1. science
2. weather

The alpine dwarf shrub Cassiope fastigiata
in the Himalayas: does it reflect site-specific
climatic signals in its annual growth rings?
Eryuan Liang, Wenwen Liu, Ping Ren,
Binod Dawadi & Dieter Eckstein
Trees
Structure and Function
ISSN 0931-1890
Volume 29
Number 1
Trees (2015) 29:79-86
DOI 10.1007/s00468-014-1128-5
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Trees (2015) 29:79–86
DOI 10.1007/s00468-014-1128-5
ORIGINAL PAPER
The alpine dwarf shrub Cassiope fastigiata in the Himalayas: does
it reflect site-specific climatic signals in its annual growth rings?
Eryuan Liang • Wenwen Liu • Ping Ren
Binod Dawadi • Dieter Eckstein
•
Received: 2 May 2014 / Revised: 17 October 2014 / Accepted: 7 November 2014 / Published online: 23 November 2014
Ó Springer-Verlag Berlin Heidelberg 2014
Abstract
Key message This is the first time to show that alpine
Cassiope fastigiata shrubs form distinct annual growth
rings and record climatic signals.
Abstract Cassiope species grow as dwarf shrubs at high
latitudes and high elevations. Unlike in the High Arctic, not
much is known about their age and growth on the Tibetan
Plateau and in the Himalayas. There, Cassiope fastigiata
could potentially serve as indicator species for climate
change. The objective of our study, therefore, was to
investigate its dendroecological potential. For this purpose,
20 shoots were collected both on the south-eastern Tibetan
Plateau (site 1) and in the central Himalayas (site 2). Crosssections of 8–10 lm in thickness were cut and the widths
of the clearly distinguishable growth rings were measured.
No missing outer rings were detected at the shoot base
when serial sectioning was applied. Of the 40 shoots, 19 at
site 1 and 10 at site 2 showed similar growth patterns. The
remaining shoots were excluded from further analyses. C.
fastigiata formed up to 30 annual growth rings whose
width varied from 13 to 150 lm. Its growth at both sites
was positively associated with temperature in late winter/
early spring, and at site 2 additionally with precipitation in
late autumn of the preceding year and spring of the current
year. Our study confirmed that C. fastigiata forms distinct
annual growth rings. The growth response to precipitation
at site 1 and the lack thereof at site 2 result from differences in hydrology between the south-eastern Tibetan
Plateau and the central Himalayas.
Keywords Dendroecology Growth-ring formation High altitude Treeline Tibetan Plateau Central
Himalayas
Introduction
Communicated by A. Braeuning.
E. Liang (&) W. Liu P. Ren B. Dawadi
Key Laboratory of Alpine Ecology and Biodiversity, Key
Laboratory of Tibetan Environment Changes and Land Surface
Processes, Institute of Tibetan Plateau Research, Chinese
Academy of Sciences, Beijing 100101, China
e-mail: [email protected]
W. Liu P. Ren
University of Chinese Academy of Science, Beijing 100049,
China
B. Dawadi
Central Department of Hydrology and Meteorology, Tribhuvan
University, Kathmandu, Nepal
D. Eckstein
Centre of Wood Sciences, Wood Biology, University of
Hamburg, Hamburg, Germany
Shrubs and dwarf shrubs have wider ecological amplitudes
than trees and thus are suitable bioindicators for extreme
environments (Schweingruber and Dietz 2001). Moreover,
shrubs and dwarf shrubs offer a unique opportunity to
extend the existing dendrochronological networks into
treeless plant communities (e.g., Woodcock and Bradley
1994; Forbes et al. 2010; Hallinger et al. 2010; Liang et al.
2012; Camarero et al. 2013; Schweingruber et al. 2013;
Zimowski et al. 2014) and to track the influence of climate
change along vegetation-range margins (Myers-Smith et al.
2011; Elmendorf et al. 2012; Pearson et al. 2013).
The genus Cassiope (Ericaceae) consists of about 20
evergreen dwarf shrub species, growing in harsh environments (Fang et al. 2005). To date, dendroecological studies
have mainly been focussed on C. tetragona in the High
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80
Arctic. Various annual growth parameters of this species,
such as the annual average leaf length and the annual shoot
increment, have been used as high-resolution, arctic-wide
climate proxy records (e.g. Callaghan et al. 1989; Rayback
and Henry 2005; Rozema et al. 2009; Weijers et al. 2010,
2013). Although some evidence for a periodic growth in
girth of C. tetragona shoots was noted (Rayback et al.
2012a; Schweingruber et al. 2013; Weijers et al. 2013), no
ring-width chronology of this species has been developed.
From Cassiope species at alpine regions, other than C.
mertensiana (Rayback et al. 2012b), not much is known as
to their longevity and growth.
In this study, we focus on the alpine species C. fastigiata, widespread on the Tibetan Plateau and in the Himalayas (Fang et al. 2005). It often grows above the treeline.
The objectives of this study were to develop ring-width
chronologies and to find the climate drivers for its growth.
Recent studies on, e.g., Hippophae rhamnoides, Juniperus
pingii var. wilsonii and Rhododendron spp. showed that
alpine shrubs recorded climatic signals in their growth
rings similar to those of close-by timberline trees (Xiao
et al. 2007; Liang and Eckstein 2009; Liang et al. 2012; Li
et al. 2013). Similar to tree growth on the south-eastern
Tibetan Plateau (Liang et al. 2009) and in the central
Himalayas (Liang et al. 2014), the growth of C. fastigiata
may respond differently to the differing climatic conditions
at both sites.
Materials and methods
Dwarf shrub species studied, sampling sites
and regional climate
C. fastigiata grows from 3,000 to 4,500 m a.s.l. in Yunnan
and Tibet, China, and along the southern Himalayas such
as in Pakistan, India, Nepal and Bhutan. It is an evergreen
dwarf shrub of up to 30 cm high, preferring open and
Trees (2015) 29:79–86
sunny sites. Its leaves and bell-like flowers are similar to
those of the circumarctic dwarf shrub C. tetragona. The
thick, lance-like, leaves are up to 5 mm long, and several
shoots are usually clustered together (Fig. 1).
We selected two sampling sites, approximately 800 km
apart, representing the northern and southern distribution
margins of C. fastigiata (Fig. 2). The growing period was
assumed to last from May to August/September. Site 1 is
located on the south-eastern Tibetan Plateau where C.
fastigiata grows just above the Juniperus saltuaria treeline
(4,400 m a.s.l.) on a south-facing slope covered by Rhododendron shrubs (up to 3 m high) up to 70 % and by C.
fastigiata up to 10 %; the soil is podzolic. Close to site 1,
an automatic weather station (AWS) is in operation since
November 2006 (Liu et al. 2011). From 2007 to 2013, the
annual mean temperature ranged from -0.2 to 0.9 °C. The
mean temperature for the coldest (January) and warmest
month (July) were -8.0 ± 1.7 and 7.9 ± 0.5 °C, respectively. In extreme cases, temperature may drop down to 18 °C. The mean annual sum of precipitation amounted to
957 mm, of which 62 % fell during the monsoon season
(June–September). Snowfall mainly occurred between
November and May.
Site 2 is located 10 km south of the Mt. Everest in the
Khumbu Valley of the central Himalayas and 150 km
northeast of Kathmandu (1,369 m a.s.l.). There, C. fastigiata occurs just above the Betula utilis treeline (4,150 m
a.s.l.) [close to site SKB1 in Liang et al. (2014)] in an open
terrain on a northwest-facing slope. Here, up to 30 cm high
Rhododendron anthopogon and C. fastigiata, which together cover 20–30 % of the area, are dominant on a thin
layer of rocky soil. As recorded by the high-altitude Pyramid meteorological station (5,050 m a.s.l.) (http://evk2.
isac.cnr.it/) in the Khumbu Valley, the average annual sum
of precipitation was 343 mm from 2005 to 2008. The
wettest month was July (103 mm); very little precipitation
(13 mm) fell from December to April. Based on a lapse
rate of 0.6 °C/100 m, the mean temperatures in the coldest
Fig. 1 Landscape with C. fastigiata dwarf shrubs above the Juniperus saltuaria treeline (4,400 m a.s.l.) on the south-eastern Tibetan Plateau
during midsummer; the sampling site is indicated by a vertical arrow (a). C. fastigiata growing in clusters (b)
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Fig. 2 Location of the study
area in a larger context of the
Tibetan Plateau (inset) and of
the two study sites (yellow
triangles) of C. fastigiata on the
south-eastern Tibetan Plateau
(site 1) and in the central
Himalayas (close to Mt.
Everest) (site 2) as well as of the
nearby meteorological station in
Nyingchi (3) (black square) and
one grid dataset from CRU TS
3.0 at 0.5° spatial resolution (4)
(black square)
(January) and the warmest month (July) were calculated to
be -3.2 and 10.1 °C at the sampling site, respectively.
Precipitation in the form of snow is common except for the
monsoon season.
The main differences between sites 1 and 2 are the
exposition, south facing vs. north facing, and the annual
sum of precipitation, 957 vs. 343 mm.
From each site, 20 shoots, as thick as possible, with
diameters from 0.6 to 3.0 mm were sampled with a distance of 2–3 m in-between them to avoid sampling of the
same genotype twice. Samples were collected in 2012 in
the central Himalayas and in 2010 and 2012 on the southeastern Tibetan Plateau.
2010). For this purpose, cross-sections were taken every
2–3 cm along the shoots.
The ring widths were measured based on digital images
along two radii per cross-section under a reflected light
microscope using the program ImageJ (Schneider et al.
2012) with a precision of 1 lm. After visual cross-dating,
these two series of measurements were averaged to one
series for each shoot. The correlation of each individual
ring-width series with the site chronology (made from all
individual ring-width series of a site except the candidate
growth-ring series to be tested) was calculated using the
COFECHA program (Holmes 1983); poorly correlating
ring-width series (r \ 0.40) were eliminated from further
analysis.
Wood anatomy and cross-dating
Data analysis
A 5-mm long piece of each shoot was taken from close to
soil level and embedded in paraffin. Then, 8–10 lm thick
cross-sections were cut using a sledge microtome and
stained with 3 % safranin (Merck, Darmstadt, Germany)
for enhancing the contrast. The relevance of missing outer
rings close to the soil level, occurring at various distributional margins of woody plant species, has recently been
described by Wilmking et al. (2012). The presence of
missing (outer) rings can be problematic for the establishment of shrub-ring chronologies, because of cross-dating difficulties. To get an impression from the growth
variations along the shoots, three individuals from site 1
were examined using the so-called serial sectioning technique (Kolishchuk 1990; Ba¨r et al. 2007; Hallinger et al.
The mean correlation among all shoots from a site (rbar)
was calculated as a common measure for the similarity
within a group of growth-ring series. The mean sensitivity,
measuring the year-to-year variability within a ring-width
series, was also calculated. The mean autocorrelation of a
ring-width series measures how much the ring width in
year n is correlated with the ring width in year n-1 (Fritts
1976).
The two site chronologies assembled were correlated
with monthly meteorological data for temperature and
precipitation. For site 1, the meteorological data were
obtained from the station in Nyingchi (3,000 m a.s.l.). For
site 2, the data from one nearby grid point (27.75°N,
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86.75°E) of the CRU TS 3.0 (Climatic Research Unit,
Time Series Datasets, version 3.0) were used (Mitchell and
Jones 2005). The CRU data correlate well with the local
meteorological measurements (Liang et al. 2014).
The similarity between the site chronologies and the
significant, seasonalized climatic variables was described
by the simple correlation coefficient (r), measuring the
medium-term coherence, and the coefficient of coincidence
(G) (‘Gleichla¨ufigkeit’) for the year-to-year agreement
(Eckstein and Bauch 1969).
Results and discussion
four shoots were eliminated because of abnormal growth
patterns of which the causes remained unknown.
The synchronism of the variation in the ring-width series
from different shoots suggested the influence of an external
factor, very likely of climate, on the annual growth. The
average correlation coefficient between the tree-ring series
of the shoots was 0.68 at site 1 and 0.54 at site 2, thus
confirming the reliability of cross-dating. The average firstorder autocorrelation of the individual ring-width series per
site (calculated from the raw measurements) was low (0.09
and 0.16, respectively), thus making a trend elimination
redundant. The mean sensitivity was 0.44 at both sites
which is evidence for high year-to-year differences in ring
widths.
Cross-dating and chronology development
Wood anatomy and age of C. fastigiata
The outer growth rings throughout each C. fastigiata shoot
were obviously formed at the same time, as shown by ring
widths measured on seven cross-sections taken along one
shoot (Fig. 3). The results obtained for the other two plants
were identical. The same holds for rhododendron and
juniper shrubs on the Tibetan Plateau (Liang and Eckstein
2009; Liang et al. 2012). Therefore, we concluded that
cross-sections taken close to the soil level contain the
maximum possible number of growth rings.
Cross-dating between tree-ring series was facilitated by
the occurrence of narrow (and missing) rings in 2000 and
2004 on the south-eastern Tibetan Plateau and in 2002,
2005 and 2008 in the central Himalayas (Fig. 6). Out of a
total of 20 shoots per site, 19 and 10 shoots could be crossdated for site 1 and 2, respectively. Seven shoots were
excluded because their tree-ring series correlated poorly
with the site chronologies. Moreover, the tree-ring series of
Annual ring width (μm)
100
80
ο
60
40
20
1998
2000
2002
2004
2006
2008
2010
Year
Fig. 3 Ring-width series obtained from serial sectioning (seven
cross-sections) from soil level up to the top of one shoot of C.
fastigiata, sampled in 2010; accordingly, the uppermost cross-section
contains only one growth ring marked by a small circle on the y-axis
on the right-hand side
123
Cross-sections of C. fastigiata shoots show a diffuse-porous to semi ring-porous growth-ring structure leading to
clear ring boundaries (Fig. 4). The latter is further highlighted by nearly vessel-free tissue consisting of thickwalled fibers. The ring widths ranged from 13 to 150 lm,
and their average was 51.8 ± 19.8 lm at site 1 and
64.4 ± 25.7 lm at site 2. In some shoots, a few growth
rings were completely missing but their position could be
identified through cross-dating with ring series from different shoots. In the time series, missing rings were given a
width of zero.
The ring width of C. fastigiata is much narrower than of
several alpine and arctic shrub species under cold environments, such as Empetrum hermaphroditum with ring
widths from 70 to 110 lm, depending on topographical
aspects (Ba¨r et al. 2007), and Juniperus nana with ring
widths from 117 to 321 lm along an elevation gradient
from 770 to 1,100 m a.s.l. (Hallinger et al. 2010), both in
Scandinavia. The mean ring width of C. fastigiata is also
narrower than those of Salix pulchra (210 lm) and Betula
nana (110 lm) (Blok et al. 2011) in the north-eastern
Siberian tundra. According to Larcher (1987), organisms in
harsh environments are not designed to maximize their
biomass, but to stabilize at least a minimum of life functions for their survival. Moreover, cell physiological processes and metabolic activities of plants have been found to
be more resource demanding in extreme ecosystems than
under temperate conditions (Lu¨tz et al. 2012), likely
resulting in the extremely narrow growth rings of highelevation C. fastigiata.
The C. fastigiata shoots reached an age of around
30 years. More fieldwork is needed to locate older populations. Based on the annual shoot elongation, C. tetragona
in the High Arctic can reach a life span of more than
100 years (Rayback and Henry 2005; Rozema et al. 2009;
Weijers et al. 2010, 2013; Rayback et al. 2012a). Genets of
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Trees (2015) 29:79–86
83
Fig. 4 Cross-sections (a, b) from a shoot of C. fastigiata, showing clear annual growth rings; scale bar length 200 lm
0.6
0.6
(A)
*
*
0.4
0.4
0.2
0.2
0.0
0.0
Correlation coefficient
pS
pO
pN
pD
J
F
M
A
M
J
J
A
pS
-0.2
-0.2
-0.4
-0.4
-0.6
-0.6
0.6
pO
pN
pD
0.6
(B)
*
0.4
0.4
0.2
0.2
0.0
J
F
M
A
M
J
J
A
*
*
*
0.0
pS
pO
pN
pD
J
F
M
A
M
J
J
A
pS
-0.2
-0.2
-0.4
-0.4
-0.6
pO
pN
pD
J
F
M
A
M
J
J
A
-0.6
pS pO
pN pD
J
F
M
A
M
J
J
A
Monthly mean maximum temperature
Monthly mean minimum temperature
Monthly mean temperature
pS pO pN pD
J
F
M
A
M
J
J
A
Month
Monthly sum of precipitation
Fig. 5 Correlation between the ring-width chronologies of C. fastigiata and various climatic variables from September of the previous year to
August of the current year at site 1 (a) and site 2 (b); asterisk represents the significance at the p \ 0.05 level
C. tetragona may live even up to several hundred years
(Havstro¨m et al. 1993; Johnstone and Henry 1997). We
deem it likely that C. fastigiata is able to reach similar
ages.
Climate/growth association
The growth of C. fastigiata at both sites is positively
associated with temperature in late winter/early spring
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84
3
(A)
2
Chronology at Site 1
Mean monthly minimum temperature
from Feb to Mar
20
15
1
10
0
-1
5
0
-3
1985
3
(B)
1990
1995
2000
2005
2010
Chronology at Site 2
Sum of precipitation in prior Sep-Dec
15
2
Sample depth
-2
Z score
Fig. 6 Graphical comparison
between the two C. fastigiata
site chronologies and
seasonalized climate records.
a at site 1, annual ring width is
associated with February to
March temperature (r = 0.54,
p \ 0.01; G = 68 %, p = 0.5);
b at site 2, annual ring width is
associated with sum of
precipitation from September to
December in the previous
autumn (r = 0.60, p \ 0.001;
G = 88 %, p = 0.01). All
variables were transformed to
Z-scores to facilitate visual
comparison. The dotted lines
(smallest dots) indicate sample
depth
Trees (2015) 29:79–86
10
1
0
5
-1
-2
0
-3
1985
1990
1995
2000
2005
2010
Year
(February–March) (Figs. 5, 6a). According to Ko¨rner
(2003), winter temperatures are critical for the distribution
of plant species. This holds also true for most tree species
at high elevations, showing a strong positive association to
temperature in late winter/early spring (e.g., Oberhuber
2004; Zhu et al. 2008; Liang et al. 2009). Low temperatures in late winter/early spring may damage the leaf buds
of C. fastigiata and hence result in narrow rings. Its growth,
however, does not show any significant association with
summer temperature, unlike C. tetragona in the High
Arctic (Rayback and Henry 2005; Weijers et al. 2010).
Other than with temperature, radial growth of C. fastigiata at sites 1 and 2 responded differently to precipitation. At site 1, its growth did not correlate with
precipitation, similar as Abies georgei var. smithii at humid
timberlines (Liang et al. 2009) in the same area. At site 2,
however, it showed significantly positive correlations with
precipitation in the autumn prior to growth (September–
December) (Figs. 5, 6b) and in the current spring (April–
May). From September to December, precipitation falls as
snow thus preventing frost damage and increasing soil
moisture availability in the early growing season. April–
May precipitation amounted to only 17 mm from 2005 to
2008, as recorded at the Pyramid station (5,050 m a.s.l.);
our sampling site in the rain shadow may receive even less
precipitation. This explains the correlation found with
April–May precipitation at site 2. Such climate response is
similar as of timberline Betula utilis in the central Himalayas whose growth is strongly limited by precipitation in
spring (Liang et al. 2014). The same situation is valid for
123
high-elevation (up to 4,800 m a.s.l.) juniper shrubs on the
central Tibetan Plateau (Liang et al. 2012).
Conclusions
C. fastigiata, in spite of its extremely slow growth, forms
distinct annual growth rings, and the selected ring-width
series cross-date well, indicating its dendroecological
potential. Its annual radial growth reflects a temperature
signal in late winter/early spring at both sites. Precipitation
is the main growth-controlling factor in the central Himalayas, but not on the south-eastern Tibetan Plateau. In spite
of its markedly different growth form as compared to trees,
C. fastigiata partly captures the same year-to-year macroclimatic variations as nearby timberline trees.
Author contribution statement Eryuan Liang: funding, experimental design, fieldwork, data analysis, development and writing of
the manuscript, review and discussion of the manuscript. Wenwen
Liu: processing samples and data analysis, review and discussion of
the manuscript. Ping Ren: processing samples and data analysis,
review and discussion of the manuscript. Binod Dawadi: fieldwork,
review and discussion of the manuscript. Dieter Eckstein: data analysis, writing of the manuscript, review and discussion of the
manuscript.
Acknowledgments This work was supported by the National Natural Science Foundation of China (41471158, 41130529) and the
National Basic Research Program of China (2012FY111400). We
appreciate the great support from the Southeast Tibet Station for
Alpine Environment, Observation and Research, Chinese Academy of
Sciences. We thank the Department of National Parks and Wildlife
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Trees (2015) 29:79–86
Conservation, the government of Nepal for granting permission to
carry out this research in the Sagarmatha national park, the Ev-K2CNR Pyramid Meteorological Station (5,050 m a.s.l.) for sharing
climatic data, and two reviewers for their valuable comments.
Conflict of interest
of interest.
The authors declare that they have no conflict
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