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. 2011 Dec 30;109(4):721–728. doi: 10.1093/aob/mcr315

Annual increments of juniper dwarf shrubs above the tree line on the central Tibetan Plateau: a useful climatic proxy

Eryuan Liang 1,*, Xiaoming Lu 1, Ping Ren 1, Xiaoxia Li 1, Liping Zhu 1, Dieter Eckstein 2
PMCID: PMC3286282  PMID: 22210848

Abstract

Background and Aims

Dendroclimatology is playing an important role in understanding past climatic changes on the Tibetan Plateau. Forests, however, are mainly confined to the eastern Tibetan Plateau. On the central Tibetan Plateau, in contrast, shrubs and dwarf shrubs need to be studied instead of trees as a source of climate information. The objectives of this study were to check the dendrochronological potential of the dwarf shrub Wilson juniper (Juniperus pingii var. wilsonii) growing from 4740 to 4780 m a.s.l. and to identify the climatic factors controlling its radial growth.

Methods

Forty-three discs from 33 stems of Wilson juniper were sampled near the north-eastern shore of the Nam Co (Heavenly Lake). Cross-dating was performed along two directions of each stem, avoiding the compression-wood side as far as possible. A ring-width chronology was developed after a negative exponential function or a straight line of any slope had been fit to the raw measurements. Then, correlations were calculated between the standard ring-width chronology and monthly climate data recorded by a weather station around 100 km away.

Key Results

Our study has shown high dendrochronological potential of Wilson juniper, based on its longevity (one individual was 324 years old), well-defined growth rings, reliable cross-dating between individuals and distinct climatic signals reflected by the ring-width variability. Unlike dwarf shrubs in the circum-arctic tundra ecosystem which positively responded to above-average temperature in the growing season, moisture turned out to be growth limiting for Wilson juniper, particularly the loss of moisture caused by high maximum temperatures in May–June.

Conclusions

Because of the wide distribution of shrub and dwarf shrub species on the central Tibetan Plateau, an exciting prospect was opened up to extend the presently existing tree-ring networks far up into one of the largest tundra regions of the world.

Keywords: Central Tibetan Plateau, high altitude, Juniperus pingii var. wilsonii, dwarf shrub, cross-dating, dendrochronology, dendroclimatology, growth ring, tree ring, growth-limiting factor, climate proxy

INTRODUCTION

During recent decades, hundreds of tree species world-wide have been employed for dendrochronological studies, thus contributing to a better understanding of climate change over the last 2000 years (Hughes et al., 2011). In contrast, little is known about the dendrochronolgical potential of shrubs and dwarf shrubs in spite of the unique possibility to extend the present tree-ring networks beyond latitudinal and altitudinal tree lines to harsh and treeless environments (Ferguson, 1959; Woodcock and Bradley, 1994; Schweingruber and Dietz, 2001; Cherubini et al., 2003; Schweingruber and Poschlod, 2005; Rayback and Henry, 2006; Schmidt et al., 2006; Au and Tardif, 2007; Bär et al., 2008; Sass-Klaassen et al., 2008; Rozema et al., 2009; Srur and Villalba, 2009; Büntgen and Schweingruber, 2010; Hallinger et al., 2010; Weijers et al., 2010; Blok et al., 2011; Hallinger and Wilmking 2011). This is particularly desirable for the Tibetan Plateau (Xiao et al., 2007; Liang and Eckstein, 2009).

The Tibetan Plateau is one of the key areas for global change studies (Zheng and Yao, 2004), whereby tree-ring-based climate reconstructions are playing an important role in understanding the variability of climate during the past millennia (Shao et al., 2010). Forests are, however, confined to the eastern part of the Tibetan Plateau (Li, 1985), whereas alpine shrubs and dwarf shrubs are widely distributed on the central Tibetan Plateau and thus pose a challenge to expand the network of tree-ring chronologies beyond tree lines (Xiao et al., 2007; Liang and Eckstein, 2009).

The Nam Co (Heavenly Lake, in Tibetan) on the central Tibetan Plateau is located around 4725 m a.s.l. (G. Q. Zhang et al., 2011). Since 2005, a series of studies and continuous observations have been made here to reveal the multifaceted interactions between atmosphere, glaciers, hydrology, permafrost and vegetation (Kang et al., 2007; Ma et al., 2008; Yao et al., 2010; Zhu et al., 2010; Yang et al., 2011). Around the Nam Co, patches of the alpine dwarf shrub Wilson juniper (Juniperus pingii var. wilsonii) are growing. Because of the longevity of junipers in general (Bräuning, 1994; Brown, 1996; Zhang et al., 2003; Liu et al., 2005; Liang et al., 2006b; Liu et al., 2006; Gou et al., 2008; Shao et al., 2010), Wilson juniper may be a promising species to retrieve past climate change in the treeless Tibetan Plateau tundra ecosystem. We hypothesized that it may depend on temperature, as shown by timberline trees and the alpine Rhododendron shrub on the south-eastern Tibetan Plateau (Liang and Eckstein, 2009; Liang et al., 2009, 2010b, 2011).

The objectives of our study, therefore, were to explore the dendrochronological potential of Wilson juniper and to identify the climatic factors controlling its radial growth. This study is part of our ongoing efforts to expand the present tree-ring networks to alpine tundra regions on the Tibetan Plateau.

MATERIALS AND METHODS

Study area and climate

The Nam Co (latitude 30°30′–30°55′, longitude 90°16′–91°03′, 4725 m a.s.l.), at the north foot of the Nyainqentanglha range of the central Tibetan Plateau (Fig. 1A), has a surface area of 2015 km2 (measured in 2004) (Zhu et al., 2010). It is situated in the transition zone from a semi-arid to a sub-humid climate, with a high total solar radiation of around 317 W m−2 (Y. J. Zhang et al., 2011). As recorded by the nearby automatic weather station (AWS) from 2006 to 2008 at the Nam Co Comprehensive Observation and Research Station (30°46·44′N, 90°59·31′E, 4730 m a.s.l.), Institute of Tibetan Plateau Research, Chinese Academy of Sciences, the annual mean temperature is –0·4 °C, with July (mean temperature of 9·5 °C) and January (–8·4 °C) the warmest and coldest months, respectively (Y. J. Zhang et al., 2011). The amount of annual precipitation is around 404·5 mm, of which about 85 % falls from June to October (Y. J. Zhang et al., 2011). The mean wind speed is 3·6 m s−1. At the meteorological station of Baingoin, about 100 km north-west of the Nam Co, the annual total precipitation, measured from 1957 to 2010, varied between 170 and 469 mm with a mean of 312 mm.

Fig. 1.

Fig. 1.

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(A) Study area, sampling sites for Wilson juniper and meteorological stations around the Nam Co; inset, location of the study area within the Tibetan Plateau. (B) Wilson juniper woodland close to the shore of the Nam Co (photo by Dr Haifeng Zhu).

Correlations for the monthly mean temperature and monthly total precipitation between the AWS (close to the Nam Co) and the meteorological station of Baingoin show a consistent variation despite differences in the monthly values. Their correlations are 0·99 for temperature (P < 0·001, n = 51 months) and 0·83 for precipitation (P < 0·001, n = 51) from October 2005 to December 2009, an update of data based on Y. J. Zhang et al. (2011). Thus, the variations in the instrumental records of Baingoin represent the study area close to the Nam Co well and hence could be confidently used for calibrating the growth–climate relationships.

The meteorological data indicate that the continuously rising air temperature resulted in an increasing amount of water from the glaciers melting around the Nam Co (Zhu et al., 2010). This part of the water supply, together with increasing precipitation and declining evaporation, contributed to the enlargement of the surface area of the Nam Co. As shown by the climatic records at Baingoin, the general warming trend is based on the mean minimum temperature rather than on the mean maximum temperature (Fig. 2). At the same time, the annual total precipitation has been increasing highly significantly, whereas the evaporation has been declining.

Fig. 2.

Fig. 2.

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Variation and trend of various climatic variables from 1957 to 2010 at Baingoin (4700 m a.s.l.), whose meteorological records are representative for the Wilson juniper sampling sites (4740–4780 m a.s.l.). Evaporation is measured as that from a standard 20-cm pan.

Shrub sampling

The area around the Nam Co is characterized by wetland close to the lake shore, an alpine Stipa purpurea steppe (up to 5100 m a.s.l.) and an alpine Kobresia spp. meadow (above 5200 m a.s.l.). Patches of woodland around the lake (>20 m distant from the lake shore) are dominated by the evergreen endemic Wilson juniper dwarf shrub (Juniperus pingii var. wilsonii) on sandy and south-facing slopes, always accompanied by Rhodiola fastigiata, Aster vestitus, Delphinium candelabrum, Allium prewalskianum and the like (Chen and Yang, 2011). Wilson juniper, in its prostrate growth form, reaches a height of around 0·5 m and a length of 3 m; the stem diameter at the root collar is from 5 to 20 cm. Its distinct main stems creep along the ground and altogether have a carpet-like aspect (Fig. 1B). Its populations are disturbed by human activities, mainly from cutting firewood. In order to minimize detrimental impacts on this ecologically important vegetation, we collected only discs from stems remaining after being cut several months or several years previously. The gaps in the vegetation caused by the removal of firewood presumably did not change the climatic influence on the remaining shrubs because of their sparse occurrence.

Four patches (30°53′N, 90°52′E, 4740–4780 m a.s.l.), 1–3 km apart, were selected. To our knowledge, it could be the world's highest dendrochronological study site. At each patch, around ten stems were collected close to the root collar. As described by Kolishchuk (1990), an additional five cross-sections were taken at 20 cm intervals along the entire stem of two individuals to assess intraplant growth variability in the axial direction and to detect possibly absent rings. Altogether, 43 discs (ten additional discs were taken along the main stem of two individuals) from 33 stems were sampled and processed.

Growth-ring dating

The samples were processed following standard dendrochronological practices (Cook and Kairiukstis, 1990). All selected prostrate stems had built compression wood on their underside. Based on the year-to-year ring-width variability, we compared the growth pattern of each stem section. Cross-dating was performed in two directions, avoiding the compression-wood side as far as possible (Stokes and Smiley, 1968), and discontinuous and missing rings were carefully dated. Then, ring widths along the two radii were measured with a precision of 0·01 mm, and the quality of cross-dating was checked by the COFECHA program (Holmes, 1983). Based on the cross-dating and the serial sectioning test, applied on two individuals, it became evident that there was no loss of the outer, most recent growth rings proceeding from the tip of the shrub towards the root collar. Finally, 31 out of the 33 stem sections (close to the root collar) from the four sampling sites remained for further analyses.

The raw data of the 62 cross-dated ring-width series from 31 stems close to the root collar fluctuated around a horizontal straight line. Nevertheless, they were transformed into indices by fitting a conservative detrending function (a negative exponential function or a straight line of any slope) using the ARSTAN program (Cook and Kairiukstis, 1990). To reduce the influence of outliers during the assembly of the standard ring-width chronology, all detrended series were averaged using the bi-weight robust mean.

Data analysis

Several descriptive statistics, including mean sensitivity (MS), mean series intercorrelation (RBAR) and expressed population signal (EPS) (Briffa and Jones, 1990), were used to qualify the standard chronology and to compare it with other chronologies. The MS measures the year-to-year variability within a ring-width series, RBAR is the mean correlation coefficient among tree-ring series, and the EPS assesses the degree to which the chronology represents a hypothetical chronology based on an infinite number of cores; an EPS ≥ 0·85 is often taken to identify the reliable part of a tree-ring chronology (Briffa and Jones, 1990).

To determine the climate–tree growth relationships, bootstrapping correlations (Biondi and Waikul, 2004) were calculated between the standard chronology and monthly climate data obtained from the meteorological stations surrounding the Nam Co. Considering the elevation and distance of the meteorological stations from the sampling sites, climatic records from Baingoin (4700 m a.s.l. ), Xainza (4672 m) and Nagqu (4507 m) were employed over a common period from 1960 to 2010. The meteorological stations at Damxung (4200 m) and Lhasa (3648·7 m), located on the southern slope (whereas our study sites were on the northern side) of the Nyainqentanglha range (Fig. 1), were excluded from the analysis. The climate variables included total monthly precipitation, the monthly mean temperature as well as the monthly mean maximum and minimum temperature, monthly relative humidity and standard 20 cm pan evaporation, for a 15 month period from July of the year prior to ring formation to September of the year of ring formation.

RESULTS AND DISCUSSION

Wood anatomical characteristics

Wilson juniper forms distinct annual growth rings (Fig. 3), except in cases of discontinuous rings related to compression wood. The mean width of 10 334 growth rings measured was 0·29 ± 0·15 mm, indicating a strong environmental stress. The growth rings of Wilson juniper were narrower than those of the alpine Rhododendron shrub (0·36 mm; Liang and Eckstein, 2009) and of shrubs in the semi-arid Andes of north-central Chile (0·89–1·06 mm; Barichivich et al., 2009), but wider than those of dwarf shrubs in sub-arctic and arctic regions (Woodcock and Bradley, 1994; Au and Tardif, 2007; Bär et al., 2008; Hallinger et al., 2010).

Fig. 3.

Fig. 3.

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Cross-section of Wilson juniper wood showing well-defined annual growth rings, including one extremely narrow growth ring in 1984 with one row of earlywood cells and one row of latewood cells; scale bar = 200 µm.

Normally, the earlywood consisted of up to around 20 rows of tracheids with a radial diameter from 5 to 22 µm. The latewood tracheids are characterized by an abrupt reduction in lumen area and an increase in cell wall thickness. The latewood was very narrow, consisting of 1–3 rows of tracheids whereby the earlywood/latewood transition was set as soon as a cell wall thickness twice that of the lumen diameter was achieved (Denne, 1989). The narrowest visible growth ring consisted of one row of earlywood cells and one row of latewood cells (Fig. 3).

Cross-dating and chronological statistics

The oldest Wilson juniper individual was 324 years of age (1687–2010), illustrating the high potential for developing long ring-width chronologies at high altitudes on the central Tibetan Plateau, where the physiological thresholds for tree growth have been surpassed. The mean number of growth rings of all samples selected from 31 stems was 167. This is more than reported for the shrub species Hippophae rhamnoides in the river valley (Xiao et al., 2007) and the Rhododendron nivale higher up on the slope (Liang and Eckstein, 2009) of the Tibetan Plateau. Missing rings accounted for 1·3 %, with high percentage values in 1908 (46 %), 1943 (18·5 %), 1984 (27·8 %) and 1995 (22 %). The mean intercorrelation between all 62 ring-width series from 31 stems was 0·60, showing not only a high quality of cross-dating among the four patches but also a high amount of common ring-width variability and hence a strong climatic signal. Unlike dwarf shrub species in the circum-arctic tundra (Bär et al., 2008; Hallinger et al., 2010), the cambium along the stems of Wilson juniper kept active so that there was no problem of missing outer rings in lower stem parts. A large year-to-year variation (average MS = 0·39) in ring width implied that Wilson juniper may be useful for dendroclimatic studies (Figs 3 and 4). All these descriptors together with the occurrence of missing rings suggested that the growth of Wilson juniper is dominated by extremely harsh living conditions.

Fig. 4.

Fig. 4.

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Standard ring-width chronology of Wilson juniper and sample depth (starting with six ring-width series from three stems). The ring-width indices and their 10-year moving average, and the sample depth are indicated. The year (1766) with EPS ≥ 0·85 is marked by a vertical dashed line.

The MS of the standard chronology was around 0·22, which is higher than that of the temperature-sensitive alpine Rhododendron shrub (Liang and Eckstein, 2009) and timberline fir (Liang et al., 2009) on the south-eastern Tibetan Plateau and lower than that of Qilian juniper [Juniperus (Sabina) prewalskii] in the semi-arid and arid areas of the north-eastern Tibetan Plateau (Zhang et al., 2003; Shao et al., 2005; Liu et al., 2006; Liang et al., 2010a). Over the common period, 1848–2010, the standard ring-width chronology has an RBAR of 0·21 and an EPS = 0·88 (16 stems included); since 1766, when 11 stems were included, the EPS was ≥ 0·85 (Fig. 4).

Climate–growth relationships

The Wilson juniper ring width variability is positively correlated with precipitation/relative air humidity and negatively correlated with the mean maximum temperature/pan evaporation in May and June of the current year, all recorded at Baingoin (similar results were obtained using the climatic records registered at Xainza and Nagqu) (Fig. 5); even the moisture/temperature conditions during the previous growing season provided some evidence. Such climatic responses were also reported for Qilian juniper at dry sites on the north-eastern Tibetan Plateau (Zhang et al., 2003; Shao et al., 2005; Liang et al., 2006a; Liu et al., 2006; Yang et al., 2010) and for Juniperus (Sabina) tibetica on the eastern Tibetan Plateau (Bräuning, 1994; Gou et al., 2008; Zhu et al., 2011). Apparently, a drought can be caused not only by little or no rainfall (the long-term average precipitation in May and June is 70·4 mm at Baingoin) but also by a high evaporation (245·1 mm on average), strong radiation and a high maximum temperature (on average 12·1 °C for May–June at Baingoin). The occurrence and distribution of Wilson juniper dwarf shrubs around the Nam Co may partly depend on the moist growing condition due to the so-called ‘lake effect’ (Kropacek et al., 2010).

Fig. 5.

Fig. 5.

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Correlation between the ring-width chronology of Wilson juniper and various climatic variables from July of the previous year to September of the current year; months with significant differences (P < 0·05) are indicated by an asterisk.

In order to determine the relevance of moisture vs. temperature in their combined effect on growth we graphically compared the Wilson juniper ring-width chronology with various May–June climatic variables (maximum temperature and evaporation as well as May–June precipitation and relative air humidity) at Baingoin (Fig. 6). In addition, we applied the coefficient of coincidence (cc) (Eckstein and Bauch, 1969) which measures the year-to-year agreement between two time series better than the simple correlation coefficient (r). The year-to-year variations (cc) of the chronology and the amount of rainfall coincided in 72 % of the years (at the 99·9 % confidence level). Hence, growth responded immediately, i.e. mostly within the same year, to changes in the amount of water availability, whereas temperature acted less directly (cc = 62·2 %; at the 95 % confidence level). The correlation coefficients (r), in contrast, were +0·43 for rainfall and –0·52 for temperature.

Fig. 6.

Fig. 6.

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Wilson juniper ring-width chronology, 1957–2010, compared with various normalized May–June climate variables. (A) Maximum temperature and evaporation; note that the two curves are presented as inverse values. (B) Precipitation and relative air humidity at Baingoin.

Conclusions

Our study has proved the high dendrochronological potential for Wilson juniper around the Nam Co on the central Tibetan Plateau, based on its longevity, well-defined growth rings, reliable cross-dating between different individuals, and distinct climatic signals reflected by the ring-width variability. To our knowledge, this could be the world's highest dendrochronological study. Due to the wide distribution of shrub and dwarf shrub species on the central Tibetan Plateau, our study does show an exciting prospect for extending the presently existing tree-ring network far up into one of the largest tundra regions of the world. To date, most growth-ring chronologies from dwarf shrubs are <100 years. We developed a 245 year (EPS ≥ 0·85) ring-width chronology of the alpine Wilson juniper dwarf shrub that has not been used before in dendroclimatology. The variability of its growth-ring widths clearly reflects that dry/hot conditions in May and June cause moisture stress which becomes the main limiting factor for Wilson juniper's growth. This is different from shrubs and dwarf shrubs in the circum-arctic tundra where the growth is limited by low temperature during the growing season and where the shrub expansion and growth increase in the recent decades is commonly attributed to climate warming (Rozema et al., 2009; Forbes et al., 2010; Hallinger et al., 2010; Blok et al., 2011). This difference in the climate–growth relationship may be due to the fact that there is a stronger solar radiation and evaporation as well as less precipitation on the central Tibetan Plateau as compared with the circum-arctic tundra ecosystems. As a result, warming without an increase in precipitation, in particular in the early growing season, will have a deteriorative influence on Wilson juniper's growth on the central Tibetan Plateau. However, if the present environmental conditions, characterized by a low evaporation rate, persist, the distribution range of Wilson juniper may expand.

ACKNOWLEDGEMENTS

This work was supported by the National Natural Science Foundation of China (41130529, 40871097), the ‘Strategic Priority Research Program – Climate Change: Carbon Budget and Relevant Issues’ of the Chinese Academy of Sciences (XDA05090311), and the Special Scientific Research Project for Public Interest (GYHY201106013-2-2). We thank Dr Haifeng Zhu for collecting samples and Mr Peter Prislan for preparing wood cross-sections. We appreciate the great support (including climatic data) from the Nam Co Monitoring and Research Station for Multisphere Interactions, Chinese Academy of Sciences.

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