTAB linear table and a micrometer with a resolution
of 0.01 mm. Then samples were visually crossdated (Stokes and
Smiley, 1968) and the program COFECHA (Holmes, 1983) was run
to validate the crossdating and to find potential errors.
Subsamples from each disc were cross-sectioned with a sliding microtome. Sections (15 ␮m thick) were stained with safranin
and astra blue, dehydrated through an ethanol series, immersed in
xylene and mounted on slides with Canada balsam (Schweingruber,
1978; Gärtner et al., 2001). The micro-sections were studied under
a transmitted light microscope (Olympus BH-2, Germany) and
compared to the correspondent cross-dated disks to identify IADFs.
These were classified according to their position along tree-ring
width following Battipaglia et al. (2010). 78 tree rings were selected
for subsequent anatomical measurements. More specifically, 39
tree rings were without IADFs (i.e., normal rings with a gradual
transition from early-to latewood), while 39 showed middle-IADFs
(i.e., rings characterised by a layer of latewood-like xylem elements
in the middle of earlywood). For the analysis of anatomical parameters, the two groups of rings with and without IADFs were randomly
separated into two series of three replicates each (13 rings per
replicate).
Quantitative wood anatomy and data elaboration
Plant material
Microsections of the selected rings were analysed under a transmitted light microscope (BX60, Olympus). Photo-micrographs of
them, including the whole tree-ring width, were taken with a digital camera (CAMEDIA C4040, Olympus). The images were analysed
with AnalySIS 3.2 (Olympus) to quantify anatomical features. In
each microphotograph, a transect, 300–400 ␮m wide, throughout
the ring, was selected (Fig. 1a and b). Care was taken in order to
make the beginning of each transect correspond to the beginning
of earlywood (EW). Similarly, the end of each transect had to correspond to the ending of latewood (LW). In each transect, anatomical
parameters were automatically measured in all vessel elements
encountered moving from the left (beginning of EW) to the right
(ending of LW), following the in continuum method described by De
Micco et al. (2012). More specifically, per each encountered vessel,
the following parameters were measured: (a) lumen area, (b) the
centre of gravity of lumen defined as the Y-distance between the
lumen centre and the left border of the transect (beginning of EW).
During the measurement, the progressive number of each vessel
was recorded while scanning the transect from left to right.
Measured parameters were used to build dispersion graphs with
Y and X as coordinates of each vessel. Y corresponded to vessel
lumen area and Xi was defined according to four methods as follows.
Stem disks were sampled from E. arborea L. plants growing on
Isola d’Elba, an island in the Tyrrhenian sea (Italy). The main vegetation type of the island is maquis, and the climate is Mediterranean,
with hot and dry summer, followed by mild and wet autumn and
winter (Daget, 1977; Nahal, 1981). During the period 1970–2007,
the average summer and winter temperatures were 23.4 and
9.4 ◦ C, respectively, while precipitation was mainly concentrated
in autumn and winter, with an annual average of 375 mm. Climatic
(1) X1 = Absolute progressive number: the progressive number of
vessel detection while scanning the transect from left to right.
(2) X2 = Absolute centre of gravity: the centre of gravity of vessel
lumen (i.e. vessel distance from the beginning of the transect).
(3) X3 = Standardised progressive number: the progressive number
of vessel detection (while scanning the transect from left to
right), standardised dividing by the total number of vessels
encountered along the transect and multiplying by 100. In other
Materials and methods
V. De Micco et al. / Dendrochronologia 32 (2014) 1–6
3
to the distance between the beginning of the transect and the
last crossing between the two curves, either SMA or PC (Fig. 1c,
short arrow). According to these two principles, we calculated IADF
width as difference between Xend and Xbeg . IADF width was thus
measured following four procedures:
(a) Xend and Xbeg values taken from PC lines in graphs built with
Standardised progressive number (3p);
(b) Xend and Xbeg values taken from SMA lines in graphs built with
Standardised progressive number (3 m);
(c) Xend and Xbeg values taken from PC lines in graphs built with
Standardised centre of gravity (4p);
(d) Xend and Xbeg values taken from SMA lines in graphs built with
Standardised centre of gravity (4 m).
Data of IADF beginning and ending (i.e. Xbeg and Xend ) obtained
through the four procedures were compared by means of ANOVA
using SPSS statistical package (SPSS Inc., Chicago, Illinois, USA).
Multiple comparison tests were performed with LSD, Bonferroni
and Student–Newman–Keuls coefficients using P < 0.05 as the level
of probability.
Results
Fig. 1. Microphotographs of tree rings without (a) and with (b) middle-IADF, showing the selection of a transect for vessel size detection. Bar = 100 ␮m. Example of a
dispersion graph (c) with polynomial curves interpolating vessel-size data from tree
rings with middle-IADFs (black line) and without IADFs (grey line). Arrows point to
the beginning and ending of IADF.
words, the total number of vessels in each transect was always
considered equal to 100. In a diffuse-porous wood, X3 can be
considered as a parameter indicating the distance from the
beginning of the ring, expressed as a percentage of ring width.
(4) X4 = Standardised centre of gravity: the centre of gravity of vessel
lumen standardised with the whole ring width being considered equal to 100%. This standardisation was obtained by
dividing the Absolute centre of gravity by the total ring width and
multiplying by 100. In other words, X4 corresponds to the distance from the beginning of the ring, expressed as a percentage
of ring width.
The patterns of vessel size variability along ring width, obtained
through the four types of dispersion graphs, were visually compared in rings with and without IADFs.
Definition of the IADF region and statistical analyses
In the standardised data series (methods n. 3 and n. 4), simple
moving average (SMA, 40-points) and interpolation equations (PC,
fourth-order polynomial curve) were calculated. Per each couple
of replicates (13 rings with middle-IADF + 13 rings without IADFs),
dispersion graphs of data from tree rings with middle-IADF were
superimposed to those of rings without IADFs (Fig. 1c).
The beginning of IADF was assumed as the X-value (Xbeg ) corresponding to the distance between the beginning of the transect
and the first crossing between the two curves (point where the two
curves diverge), either with SMA or PC (Fig. 1c, long arrow). The
ending of IADF was assumed as the X-value (Xend ) corresponding
Tree rings without IADFs of E. arborea were characterised by
diffuse porous wood, mainly composed of solitary vessels. Rings
showed a gradual transition from earlywood, with large vessels,
to latewood with narrower vessels (Fig. 1a). Rings with IADFs
appeared as double rings where a sudden decrease in vessel lumen
size occurs in the middle of earlywood, forming a band of latewoodlike cells (Fig. 1b).
The graphs in Fig. 2 report the trends of vessel size variation
along the tree ring following the four proposed methods in both
rings with and without IADFs. The trend of gradually decreasing
vessel size typical of tree rings without IADFs clearly emerged only
when a standardisation of the position of each vessel along the ring
was considered (Fig. 2c and d; methodologies n. 3 and n. 4, based
on Standardised progressive number and Standardised centre of gravity respectively). When data standardisation was not performed
(Fig. 2a and b; methods n. 1 and n. 2 based on Absolute progressive
number and Absolute centre of gravity respectively), graphs failed
to illustrate reliable trends of gradual decrease of vessel size from
earlywood to latewood in rings without IADFs (Fig. 2a and b). In
rings with IADFs, methods n. 1 and n. 2 failed to reveal reliable
trends of vessel size variation as well (Fig. 2a and b). Only graphs
built with X-axis corresponding to Standardised progressive number or Standardised centre of gravity allowed to evidence the typical
trend of vessel size variation of rings with middle-IADFs (Fig. 2c
and d). This trend is characterised by the occurrence of an abruptly
steep decrease of vessel lumen area in the middle of earlywood, followed by an increase of vessel size which reaches, moving towards
latewood, values higher than those generally measured in rings
without IADFs at the corresponding ring width. Fig. 2 confirms
that to obtain reliable information on the patterns of vessel size
variation in tree rings with and without IADFs, data need to be standardised according to ring width: methods n. 3 and n. 4 have to be
followed. As a consequence, subsequent elaborations were done on
methods based on Standardised progressive number or Standardised
centre of gravity. Fig. 3 reports the dispersion graphs obtained by
plotting the whole set of data [vessel size coupled with either Standardised progressive number (method n. 3, Fig. 3a–c) or Standardised
centre of gravity (method n. 4, Fig. 3d–f)] of a replicate of rings without IADFs (Fig. 3a and d) and with middle-IADFs (Fig. 3b and e).
In the four dispersion graphs, PC and SMA are reported. Although
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V. De Micco et al. / Dendrochronologia 32 (2014) 1–6
different trends of vessel size variation between tree rings with and
without IADFs were evident when analysing the dispersion graphs
of the whole set of raw data (Fig. 3a, b, d and e), polynomial curves
were characterised by low correlation coefficients (0.20 < r2 < 0.41),
with minimum values occurring in rings with IADFs. The graphs in
Fig. 3c and f were built by superimposing PC and SMA curves of
tree rings with IADFs to those without IADFs according to methods n. 3 (Fig. 3c) and n. 4 (Fig. 3f). The analysis of graphs in Fig. 3c
and f indicated that both methods n. 3 and n. 4 allow the detection
of IADF in the same region of tree rings. These graphs were used
to calculate the Xbeg (beginning) and Xend (ending) values according to the two types of data interpolations. More specifically, the
Xbeg and Xend values derived always from graphs based on a standardised vessel position [i.e. either progressive number (Fig. 3c) or
centre of gravity (Fig. 3f)], but interpolated either with polynomial
curve or simple moving average. Statistical comparison between
data obtained following the four different methods showed that
there are no significant differences between the percentage of ring
width at which the IADFs begin (Xbeg ) and end (Xend ) in the four
cases (Fig. 4). In other words, the position and size (width) of IADFs
is always the same notwithstanding the method followed to calculate its beginning and ending.
Discussion
Fig. 2. Variation in vessel lumen area (VLA) along ring width in tree rings with
IADFs (black lines) and without IADFs (grey lines). X-data are relative to the four
methods: (a) absolute progressive number (APN); (b) absolute centre of gravity (ACG);
(c) standardised progressive number (SPN); (d) standardised centre of gravity (SCG).
Simple moving average is reported.
Dendrochronology has been increasingly interacting with other
disciplines, also introducing analytical approaches at time scales
shorter than one year (Rossi and Deslauriers, 2007). The analysis
of intra-annual variations of anatomical and isotopic data in tree
rings helps improving the extraction of ecophysiological information with seasonal time scale especially when IADFs are frequent
(Battipaglia et al., 2010). However, the correct identification of
IADFs is required as well as a correct standardisation of measurement procedures is needed to reduce subjectivity in data collection.
In our paper, we propose a new approach for the study of IADFs in
tree rings to reach a more objective classification and analysis of
IADFs features. The proposed method might follow the traditional
dendrochronological analysis which allows IADFs identification
through cross-dating techniques (Cherubini et al., 2003). We aimed
to verify whether, in the analysis of intra-annual chronologies of
vessel size in a diffuse-porous wood, it is possible to avoid coupling
data of vessel lumen area with data about the exact position of each
vessel along the ring. In order to do this, we visualised in dispersion graphs data of vessel lumen area coupled with four sets of data
(absolute progressive number, absolute centre of gravity, standardised progressive number and standardised centre of gravity) referred
to the position of each vessel along the tree ring. When absolute
values were considered, the evidenced trends of vessel size variation along the tree ring from earlywood to latewood were not
reliable either in rings with and without IADFs, partly due to the
lack of synchronization among tree rings characterised by different widths or number of vessel elements. Only graphs built with
X-axis corresponding to Standardised progressive number or Standardised centre of gravity allowed to evidence the typical trend of
vessel size decrease from earlywood to latewood in rings without
IADFs, and the typical vessel size fluctuation in the middle of earlywood in rings with middle-IADFs. The latter trend is characterised
by the occurrence of an abruptly steep decrease of vessel lumen
area in the middle of earlywood, followed by an increase of vessel size which reaches, moving towards latewood, values higher
than those generally measured in rings without IADFs at the corresponding ring width. This phenomenon is in agreement with vessel
lumen area variation evidenced in tree rings with IADFs in A. unedo
L. (De Micco et al., 2012). The analysis of data in E. arborea allowed
V. De Micco et al. / Dendrochronologia 32 (2014) 1–6
5
Fig. 3. Dispersion graphs obtained by plotting the whole set of vessel lumen area (VLA) and standardised data of a replicate of rings with IADFs (b and e) and without IADFs
(a and d). Polynomial curves and Simple moving average are shown for data measured with method n. 3 (based on standardised progressive number – a, b and c) and method
n. 4 (based on standardised centre of gravity – d, e and f).
us to confirm that to obtain reliable information on the patterns
of vessel size variation in tree rings with and without IADFs, data
need to be objectively standardised according to ring width to avoid
incorrect identification of IADFs and misleading interpretations of
anatomical variation at IADF level.
Once established the need to standardise the position of each
measured vessel, we verified that both interpolation with simple
moving average (SMA) and polynomial curves (PC) allowed to identify reliable trends of vessel size variation. Moreover, the position
and size (width) of IADFs was always the same notwithstanding
the interpolation method followed to calculate their beginning
and ending. However, the use of SMA should be preferred because
this parameter is more robust than polynomial curves (PC), especially when correlation coefficients are low, given that PC patterns
can change depending on their order. Our finding of the occurrence of lower correlation coefficients in tree rings with IADFs is in
agreement with the higher variability between rings under variable
environmental conditions (Battipaglia et al., 2010).
Therefore, the easiest and fastest procedure to detect and measure the position and width of IADFs along tree rings would
be: (a) the construction of dispersion graphs based on X-values
corresponding to the standardised progressive number, (b) the interpolation of the data series with simple moving average (SMA), (c)
Fig. 4. Comparison among the four methods to calculate the percentage of ring
width at which the IADFs begin (Xbeg ) and end (Xend ). 3p, polynomial curve (PC)
in graphs showing standardised progressive number; 3 m, simple moving average
(SMA) in graphs showing standardised progressive number; 4p, PC in graphs showing
Standardised centre of gravity; 4 m, SMA in graphs showing standardised centre of
gravity. Mean values and standard errors are shown. Different letter correspond to
significantly different values (P < 0.05).
6
V. De Micco et al. / Dendrochronologia 32 (2014) 1–6
the superimposition of curves belonging from the data series of tree
rings with and without IADFs, and (d) the analysis of points where
the two curves cross each other.
The use of standardised values allowed overcoming the problems related to the comparison between rings characterised by
different width. Moreover, our data demonstrate that in a diffuseporous wood, as that of E. arborea, the Standardised progressive
number can be used instead of the Standardised centre of gravity,
thus disregarding the information about exact vessel position. The
Standardised progressive number, being an easy parameter to detect,
helps quickening the procedure of data acquisition and treatment. This is in agreement with the general tendency to simplify
methodologies and to use anatomical characters easy to measure
(Wimmer, 2002). Besides, it encounters the general need to follow
automatic procedures to quickly collect anatomical data from large
number of samples and avoid subjectivity (Gartner et al., 2002; De
Micco et al., 2006).
In conclusion, the comparison between the different methods
reported in this paper allowed to indicate the first easy and quick
procedure of digital image analysis and data treatment to detect
the size and position of IADFs along tree rings.
Moreover, the graphs proposed, deriving from the superimposition of tendency curves of tree rings with and without IADFs,
can be useful also for ecological interpretations. Indeed, the position of the ring where the IADF begins (Xbeg ) might be related to
the period of the season when the stress priming the fluctuation
occurs. The width of IADFs might be related to the duration of conditions triggering their formation, while the Y-difference between
the two curves might give an idea of the magnitude of the stress
conditions. In this specific case study, the size of IADFs could be
related to the duration and intensity of a sudden drought during
earlywood formation in E. arborea. Such a phenomenon would be
in agreement with what found in other species such as A. unedo
and P. pinaster where the sudden decrease of conduit size in earlywood was accompanied by increased ı13 C values and interpreted
as stomata closure due to an unexpected period of drought (De
Micco et al., 2007; Battipaglia et al., 2010). Indeed, the proposed
procedure to analyse vessel size variation in tree rings might be
useful for ecological interpretations especially in Mediterranean
tree rings which have a tendency to form frequent IADFs. Given
that this procedure provides reliable understanding of vessel size
variation along tree rings with and without IADFs in diffuse porous
species, it will likely work also on softwoods whose conduits are
even more ordered.
Considering that environmental conditions, and consequently
also tree-ring features, can encounter variations from year to
year (De Micco and Aronne, 2009; de Luis et al., 2011), the proposed procedure has been devised to make general trends emerge,
supporting further studies combining integrated dendroecological
approaches.
Acknowledgements
The authors thank L. Nardella (Parco Nazionale dell’Arcipelago
Toscano) and D. Giove (Comunità Montana dell’Arcipelago
Toscano) for assistance in the field. We also acknowledge W.
Schoch, H. Gärtner and M. Nötzli for their support during the laboratory phase of this project.
References
Battipaglia, G., Cherubini, P., Saurer, M., Siegwolf, R.T.W., Strumia, S., Cotrufo, M.F.,
2007. Volcanic explosive eruptions of the Vesuvio decrease tree-ring growth but
not photosynthetic rates in the surrounding forests. Global Change Biology 13,
1122–1137.
Battipaglia, G., Saurer, M., Cherubini, P., Siegwolf, R.T.W., Cotrufo, M.F., 2009. Tree
rings indicate different drought resistance of a native (Abies alba Mill.) and a non
native (Picea abies (L.) Karst.) species co-occurring at a dry site in Southern Italy.
Forest Ecology and Management 257, 820–828.
Battipaglia, G., De Micco, V., Brand, W.A., Linke, P., Aronne, G., Saurer, M., Cherubini,
P., 2010. Variations of vessel diameter and ı13 C in false rings of Arbutus unedo
L. reflect different environmental conditions. New Phytologist 188, 1099–1112.
Cherubini, P., Gartner, B.L., Tognetti, R., Bräker, O.U., Schoch, W., Innes, J.L., 2003.
Identification, measurement and interpretation of tree rings in woody species
from Mediterranean climates. Biological Reviews 78, 119–148.
Daget, P., 1977. Le bioclimat méditerranéen: caractères généraux, mode de caractérisation. Vegetatio 34, 1–20.
de Luis, M., Novak, K., Raventós, J., Gričar, J., Prislan, P., Čufar, K., 2011. Climate factors
promoting intra-annual density fluctuations in Aleppo pine (Pinus halepensis)
from semiarid sites. Dendrochronologia 29, 163–169.
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., Toraldo, G., Aronne, G., 2006. Method to classify xylem elements using
cross sections of one-year-old branches in Mediterranean woody species. Trees
– Structure and Function 20, 474–482.
De Micco, V., Saurer, M., Aronne, G., Tognetti, R., Cherubini, P., 2007. Variations of
wood anatomy and ı13 C within tree rings of coastal Pinus pinaster ait. showing
intra-annual density fluctuations. IAWA Journal 28, 61–74.
De Micco, V., Ruel, K., Joseleau, J.-P., Aronne, G., 2010. Building and degradation
of secondary cell walls: are there common patterns of lamellar assembly of
cellulose microfibrils and cell wall delamination? Planta 232, 621–627.
De Micco, V., Battipaglia, G., Brand, W.A., Linke, P., Saurer, M., Aronne, G., Cherubini,
P., 2012. Discrete versus continuous analysis of anatomical and ı13 C variability in
tree rings with intra-annual density fluctuations. Trees – Structure and Function
26, 513–524.
Deslauriers, A., Morin, H., 2005. Intra-annual tracheid production in balsam fir stems
and the effect of meteorological variables. Trees – Structure and Function 19,
402–408.
Eckstein, D., Schweingruber, F., 2009. Dendrochronologia – a mirror for 25 years
of tree-ring research and a sensor for promising topics. Dendrochronologia 27,
7–13.
Edmondson, J.R., 2010. The meteorological significance of false rings in eastern red
cedar (Juniperus virginiana L.) from the Southern Great Plains. Tree Ring Research
66, 19–33.
Fonti, P., García-González, I., 2004. Suitability of chestnut earlywood vessel
chronologies for ecological studies. New Phytologist 163, 67–86.
Fonti, P., von Arx, G., García-González, I., Eilmann, B., Sass-Klaassen, U., Gärtner, H.,
Eckstein, D., 2010. Studying global change through investigation of the plastic
responses of xylem anatomy in tree rings. New Phytologist 185, 42–53.
Gärtner, H., Schweingruber, F.H., Dikau, R., 2001. Determination of erosion rates
by analyzing structural changes in the growth pattern of exposed roots. Dendrochronologia 19, 81–91.
Gartner, B.L., Aloni, R., Funada, R., Lichtfuss-Gautier, A.N., Roig, F.A., 2002. Clues
for dendrochronology from studies of wood structure and function. Dendrochronologia 20, 53–61.
Glock, W.S., Reeds Sr., E.L., 1940. Multiple growth layers in the annual increments
of certain trees at Lubbock, Texas. Science 91, 98–99.
Glock, W.S., 1951. Cambial frost injuries and multiple growth layers at Lubbock,
Texas. Ecology 32, 28–36.
Grozdits, G.A., Ifju, G., 1984. Differentiation of tracheids in developing secondary
xylem of Tsuga canadiensis L. Carr. Changes in morphology and cell-wall structure. Wood and Fiber Science 16, 20–36.
Holmes, R.L., 1983. Computer-assisted quality control in tree-ring dating and measurement. Tree-Ring Bulletin 43, 68–78.
Lupi, C., Hubert, M., Deslauriers, A., Rossi, S., 2010. Xylem phenology and wood
production: resolving the chicken-or-egg dilemma. Plant Cell and Environment
33, 1721–1730.
Moreno-Gutiérrez, C., Battipaglia, G., Cherubini, P., Saurer, M., Nicolás, E., Contreras,
S., Querejeta, J.I., 2012. Stand structure modulates the long-term vulnerability
of Pinus halepensis to climatic drought in a semiarid Mediterranean ecosystem.
Plant, Cell and Environment 35, 1026–1039.
Nahal, I., 1981. The Mediterranean climate from a biological viewpoint. In: di Castri,
F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World 11, MediterraneanType Shrublands. Elsevier Scientific Publishing Co., Amsterdam, pp. 63–86.
Rossi, S., Deslauriers, A., 2007. Intra-annual time scales in tree rings. Dendrochronologia 25, 75–77.
Rossi, S., Morin, H., Deslauriers, A., 2012. Causes and correlations in cambium
phenology: towards an integrated framework of xylogenesis. Journal of Experimental Botany 63, 2117–2126.
Schweingruber, F.H., 1978. Mikroskopische holzanatomie. Eidgenössische Anstalt
für das forstliche Versuchswesen. Birmensdorf, Switzerland.
Stokes, M.A., Smiley, T.L., 1968. An Introduction to Tree-Ring Dating. University of
Chicago, Chicago, IL, USA.
Wardrop, A.B., 1965. Cellular differentiation in xylem. In: Côté, W.A. (Ed.), Cellular Ultrastructure of Woody Plants. SyracuseUniversity Press, Syracuse, NY, pp.
61–97.
Wimmer, R., 2002. Wood anatomical features in tree-rings as indicators of environmental change. Dendrochronologia 20, 21–36.