The “blue ring”: anatomy and formation
hypothesis of a new tree-ring anomaly in
conifers
Alma Piermattei, Alan Crivellaro, Marco
Carrer & Carlo Urbinati
Trees
Structure and Function
ISSN 0931-1890
Trees
DOI 10.1007/s00468-014-1107-x
1 23
Your article is protected by copyright and
all rights are held exclusively by SpringerVerlag Berlin Heidelberg. This e-offprint is
for personal use only and shall not be selfarchived in electronic repositories. If you wish
to self-archive your article, please use the
accepted manuscript version for posting on
your own website. You may further deposit
the accepted manuscript version in any
repository, provided it is only made publicly
available 12 months after official publication
or later and provided acknowledgement is
given to the original source of publication
and a link is inserted to the published article
on Springer's website. The link must be
accompanied by the following text: "The final
publication is available at link.springer.com”.
1 23
Author's personal copy
Trees
DOI 10.1007/s00468-014-1107-x
SHORT COMMUNICATION
The ‘‘blue ring’’: anatomy and formation hypothesis of a new
tree-ring anomaly in conifers
Alma Piermattei • Alan Crivellaro
Marco Carrer • Carlo Urbinati
•
Received: 16 June 2014 / Revised: 6 October 2014 / Accepted: 7 October 2014
Ó Springer-Verlag Berlin Heidelberg 2014
Abstract
Key message Double-stained microsections from high
altitude Pinus nigra wood cores highlighted unlignified
latewood cells possibly linked to abrupt temperature
reduction at the end of the growing season. More
consolidated detection could increase their role in
dendroecology.
Abstract Cambial activity and wood formation are influenced by environmental factors, primarily climate. During
cell wall formation the lignification is mainly controlled by
temperature. By staining with safranin and astra blue it is
possible to distinguish cell walls richer in lignin (stained in
red) from those richer in cellulose (stained in blue). Here
we show an uncommon phenomenon observed in 41
transverse sections prepared for anatomical studies of
young European black pine (Pinus nigra Arnold) individuals. We detected some layers of incompletely lignified
cells that appear blue in safranin–astra blue-stained sections. Growth rings showing this anatomical feature were
named ‘‘blue rings’’. The aims of this preliminary study
are: (i) to describe the features of this peculiar anatomical
trait, (ii) to enhance its visualization, and (iii) to suggest
possible drivers of its formation. First results indicate the
influence of low air temperature causing a lack of
Communicated by M. Shane.
A. Piermattei (&) C. Urbinati
Dept. di Scienze Agrarie Alimentari e Ambientali,
Università Politecnica delle Marche, Via Brecce Bianche,
60121 Ancona, Italy
e-mail: alma.piermattei@univpm.it
A. Crivellaro M. Carrer
Dept. Territorio e Sistemi AgroForestali, University of Padova,
Viale dell’Università 16, 35020 Legnaro, PD, Italy
lignification in latewood cells. The added values provided
by the identification of ‘‘blue rings’’ within tree-ring series
could be (i) their possible use as pointer year, (ii) cross
dating improvement, and (iii) finer assessment of tree
sensitivity to environmental and climatic factors.
Keywords Pinus nigra Tree rings Pointer year Wood anatomy Lignification Temperature decrease
Introduction
The process of xylem formation is highly dynamic
throughout the lifetime of woody plants (Rossi et al. 2007;
Cuny et al. 2013). It is controlled by internal factors such as
gene expression (Hertzberg et al. 2001; Demura and Fukuda 2007), hormonal signals (Schrader et al. 2003; Aloni
2013) and external limitations such as photoperiod, light
intensity, day and growing season length, precipitation,
temperature, and tree vigour (Wimmer et al. 2000; Gindl
et al. 2001; Schmitt et al. 2003; Camarero et al. 2010; Cuny
et al. 2012). Xylem formation can thus be slowed down
within the growing season, or the relative proportion of
xylem tissues (e.g. relative amount of conductive area) can
be altered, as commonly seen in transverse sections under
the light microscope.
Intra-annual structural variability results mainly from
short-term changes occurring in the course of xylogenesis.
Some of the resulting features are macroscopically visible
on well-sanded increment cores and, therefore, commonly
applied in dendroecological studies. However, more
detailed anatomical analyses allow scientists to resolve
information at the intra-annual scale (Schweingruber et al.
1990; Vaganov et al. 2006). In fact, wood anatomy
investigations were applied to expand the interpretation of
123
Author's personal copy
Trees
such structural variations such as light rings (Gindl 1999;
Wang et al. 2000), frost rings (Glock and Reed 1940;
Glerum and Farrar 1966; LaMarche and Hirschboeck 1984;
Waito et al. 2013) or density fluctuations (Kuo and
McGinnes 1973; Schweingruber 1980; De Micco et al.
2007; De Luis et al. 2007, 2011; Novak et al. 2013).
In conifers, the xylem formation and the tracheid differentiation is commonly divided into four stages: (i) cell
division and post-cambial enlargement; (ii) formation of
multilayered cell walls; (iii) deposition of lignin within the
cell wall polysaccharides matrix; (iv) cell death and
autolysis of the protoplasm. The rate of cell division is
strongly related to climate, mainly determined by temperature thresholds (Oribe et al. 2001; Gričar et al. 2005; Rossi
et al. 2006; Deslauriers et al. 2008; Begum et al. 2013). In
temperate climate the cambial activity starts in spring and
ceases in late summer (Denne and Dodd 1981; Savidge
1996; Lachaud et al. 1999; Wodzicki 2001). At the end of
the growing season the cambium becomes dormant—
indicating no more cell divisions (Gričar et al. 2005).
The deposition of lignin in cell walls is the last phase of
tracheid formation. The cell wall lignification is strongly
influenced by various environmental factors such as temperature (Donaldson 1992; Gindl et al. 2000), day length
(Gindl and Grabner 2000), drought stress (Donaldson
2002), and genetics (Donaldson 1993). Moreover, lignification of latewood tracheids may be considerably delayed
when compared with deposition of secondary wall polysaccharides (Gindl et al. 2000; Gričar et al. 2005). In Picea
abies secondary cell wall lignin content of the terminal
latewood tracheids is positively correlated with September
and October temperatures (Gindl et al. 2000), showing that
long lasting favourable conditions increase the lignin
content. The deposition of cell wall material can continue
during winter or the next spring (Wilson et al. 1966; Nix
and Villiers 1985; Donaldson 1991, 2001; Gindl 2001;
Gričar et al. 2005; De Luis et al. 2007, 2011). For instance
in Pinus radiata from New Zealand, the last formed latewood cells continue to deposit cell wall material until the
following spring, whilst no cell divisions occurred at
cambium level (Donaldson 1991, 1992, 2001). In several
conifer species collected in subalpine (Italy) and boreal
forest (Canada), Rossi et al. (2006) found a relationship
between the occurrence of maximum growth rate and the
timing of lignin deposition: delays in the timing of maximum growth rate in July extended the latewood lignin
deposition toward the winter. In fact, cell wall thickening
and lignification is a cell-specific process and not directly
linked to cambial activity (Gindl et al. 2000).
Recent improvements of wood anatomical techniques
allow the slide preparation process to be more accessible
and less time consuming (Gärtner and Schweingruber
2013; Gärtner et al. 2014). The information available from
123
anatomical analysis increased after the application of
double staining in microsections preparation. The use of a
safranin and astra blue solution stains red the cell walls
richer in lignin and blue those richer in cellulose, allowing
an improved visual separation of the wood anatomical cell
types and a better tracking of the lignification process
(Gerlach 1984; Schweingruber 2007).
Here we present a peculiar anatomical feature observed
in transverse microsections of young black pine (Pinus
nigra Arnold) tree rings. Using a safranin–astra blue
staining we detected layers of cells appearing blue. We
interpreted blue-stained cell walls as cells in which the
lignification process was not completed. We assigned the
name ‘‘blue ring’’ to those tree rings showing layers of bluestained axial tracheids, due to relative lack of lignification.
The aims of this preliminary study are: (i) to describe
the anatomy of this peculiar trait, (ii) to enhance its visualization, and (iii) to suggest possible drivers of its
formation.
We highlighted the ‘‘blue rings’’ in colour pictures at
high magnification and described the laboratory preparation and the staining procedure applied. We also checked
the role of air temperature and precipitation on ‘‘blue ring’’
occurrence. Besides the anatomical relevance their presence, as in the case of frost rings, could be useful for
environmental reconstructions, allowing dating at seasonal
or monthly scale.
Materials and methods
The study site is located on a Karst Plateau of Mount Sirente (2,348 m a.s.l., 42°150 N latitude and 13°600 E longitude) in the Velino-Sirente Regional Natural Park in the
central Apennines, Italy. A beech forest forms the current
treeline at around 1,500 m a.s.l. and above it, along a
W–SW slope, a black pine-encroachment process started
30–40 years ago (Piermattei et al. 2014). Between October
2012 and July 2013 we sampled 210 trees along an altitudinal transect from 1,750 m to the upper limit for living
pines at 2,155 m a.s.l. Since pine removal was not allowed
by the Park we used a 10-cm-long Pressler borer to extract a
single core nearest to the ground from each tree having a
stem basal diameter[4 cm. We collected 140 cores in total
and we selected those having at least 15 tree rings, free of
compression wood and mechanical damages. The following
analyses were conducted on 41 cores. Slides preparation for
anatomical investigation followed standard methods
(Chaffey 2002; Gärtner and Schweingruber 2013). We cut
15–20 lm thin transverse sections with a rotary microtome
(Leica RM2245) and applied the double staining procedure.
Safranin-dye entails 1 g of safranin powder in 100 ml of
distilled water. Astra blue dye contains 0.5 g of astra blue
Author's personal copy
Trees
powder in 100 ml of distilled water, and 2 ml of acetic acid.
The two dyes were mixed (1:1 proportion) and the sections
were soaked into the staining solution for 3–5 min (Gärtner
and Schweingruber 2013). The samples were then washed
with distilled water, dehydrated (50, 75 and 95 % ethanol)
and then permanently mounted on single microscope slides.
All slides were photographed at 409 magnification using a
digital camera integrated to a light microscope (Nikon
Eclipse 80i; Nikon, Tokio, Japan). A blue filter was applied
to increase the contrast between tracheid walls and the cell
lumen. The single digital images were stitched using
the software PTGui (http://www.ptgui.com) to produce a
picture enclosing the entire cross section of every single
core.
Fig. 1 a Close view of a blue ring. The lignin (red stained) is visible
at axial tracheid corners (9400); b the blue ring is visible in doublestained sections (9200); c the same ring in a pure safranin-stained
section (9200); d view of tree-ring sample containing the blue ring as
seen under binocular microscope
Fig. 2 Blue rings occurring on three different samples: a clear example in 2009 from a wide ring (a); a narrow ring (b) and few layers of blue
cells in the earlywood in 1995 (c)
123
Author's personal copy
Trees
abruzzo.it/xIdrografico). After selecting the years with the
highest occurrence of blue rings we compared graphically,
for these years, the daily trend of both precipitation and
temperature at the end of the growing season to the corresponding mean values of the period 1980–2012. Single
anomalous days were detected graphically.
Results
The ‘‘blue ring’’
Fig. 3 Number of blue rings in each year counted in all samples
displayed with sample depth
To discriminate the factors involved in the residual
unlignified cells we investigated tree-ring width, tracheid
lumen area within the unlignified cells and searched
relationships with precipitation and temperature. Treering width measurement at 0.01 mm accuracy was provided by the semi-automatic LINTAB system and software TSAPWin (Rinntech). We measured the tracheid
lumen areas of 10 radial files of cells within the tree
rings featuring the highest occurrence of unlignified cells
using the software ImageJ (ver. 1.46; developed by W.
Rasband, National Institutes of Health, Bethesda, MD,
USA).
Meteorological data were retrieved from the nearest
weather station located near the city of L’Aquila (600 m
a.s.l.), 30 km from the study area (http://www.regione.
Fig. 4 Lignification on three
different samples in the year
2009. The last formed cells are
completely lignified (a, b); the
last formed cells are partially
lignified, only at the margins (c)
123
In some samples we detected growth rings having tracheids
with distinct-stained blue cell walls (Fig. 1). At higher
magnification these cells showed some red-stained areas
located at the cell corners (Fig. 1a, b). For comparison we
stained some transverse sections from the same samples
with safranin alone (Fig. 1c), but no specific structural
feature was detected. Macroscopically, the ‘‘anomalous’’
ring did not show any particular feature compared to previous or following rings (Fig. 1d). We recorded bluestained cell walls within the same growth ring in different
trees (Fig. 2a, b). Only in a few cases we found this type of
cells in earlywood (Fig. 2c).
We defined as a ‘‘blue ring’’ a continuous layer of unlignified axial tracheids occurring either in the earlywood
or in the latewood.
In all the samples the highest number of ‘‘blue ring’’
occurrence is in the latewood of the years 1997, 2007 and
2009 (Fig. 3). Nonetheless, the lignification process is not
homogeneous throughout the growth ring: in some samples
Author's personal copy
Trees
Fig. 5 The averaged tracheid
lumen areas measured in 10
radial files (from earlywood to
latewood) for each of the nine
samples showing a clear blue
ring in 2009. The blue lines
represent the blue cells
the last formed cells are red stained (Fig. 4a, b), whereas in
others only latewood external wall cells are lignified
(Fig. 4c).
Anatomical analysis
Ten trees showed clearly detectable ‘‘blue rings’’ in 2009.
Only in nine of these samples the tracheid lumen areas of
that year were measured and plotted (Fig. 5), since in one
case we could not find 10 measurable radial files due to the
lower quality of the core.
The red lines in all graphs show the number of completely
lignified cells and appear red on the slides (Fig. 5). Similarly,
the blue lines correspond to the incompletely lignified cells
stained blue on the slides. The number of unlignified cells per
file ranges from 6 to 16 and it is correlated with the total
number of cells and the ring width (respectively, r = 0.71
and r = 0.74, p \ 0.05). In all the graphs, cell lumen area is
typically larger at the beginning of the growth ring in correspondence to the earlywood tracheids, and smaller later in
the season when latewood cells are formed. Toward the end
of the growing season lumen area increased abruptly in all
samples and decreased again in the last formed cells. This
structural change occurs in all samples regardless of the
mean lumen area or the total number of cells within the ring,
as clearly visible for trees PN302 and PN328 (Fig. 5). These
Fig. 6 Mean daily temperatures of the years 2009 (a), 2007 (b) and
1997 (c) (black lines) and of the reference period 1980–2012 (red
lines). The shaded area highlights the temperature decrease occurred
in the different years
123
Author's personal copy
Trees
trends permitted also the observation of the effect of intraannual density fluctuations in terms of cell number and
lumen area, occurring especially with earlywood-like cells in
the latewood.
Climatic analysis
We tested the presence of significant relationships between
the occurrence of ‘‘blue rings’’ and temperatures and precipitation. We compared the 3 years with most ‘‘blue
rings’’ and the mean daily temperature for the period
1980–2012, we found in mid-late October (285–295 Julian
days) a negative difference of 9 °C from the reference
values, especially in 2009 (Fig. 6). No relevant results
emerged with precipitation.
Discussion and conclusion
Several studies showed a strong relationship between lignification and environmental factors such as temperature
(Donaldson 1991; Gindl et al. 2000; Schmitt et al. 2003; De
Luis et al. 2007), day length (Gindl and Grabner 2000),
drought stress, and ratio of earlywood and latewood
(Donaldson 2001, 2002). In Norway spruce, at the treeline
the secondary wall lignification of terminal tracheids may
be inhibited by cool climate toward the end of the growing
season (Gindl and Grabner 2000). Lignification of latewood cells may persist long after the radial expansion and
cell wall thickening phases have been completed. In P.
radiata from New Zealand, lignification of latewood cells,
formed in autumn, is usually not completed until the following spring. In this case only a few trees conclude the
lignification of latewood cells prior to the onset of winter
dormancy (Donaldson 1991).
In our samples (Fig. 1a), we observed red-stained cell
wall corners, which are known to be the starting point for
lignification (Evert 2006). This can occur both in broadleaf
(Sutton and Tardif 2005) and in conifer tree species (Donaldson 2001; Rossi et al. 2006). For this reason ‘‘blue ring’’
formation could be due to exceptionally low temperatures in
the late growing season suppressing lignification.
In agreement with Donaldson (1992), we noted that
lignification can be switched on and off in response to
climatic conditions, and temperatures in particular. Nonetheless lignification was not resumed in the following
spring, as if the tree had ‘‘left behind’’ the non-lignified
cells. The scattered cells with blue-stained cell walls, visible in the earlywood are a clear example of this.
The causal relationship between temperature, cambial
activity and the lignification process has been proved in several
species (Barnett 1971; Gindl et al. 2000; Rossi et al. 2007,
2008). The reactivation of cambium produces earlywood-like
123
cells in the latewood and the colder temperatures withdraw the
lignification process. However, due to the remarkable intraannual climate variability in the Mediterranean basin, it is
recommended to continue the monitoring of cambial activity
for several years to assess the influence of climate on wood
formation and to better understand the physiological processes
behind these climate–growth relationships (De Luis et al.
2007; Cuny et al. 2012).
The presence of ‘‘blue rings’’ in P. nigra related to
abrupt temperature decrease at the end of growing season
could be considered an adaptive trait of pioneer species as
for Pinus sylvestris in French temperate forests (Cuny
et al., 2012). This species compared to Abies alba and
Picea abies, features a more ‘‘extensive’’ growth strategy,
but it is exposed to higher risks of injurious climatic events
(Cuny et al. 2012).
Finally the presence and detection of ‘‘blue rings’’ in
tree-ring series could be an added value for dendroecology.
Once their formation and dynamics will be better understood and their occurrence more widely explored in other
species and geographic areas, ‘‘blue rings’’ could be used
as pointer years, as well as missing, false, light and frost
rings (Kaennel and Schweingruber 1995) or also cell size
distribution and density (Schweingruber et al. 1990). Their
presence within tree ring series could improve crossdating
and the analysis of climate sensitivity (Parker and Henoch
1971; Schweingruber 1996).
Author contribution statement Alma Piermattei and Alan Crivellaro performed fieldwork, collected data, conducted analyses and
wrote the manuscript; Marco Carrer and Carlo Urbinati supervised the
analyses and contributed to the preparation and the overall revision of
the manuscript.
Acknowledgments We wish to thank Prof. Malcolm Hughes and
three anonymous reviewers for helpful suggestions and for the text
revision, which significantly improved the manuscript. We also like to
thank: the Sirente-Velino Regional Park staff for sampling authorization and field work assistance; Dr. Bruno Petriccione of the State
Forest Service at L’Aquila for field assistance; the Marche Polytechnic University TreeringLab staff (Dr. Matteo Garbarino) and
collaborators (Dr. Emidia Santini, Marco Altieri) for field and laboratory work. Pinus nigra research at treeline was partially supported
by the Marche Polytechnic University ‘‘2012 RSA n. 7170 project’’
(Forests and Climate Change). Alan Crivellaro received financial
support from the University of Padova (‘‘Assegno di Ricerca Junior’’
CPDr124554/12).
Conflict of interest
of interest.
The authors declare that they have no conflict
References
Aloni R (2013) The role of hormones in controlling vascular
differentiation. In: Fromm J (ed) Cellular aspects of wood
formation. Springer, Berlin, pp 99–139
Barnett JR (1971) Winter activity in the cambium of Pinus radiata.
New Zeal J For Sci 1:208–222
Author's personal copy
Trees
Begum S, Nakaba S, Yamagishi Y, Oribe Y, Funada R (2013)
Regulation of cambial activity in relation to environmental
conditions: understanding the role of temperature in wood
formation of trees. Physiol Plant 147:46–54
Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis
in conifers from continental Mediterranean climates. New Phytol
185:471–480
Chaffey N (2002) Wood formation in trees. Cell and molecular
biology techniques. Taylor and Francis, London
Cuny HE, Rathgeber CBK, Lebourgeois F, Fortin M, Fournier M
(2012) Life strategies in intra-annual dynamics of wood
formation: example of three conifer species in a temperate
forest in north-east France. Tree Physiol 32:612–625
Cuny HE, Rathgeber CBK, Kiessé TS, Hartmann FP, Barbeito I,
Fournier M (2013) Generalized additive models reveal the
intrinsic complexity of wood formation dynamics. J Exp Bot.
doi:10.1093/jxb/ert057
De Luis M, Gričar J, Čufar K, Raventos J (2007) Seasonal dynamics
of wood formation: a comparison between pinning, microcoring
and dendrometer measurements. IAWA Journal 28:389–404
De Luis M, Novak K, Raventos 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, Saurer M, Aronne G, Tognetti R, Cherubini P (2007)
Variations of wood anatomy and d13C within-tree rings of
coastal Pinus pinaster showing intra-annual density fluctuations.
IAWA Journal 28:61–74
Demura T, Fukuda H (2007) Transcriptional regulation in wood
formation. Trends Plant Sci 12(2):64–70
Denne MP, Dodd RS (1981) The environmental control of xylem
differentiation. In: Barnett JR (ed) Xylem cell development.
Kent, Castle House, pp 236–255
Deslauriers A, Rossi S, Anfodillo T, Saracino A (2008) Cambial
phenology, wood formation and temperature thresholds in two
contrasting years at high altitude in southern Italy. Tree Physiol
28:863–887
Donaldson LA (1991) Seasonal changes in lignin distribution during
tracheid development in Pinus radiata D. Don. Wood Sci
Techno 25:15–24
Donaldson LA (1992) Lignin distribution during latewood formation
in Pinus radiata D. Don. IAWA Bulletin 13(4):381–387
Donaldson LA (1993) Lignin distribution in wood from a progeny
trial of genetically selected Pinus radiata D. Don. Wood Sci
Technol 27:391–395
Donaldson LA (2001) Lignification and lignin topochemistry: an
ultrastructural view. Phytochemistry 57:859–873
Donaldson LA (2002) Abnormal lignin distribution in wood from
severely drought stressed Pinus radiata trees. IAWA J
23:161–178
Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues
of the plant body: their structure, function, and development, 3rd
edn. John Wiley & Sons Inc, Hoboken, p 623
Gärtner H, Schweingruber FH (2013) Microscopic preparation
techniques for plant stem analysis. Verlag Dr. Kessel, Remagen-Oberwinter, p 78
Gärtner H, Lucchinetti S, Schweingruber FH (2014) New perspectives for wood anatomical analysis in Dendrosciences: the
GSL1-microtome. Dendrochronologia 32:47–51
Gerlach D (1984) Botanische Mikrotechnik, 3rd edn. Thieme, Stuttgard
Gindl W (1999) Climatic significance of light rings in timberline
spruce, Picea abies, Austrian Alps. Arct Antarct Alp Res
31(3):242–246
Gindl W (2001) Cell-wall lignin content related to tracheid dimensions in drought-sensitive Austrian pine (Pinus nigra). IAWA J
22(2):113–120
Gindl W, Grabner M (2000) Characteristics of spruce [Picea abies
(L.) Karst] latewood formed under abnormally low temperatures.
Holzforschung 54:9–11
Gindl W, Grabner M, Wimmer R (2000) The influence of temperature
on latewood lignin content in treeline Norway spruce compared
with maximum density and ring width. Trees-Struct Funct
14:409–414
Gindl W, Grabner M, Wimmer R (2001) Effects of altitude of
tracheid differentiation and lignification of Norway spruce. Can J
Bot 79:815–821
Glerum C, Farrar JL (1966) Frost ring formation in the stems of some
coniferous species. Can J Bot 44:879–886
Glock WS, Reed EL (1940) Multiple growth layers in the annual
increments of certain trees at Lubbock, Texas. Science (Washington, D.C.) 91:98–99
Gričar J, Čufar K, Oven P, Schmitt U (2005) Differentiation of
terminal latewood tracheids in silver fir during autumn. Ann Bot
95:959–965
Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R,
Blomqvist K, Bhalerao R, Uhlén M, Teeri TT, Lundeberg J,
Sundberg B, Nilsson P, Sandberg G (2001) A transcriptional roadmap
to wood formation. Proc Nat Acad Sci USA 98:14732–14737
Kaennel M, Schweingruber FH (1995) Multilingual glossary of
dendrochronology. Terms and definitions in English, German,
French, Spanish, Italian, Portuguese and Russian. Birmensdorf,
Swiss Federal Institute for Forest, Snow and Landscape
Research, Berne, Stuttgart, Viena, Haupt, p 467
Kuo ML, McGinnes EA (1973) Variation of anatomical structure of
false rings in Eastern red cedar. Wood Sci Technol 5(3):205–210
Lachaud S, Catesson AM, Bonnemain JL (1999) Structure and
functions of the vascular cambium. C R Acad Sci Paris
322:633–650
LaMarche VC, Hirschboeck KK (1984) Frost rings in trees as records
of major volcanic eruptions. Nature 307:121–126
Nix LE, Villiers K (1985) Tracheid differentiation in southern pines
during the dormant season. Wood Fiber Sci 17:397–403
Novak K, De Luı́s M, Raventós J, Čufar K (2013) Climatic signals in
tree-ring widths and wood structure of Pinus halepensis in
contrasted environmental conditions. Trees 27:927–936
Oribe Y, Funada R, Shibagaki M, Kubo T (2001) Cambial reactivation in locally heated stems of the evergreen conifer. Planta
212:684–691
Parker ML, Henoch WES (1971) The use of Engelmann spruce
latewood density for dendrochronological purposes. Can J For
Res 1:90–98
Piermattei A, Garbarino M, Urbinati C (2014) Structural attributes,
tree-ring growth and climate sensitivity of Pinus nigra Arn. at
high altitude: common patterns of a possible treeline shift in the
central Apennines (Italy). Dendrochronologia 32:210–219
Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R,
Borghetti M (2006) Conifers in cold environments synchronize
maximum growth rate of tree-ring formation with day length.
New Phytol 170:301–310
Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of
threshold temperatures for xylogenesis in conifers at high
altitudes. Oecologia 152(1):1–12
Rossi S, Deslauriers A, Gričar J, Seo JW, Rathgeber CBK, Anfodillo
T, Morin H, Levanic T, Oven P, Jalkanen R (2008) Critical
temperatures for xylogenesis in conifers of cold climates. Glob
Ecol Biogeogr 17:696–707
Savidge RA (1996) Xylogenesis, genetic and environmental regulation: a review. IAWA Journal 17:269–310
Schmitt U, Koch G, Grünwald C, Čufar K, Gričar J (2003) Wall
structure of terminal latewood tracheids of healthy and declining
silver fir trees in the Dinaric region, Slovenia. IAWA J
24(1):41–51
123
Author's personal copy
Trees
Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP,
Sandberg G (2003) Polar auxin transport in the wood-forming
tissues of hybrid aspen is under simultaneous control of
developmental and environmental signals. Proc Nat Acad Sci
USA 100:10096–10101
Schweingruber FH (1980) Dichteschwankungen in Jahrringen von
Nadelhölzern in Beziehung zu klimatisch-ökologischen Faktoren, oder das Problem der falschen Jahrringe. Ber Eidg Anst
Forstl Versuchswes 213:1–35
Schweingruber FH (1996) Tree rings and environment dendroecology. Birmendorf, Swiss Federal Institute for Forest, Snow and
Landscape Research. Verlag Paul Haupt, Berne
Schweingruber FH (2007) Wood structure and environment.
Springer-Verlag, Berlin Heidelberg, New York, p 271
Schweingruber FH, Eckstein D, Serre-Bachet F, Braker OU (1990)
Identification, presentation and interpretation of event years
and pointer years in dendrochronology. Dendrochronologia
8:9–38
123
Sutton A, Tardif J (2005) Distribution and anatomical characteristics
of white rings in Populus tremuloides. IAWA J 26(2):221–238
Vaganov EA, Hughes MK, Shashkin AV (2006) Growth dynamics of
conifer tree rings, Images of past and future environments.
Springer, Berlin, Heidelberg, New York, p 350
Waito J, Conciatori F, Tardif JC (2013) Frost rings and white
earlywood rings in Picea mariana trees from the boreal plains,
central Canada. IAWA J 34(1):71–87
Wang L, Payette S, Bégin Y (2000) A quantitative definition of light
rings in black spruce (Picea mariana) at the arctic treeline in
northern Québec, Canada. Arct Antarct Alp Res 32(3):324–330
Wilson BF, Wodzicki TJ, Zahner R (1966) Differentiation of cambial
derivatives: proposed terminology. Forest Sci 12:438–440
Wimmer R, Strumia G, Holawe F (2000) Use of false rings in
Austrian pine to reconstruct early growing season precipitation.
Can J For Res 30:1691–1697
Wodzicki TJ (2001) Natural factors affecting wood structure. Wood
Sci Technol 35:5–26