Climatic forcing of xylem formation in Qilian juniper on the northeastern Tibetan Plateau
Cambial activity of ~100-year-old Qilian juniper trees initiated before the middle of May at an elevation of 3200 m a.s.l.; June and July were the main stem radial increment period. Around the middle of August, all xylem cell differentiation periods are completed. Precipitation or relative humidity is the main limiting factor for tree radial growth on the northeastern Tibetan Plateau.
Previous studies have found that annual tree-ring width series of Qilian juniper (Sabina przewalskii Kom.) in the northeastern Tibetan Plateau (TP) are mostly moisture controlled, irrespective of site elevation. Knowing precisely the cambial growth dynamics during a vegetation period can lead to a better understanding of the climatic factors driving regional tree growth patterns. We observed wood formation with micro-cores taken at weekly intervals from late April to early October 2013, and monitored daily stem radial changes with high-resolution electronic point dendrometers in 30-min intervals. Dormant cambium contained 5–6 cell layers in the cambium zone. Cambial activity initiated before the middle of May in all the monitored trees. About three quarters of the total cell production or radial growth formed during June and July. Lignification of secondary walls of new xylem cells continued from end of May to middle of August. After the middle of August, the cambium entered into the inactive period. Dendrometer measurements confirmed that June and July were the main stem radial increment period. Nonparametric Kendall’s Tau correlations indicate that daily relative humidity and precipitation significantly influence stem growth in May. No obvious relationships were detected in June. In July, significant negative influences of maximum temperature and positive effects of relative humidity prevailed. Overall, growing season precipitation or associated relative humidity is the limiting factor for tree stem radial increments on the intra-annual scale. Our results present a thorough understanding of Qilian juniper xylogenesis and its climate forcing within the whole growing season on the northeastern TP.
KeywordsMicro-coring method Dendrometer measurements Climate factors Sabina przewalskii Kom Northeastern Tibetan Plateau
During the past decades, dendroclimatology has been developed thoroughly, aiming to establish long-term relationships between tree growth and climatic variables by examining correlations at monthly, seasonal, and annual resolution, and to reconstruct climate series predating meteorological periods (Fritts 1976). Based on calibration functions derived from seasonal averages of climate data, millennium-long records of climate change are meanwhile available for different regions (Briffa et al. 2013; Büntgen et al. 2011; Cook et al. 2010). Due to its location at the margins of the Asian summer monsoon region and to its ability to grow in climatic sensitive arid and semi-arid regions, Qilian juniper (Sabina przewalskii Kom.) plays a prominent role for the reconstruction of climate history in the northeastern Tibetan Plateau (TP) (Gou et al. 2014; Qin et al. 2013; Sheppard et al. 2004; Yang et al. 2014).
However, correlation functions between monthly means of climatic variables and annual tree-ring records do not consider the radial increment dynamics on an intra-annual scale. For a given tree, growth rates may vary considerably from year-to-year due to climate fluctuations. However, contrasting climatic conditions can yield similar amounts of annual growth depending on the timing of the climatic events during the growing season. On a yearly basis, the same amount of growth can be achieved by a faster growth rate or by a longer growing period. Moreover, the climate/growth relationships on an inter-annual time scale can sometimes be inconsistent with the climate/growth association on an intra-annual scale (Seo et al. 2011). Therefore, more species-specific and site-specific highly resolved data on radial increment dynamics are required both to better understand the association between tree growth processes and their responses to climate variability.
On the other hand, intra-annual cambium dynamics is one of the four emerging new topics in dendroclimatology and dendroecology (Eckstein and Schweingruber 2009). Detailed investigations of tree radial growth throughout the growing season are becoming more frequent in tree-ring studies in different climatic zones, especially in the Europe (Deslauriers et al. 2008; Gruber et al. 2010; King et al. 2013) and North America (Lupi et al. 2012; Rossi et al. 2011; Turcotte et al. 2009). Herein, high-resolution dendrometer measurements have been used to detect the seasonal growth patterns with a high level of precision (Biondi and Hartsough 2010; Deslauriers et al. 2007; Vitas 2011). Obviously, dendrometers have the advantage of providing continuous time series of high-resolution stem diameter variations, indicating water-related stem size fluctuations, cambial cell division, and enlargement of newly formed xylem and phloem. However, since dendrometers measure stem radius or circumference changes rather than wood formation, it is difficult to distinguish between true wood formation and hydrological swelling and shrinking (Mäkinen et al. 2003). Alternatively, wood formation can also be monitored by directly extracting wood samples at short time intervals (Rossi et al. 2008a, b, c; Saderi et al. 2013; Lenz et al. 2013). With the micro-coring technique (Bäucker et al. 1998), small wood cores are removed from a stem using an injection needle or a cutting tube. The state of wood formation at the time of coring can be determined microscopically from the cores without causing severe physiological impact on the tree. Currently, micro-coring represents one of the most reliable techniques for detailed monitoring of wood formation (Mäkinen et al. 2008; Oladi et al. 2011; Rossi et al. 2011). Despite that small increment cores are proved useful in assessing actual xylem formation, the method is laborious (Mäkinen et al. 2003) and requires sampling at short intervals during the main growing season, restricting its applicability in remote study areas. Consequently, dendrometers and micro-coring methods were used in combination to detect the cambium dynamics and wood formation (Bräuning et al. 2009; Camarero et al. 2010; Krepkowski et al. 2013). Studies like this have provided broad knowledge about which processes in the growing tree control cell production and which determine the characteristics of the produced cells, and thus are important for realizing tree growth–climate relationships on a finer time scale.
In China, however, limited researches using either the micro-coring method (Li et al. 2013; Liang et al. 2009; Ren et al. 2015) or dendrometer measurements (Jiang et al. 2014; Wang et al. 2012, 2014) to analyze xylem formation on the intra-annual scale have been conducted. Considering the vast diversity in tree species and forest ecosystems in China’s mountain areas stretching over different climatic zones, there exists large demand for further research to provide a comprehensive picture of tree growth dynamics in high altitude regions under different climate regimes.
The aim of this study is to monitor juniper tree radial formation by combining high-resolution dendrometer measurements and wood anatomy studies and to detect relationships with cambium activity-controlling climate factors in the semi-arid northeastern TP region.
Materials and methods
The study site is located at the Sidalong Forestry Station of the Qilian Mountains National Natural Reserve, on the northern slope of the middle Qilian Mountains in the northeastern Tibetan Plateau (38°26′N, 99°55′E, ~3200 m a.s.l.). According to the nearest meteorological station in Qilian (38°11′N, 100°15′E, 2787 m a.s.l.), the mean annual precipitation during the period 1951–2013 is 406 mm, about 90 % of which falls during the rainy season from May to September. The winter (December–February) mean temperature, mean minimum temperature and mean maximum temperature are −11.40, −18.89 and −1.15 °C, respectively, while those for the summer season (June–August) are 12.15, 5.70 and 20.18 °C, accordingly.
During the year 2013, four isolated, about 100 years old, healthy Qilian juniper (Sabina przewalskii Kom.) trees were selected for analysis. The selected trees have 38.7 cm (standard deviation = 7.8 cm) of diameter and 4.21 m (standard deviation = 1.1 m) height. Trees with dead crowns, tilted stems probably containing reaction wood or evident biological deterioration or mechanical damages were avoided. Micro-core samples were taken at breast height (about 1.3 m) with a Trephor corer (Costruzioni Meccaniche Carabin C., Belluno, Italy; Rossi et al. 2006) in weekly intervals from late April to early October. All samples contained the preceding 3–4 tree rings and the developing annual wood layer including the cambial zone and adjacent phloem. Immediately after sampling, the micro-cores were placed in Eppendorf microtubes filled with absolute ethanol and stored as soon as possible at 5 °C to avoid tissue deterioration.
In the laboratory, each sample was oriented by marking the transversal side with a pencil under a stereo-microscope, and then embedded in paraffin. Cross sections of ~8 to 12 µm thickness were cut with a Leica RM 2245 rotary microtome (Leica, Wetzlar, Germany). Sections were stained with safranin (0.5 % in 95 % ethanol) and astra blue (0.5 % in 95 % ethanol), and photographed with a Leica microscope system. Main xylem differentiation phases were distinguished as enlargement, secondary wall thickening and lignifications. The number of cells in the growing tree ring of each tree was counted along three radial lines, then averaged and used to assess the overall timing of xylem growth. In spring, after at least one cell row can be observed in the enlarging phase in the post-cambial zone, xylem formation is considered to have begun. In the late summer, when cambium divisional activity has ceased and no cell is observed in the phase of cell enlargement, secondary wall thickening or lignification, xylem formation can be considered complete.
In addition, the related radial increment for each sampling date was measured with the ImageJ software (http://rsbweb.nih.gov/ij/). The same standardization method and Gompertz function model as mentioned above were used for the radial increment and cumulated radial increment.
Relationships with climate data
High-resolution (30-min interval) climate data were extracted from an automatic meteorological station (HOBO U30) installed within 150 m of the monitored dendrometer and micro-coring trees. Climate parameters measured include relative humidity (%), summed precipitation (mm), mean temperature (°C), mean maximum temperature (°C), and mean minimum temperature (°C). Herein, the mean maximum and minimum temperatures were extracted from the daily 48 temperature data measured during one diurnal circle. Since the precipitation values are not normally distributed, nonparametric Kendall’s Tau correlation coefficients, instead of Pearson correlations were used to assess the relationships between daily radial increments and water losses severity obtained from dendrometer data and climate factors.
Results and discussions
Microclimate during the growing season
From initiation of cell enlargement to completion of lignification, variation among individual organisms is expected, not only because of differences of micro-environment, but also because of endogenous genetic factors. However, common growth patterns prevail. Xylem ring formation of all investigated ~100-year-old juniper trees started before the middle of May and continued to the middle of August, resulting in growth duration of 3 months in the observed year 2013. Herein, it is pointless to compare the whole growth process with the few currently available other studies conducted in North China in the year 2006 (Liang et al. 2009) or in the southeastern Tibetan Plateau (TP) in the year 2008 (Li et al. 2013), because of the differences in geographic location, tree species, site elevation, tree age and year-to-year variations of climatic conditions. We expect more thorough comparisons of the cambial phenology if the monitoring at our study site continues for several more years.
Percentages of radial growth and cell numbers (in brackets) formed during each month for the four sampled trees derived from the micro-coring method
15.74 % (16.02 %)
7.80 % (21.57 %)
22.82 % (18.93 %)
6.85 % (25.20 %)
13.30 % (20.43 %)
44.19 % (44.20 %)
50.36 % (43.94 %)
50.28 % (44.20 %)
49.73 % (54.96 %)
48.64 % (46.83 %)
30.13 % (29.92 %)
33.47 % (26.21 %)
21.97 % (27.89 %)
34.65 % (17.10 %)
30.05 % (25.28 %)
9.95 % (9.85 %)
8.37 % (8.28 %)
4.92 % (8.98 %)
8.78 % (2.73 %)
8.00 % (7.46 %)
Dendrometer measurement and relationships with climate factors
Nonparametric Kendall’s Tau correlation coefficients between the averaged stem radial changes derived from the three dendrometer series and climate parameters in the observed year 2013
Stem radial increment (Max2 − Max1)
Stem radial variation (Mean2 − Mean1)
Precipitation and relative humidity have been found to positively influence stem increment in different environments (Deslauriers et al. 2007; Duchesne and Houle 2011; Krepkowski et al. 2011; Köcher et al. 2012). In response to decreased precipitation or heat-induced drought effects during the vegetation period, trees may trigger an earlier stop of cambial activity (Vieira et al. 2014), declined cell division rate (Chaves et al. 2002), reduced cell size (Abe et al. 2003) or lumen area (Belien et al. 2012), or a bigger proportion of latewood tracheids (Pasho et al. 2012). Still, cambial activity and xylem cell development are considerable sinks of sucrose from photosynthesis (Oribe et al. 2003), the effects of drought thus can exacerbate the reduced wood production (Arend and Fromm 2007). Related studies indicated that under limited water availability, the non-structural carbohydrates in both cambium and xylem were significantly reduced during the growing season (Pantin et al. 2013; Deslauriers et al. 2014). It is generally considered that under slight water deficit, only cell expansion is physically inhibited by a decrease of cell turgor (Steppe et al. 2006; Köcher et al. 2012). If water deficit gets more severe, stress will affect the whole plant physiology, inhibiting cell metabolism and finally limiting growth (Rossi et al. 2008c). These relationships should be explored at shorter time scales by high-resolution monitoring, thus allowing higher levels of precision and more complete understanding of the roles of environmental factors on the mechanisms and components of wood formation.
This study is a systematical effort to combine wood anatomical analyses of thin sections obtained with regular micro-coring of the cambial zone, dendrometer measurements and automatic meteorological station data to analyze wood formation and stem radial variation, and their relationships with climate factors on the northeastern Tibetan Plateau. Results showed that in the experiment year 2013, the monitored Qilian juniper (Sabina przewalskii Kom.) cambial activity initiated before the middle of May. June and July were the main growth period, during which three quarters of the whole ring width were formed. At the end of July or early August, cell division stopped to leave enough time for the completion of cell formation before winter. All cell differentiation periods completed at the middle of August. Dendrometer data indicate that precipitation or related relative humidity are the main factors influencing the recorded stem radial changes on the intra-annual scale in the study region. Our current results provide detailed knowledge of Qilian juniper growth processes and contribute to a better understanding of the relationships between stem radial variation and climate factors across the full vegetation period. Qilian juniper growing in the study region has the potential to provide millennial, continuous and annually resolved paleoclimate records (Gou et al. 2014; Yang et al. 2014). Thus, to obtain a comprehensive understanding of growth reactions in the high-elevation forest ecosystems of the region, continued monitoring of wood formation during climatologically varying years is still needed.
Author contribution statement
Conceived and designed the experiments: BY, MHH. Performed the experiments: MHH, BY, ZYW, AB, KP and RO. Analyzed the data: MHH, BY, ZYW, AB, KP and RO. Contributed reagents/materials/analysis tools: MHH, BY, ZYW, AB, KP and RO. Wrote the paper: MHH, BY, ZYW, AB, KP and RO.
All necessary permits were obtained for the described field studies from the Administration of Gansu Qilian Shan National Nature Reserve. The study was jointly funded by the National Science Foundation of China (Grant No. 41325008, 31300412) and the Interdisciplinary Innovation Team project of the Chinese Academy of Sciences (29Y329B91). The research was also supported by Chinese Academy of Sciences visiting fellowship for researchers from developing countries (2014FFZA0006) and the CAS/SAFEA International Partnership Program for Creative Research Teams. The authors would like to thank Jie Wang, Jianqi Zhang, Hongyuan Ge, Wen Wang and Hongyi Wang for the maintenance of the field instruments.
Compliance with ethical standards
Conflict of interest
All the authors declare that they have no conflict of interest.
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