In arid and semi-arid areas, the severe shortages in water resources as well as the spatial and temporal differences in precipitation exacerbate the deficit in water resources and the dependency of forestry on water. The issues of drought resistance and the water consumption of trees gradually caught the attention of domestic and international experts and scholars (Daley et al., 2006; Granier et al., 1990; Lapitan et al., 1996; Baker et al., 1987; Xu et al., 2015; Yan et al., 2015). The semi-arid Lhasa river valley is one of the major "one river, two tributaries" zones in Tibet, it became the site of Tibetan settlements for more than 1 000 years. Because of past developments, the native vegetation in the river valley area is seriously damaged, which has caused a series of environmental issues such as blown sand as well as soil and water loss. Currently, native vegetation recovery is one of the critical steps that must be taken in the construction of ecological shelters in the semi-arid Lhasa river valley (Zhao et al., 2013). In particular, the aridification of the river valley further intensified during the last half century because of frequent human activities as well as unreasonable developments and the use of resources. The conflicts that exist among the population, resources, environment, and development became increasingly prominent. These issues not only influence the sustainability of socioeconomic development in the Lhasa river valley but also cause the loss of ecological protection in the "one river, two tributaries" area, thereby affecting the construction of an ecological shelter in the Tibetan Plateau (Zhao et al., 2014; Schaeffer et al., 2000).

The semi-arid Lhasa river valley has a plateau monsoon semi-arid climate. The vegetation is primarily composed of subalpine shrub, meadow vegetation, and valley plantation communities (Zhao et al., 2013; Yang et al., 2010). And, the river valley is also at a high altitude, has an annual rainfall of 200-500 mm, with a clear distinction between its wet and dry seasons, and is exposed to intense solar radiation (Lu et al., 1986). In addition, the soils are primarily composed of sand with poor water-retention capacity that cannot meet the water demand for normal forest growth and development. Thus, the survival rate of artificial afforestation is extremely low. Studies on the transpiration characteristics of plantation species and their influences on environmental factors are needed with regard to reconstructing river valley vegetation. The results might provide a scientific basis for the evaluation of the stability of plantation water use with regard to the processes of ecological restoration and sustainability management.

Stem sap flow is a critical physiological indicator for measuring plant transpiration, it reflects the physiological features of the plant and the comprehensive regulation on plant water use based on environmental factors (Daley et al., 2006). More than 99.8% of the transpiration of trees comes from stem sap flow (Granier et al., 1990; Lapitan et al., 1996). Therefore, an accurate measurement of stem sap flow reflects the transpiration of the plant (Baker et al., 1987). The changes in plant stem sap flow are highly correlated with meteorological factors (Xu et al., 2015; Zhao et al., 2014; Schaeffer et al., 2000; Ma et al., 2011; Guan et al., 2012). An accurate analysis of the transpiration pattern of a single plant is critical for accurately estimating actual water consumption and the transpiration of vegetation covering a large area (Li et al., 2016). Recently, many scholars have implemented thermal methods for measuring plant stem sap flow because of their advantages of higher sensitivity (Yunusa et al., 2000; Wu et al., 2015), and the various domestic and international research studies have been conducted on the water consumption of trees (Guan et al., 2012; Li et al., 2016; Wu et al., 2015). The research on stem sap flow has primarily focused on the trees in temperate and tropical areas, but research on the water consumption of trees in special environments such as Tibet are lacking, even fewer studies have been conducted on the transpiration characteristics of the large group of shrubs in the semi-arid Lhasa river valley.

Poplars are drought resistant, impoverishment tolerant, and able to grow rapidly. They have become the major species in the construction of farmland shelterbelts and wasteland afforestation in Tibet. They are currently widespread in the main river valley areas in Tibet. Populus szechuanica and P. beijingensis cover large planted areas in the semi-arid Lhasa river valley (He et al., 2009). There exists 2 000 hectares of P. szechuanica, and 1 500 hectares of P. beijingensis in the semi-arid Lhasa river valley. The P. szechuanica is a precious native species in the Tibetan Plateau. Because of their fast growth, long lifespan, straight stem, good quality and adaptability, P. szechuanica is widely used to the afforestation in the central and western of Tibet. P. beijingensis is easy to breed and enables fast afforestation, and with its advantages of fast growth and drought tolerance, P. beijingensis has been widely used to populate in the Lhasa river valley since the 1980s (Guan et al., 1993). Thus, these two poplar species has captured much attention form researches. However, studies on the water use of these poplar species are lacking. Information on the characteristics of the stem sap flow of trees and their responses to environmental factors in special environments (e.g., Tibet) have not been reported. Therefore, this study performed continuous measurements of the stem sap flow of the main afforestation species, P. szechuanica and P. beijingensis, and the main environmental factors in the Lhasa river valley. The primary objectives were as follows: 1) Compare and analyze the characteristics and differences in stem sap flow of P. szechuanica and P. beijingensis in the semi-arid Lhasa river valley at an altitude of 3 600 m during the wet and dry seasons; and 2) Explore the relationship between the environmental factors and stem sap flow of the main afforestation species in the semi-arid Lhasa river valley area during the dry and wet seasons. The current study sought to understand the characteristics and pattern of transpiration of the main afforestation species in the Lhasa area. The results might provide a scientific basis for the selection of drought-tolerant tree species for vegetation restoration in the semi-arid Lhasa river valley.

1 Materials and methods 1.1 Site description

The testing site was located at the Research Institute of Forestry, Forestry Bureau, Tibet Autonomous Region (29°26′13″N, 90°29′25″E, altitude 3 632 m). The site is located in a plateau monsoon semi-arid climate. The weather is warm and dry with annual average temperature at 7.4 ℃. And the intra-day temperature with minimum temperature at 1.0 ℃ and maximum temperature at 18.7 ℃. The annals precipitation is 200-500 mm. Precipitation primarily occurs during the wet season (June, July, and August alone comprise 88.3% of the annual precipitation). Rainfall often occurs at nights, the nighttime rain rate is approximately 80%. The average relative humidity is approximately 30%-50%. The frost-free period is 133 d, and the annual sunshine is more than 3 000 h. The vegetation at the research site is primarily composed of subalpine shrub, meadow vegetation, and valley plantation communities.

1.2 Plant material

The forest of the testing site is an artificial mixed forest of P. szechuanica and P. beijingensis plated in 1973. The two poplar species were planted in the same area, and the sample trees were 20 meters apart. The average diameter at breast height (DBH) is 29.8 cm, and the average height is 24.5 m. In the artificial forest, four samples of P. szechuanica and P. beijingensis that were well-grown with straight stems and without pests or disease were selected as samples for the stem sap flow measurements. The basic parameters of the measured trees are provided in Tab. 1.

1.3 Sap flow measurement

A sample of eight trees was chosen for sap flow measurements in the wet (July) and dry (October) seasons, including 4 average trees representing P. szechuanica and 4 average trees for P. beijingensis (Tab. 1). The xylem was diffuse-porous and the sapwood width was around 4.0 cm according to sampling surveys. Xylem sap flow was measured using thermal dissipation probes (Granier 1987). We used TDP50 sensor (Dynamax Inc, TX, USA) which contains two probes of 50 mm long and 1.2 mm in diameter. They were installed into the sapwood of trees at a height of about 1.3 m above ground and spaced 40 mm apart vertically. Waterproofing sealant was placed around the probes to prevent water infiltration, and the stem and probes were further wrapped with reflective bubble insulation to prevent natural heat influence. Temperature difference between the probes was recorded every 30 s and 30 min means were stored on a data logger (CR1000, Campbell Scientific Inc., Logan, UT, USA). Sap flow velocity (V, cm·s^-1) was calculated using the empirical equation of Granier (1987) as:

$ V{\rm{ = }}0.0119 \times {\left( {\frac{{{\rm{d}}{T_{\rm{m}}} - {\rm{d}}T}}{{{\rm{d}}T}}} \right)^{1.231}}. $

(1)

where dT is the temperature difference between the downstream and the upstream probes and dT_m the maximum when sap flow is nil.

Sap flux density (F, g·h^-1) was calculated using the empirical equation as:

$ F = 3{\rm{ }}600 \times V \times A. $

(2)

where V is the sap flow velocity and A (cm²) is the sapwood area.

1.4 Environmental variables

Environmental data were simultaneously measured using an automatic weather station (Delta-T Devices Ltd, Cambridge, England). Solar radiation (Q, W·m^-2), relative humidity (RH, %) and air temperature (T_a, ℃), wind speed (V_w, m·s^-1), precipitation (mm) and soil water content (SWC) were measured, respectively. The sensors were placed at 7.1 m height and 30 m from the measured trees in an open area. The data were recorded automatically every 30 min. Vapor pressure deficit (VPD, kPa) was calculated based on an empirical exponential relationship of Campbell et al. (1998) as:

$ {\rm{VPD}} = 0.611 \times {\rm{exp}}\frac{{17.502 \times {T_a}}}{{{T_a} + 240.97}} \times (1 - {\rm{RH}}). $

(3)

1.5 Data analysis

SAS 8.1 software package was used for statistical analysis. The sap flow velocity and sap flux density within replicates of poplars (n=4) trees showed similar amplitude, we thus analyzed the averages of sap flow velocity and sap flux density from replicated sample trees, the significance for differences was analyzed by t-test, P < 0.05. The relationships between sap flow velocity and environmental factors (solar radiation and vapor pressure deficit) were analyzed by Gauss-Newton method.

2 Results 2.1 Environmental factors during the wet and dry seasons

Fig. 1 illustrates the changes in the daily averages of the major meteorological factors (Ta, Q, SWC, and VPD) during the typical dry season (October) and wet season (July). The average Ta of the area during the wet and dry season is 16.4 ℃ and 9.1 ℃, respectively. The monthly average of the total Q in July was 577.53 w·m^-2, with a maximum of 727.46 w·m^-2 and a minimum of 345.92 w·m^-2. The monthly average total Q in October was 346.54 w·m^-2, with a maximum of 417.79 w·m^-2 and a minimum of 187.53 w·m^-2. The monthly average of the SWC in July was 3.13%, whereas that of October was only 2.05% (i.e., less than half that of July). The change in VPD during July ranged from 0.32-1.69 kPa, and the change during October ranged from 0.25-1.25 kPa. Because of the high absolute altitude and complex terrain of the Tibetan Plateau, the weather condition in the area is complex and varying.

2.2 Diurnal variation of solar radiation, VPD, and sap flow velocity in the wet and dry seasons

The typical daily changes in environmental factors during the dry season (October 18^th-20^th) and wet season (July 18^th-20^th) were provided in Fig. 2. In July (the wet season), Q began at 7:30 am with the most intense Q at 1:00—2:00 pm. In October, Q starts approximately an hour later than in July with the most intense Q at 2:00 pm. During the wet season, the SWC was higher than that during the dry season, and the minimum VPD appeared at 8:00 am, the appearance of the maximum VPD was relatively unstable but typically between 2:00 and 5:00 pm. During the dry season, the appearance of the minimum VPD showed greater fluctuation between 7:00 and 9:00 pm, whereas the maximum VPD appeared between 4:00 and 5:00 pm.

The changes in the stem sap flow velocity of the two poplars during three consecutive sunny days in both the dry and wet seasons are illustrated in Fig. 2c. The peak value of the sap flow velocity of P. szechuanica was greater than that of P. beijingensis. The sap flow velocity yielded a "broad peak" curve during the wet season, and during the dry season the sap flow velocity yielded a "narrow peak" curve. In addition, both poplars showed sap flow activities during the nighttime.

The intra-day changes in the sap flow velocity for both poplars differed during the dry and wet seasons, the changes in the main indices are presented in Table 2. The start of the sap flow for both poplars was between 7:30 and 8:30 am during the wet season and between 8:30 and 9:00 am during the dry season. In both the dry and wet seasons, the start of the sap flow of P. beijingensis showed a 30 min lag compared with P. szechuanica. With the increase in Q intensity, the temperature gradually increased, and the RH decreased, whereas the sap flow velocity gradually increased. During the wet season, the time of the peak sap flow for both poplars was consistent, was between 1:30 and 2:00 pm, however, the peak value of sap flow velocity of P. beijingensis were approximately 70% of those of P. szechuanica. During the dry season, a greater difference existed in the appearance time of the peak sap flow between the two poplars. The peak flow for P. szechuanica appeared at approximately 4:30 pm, whereas that for P. beijingensis was between 7:00 and 7:30 pm. The peak value of sap flow velocity of P. beijingensis were approximately 30% of those of P. szechuanica during the dry season.

2.3 Variation of sap flow velocity and sap flux density in the wet and dry seasons

Considering the continuity and integrity of the collected data, the daily averages of the sap flow velocity on July 1^st, 2^nd, 4-7^th, 11-14^th, 18-20^th and on the same days in October (13 d in each month) were subjected to analysis. As Fig. 3 shows, the daily average and the daily maximum of the sap flow velocity significantly differed between the two poplars and between the two seasons. The daily average and daily maximum of sap flow velocity in P. beijingensis in both seasons were significantly lower than those of P. szechuanica. During the wet season, the daily average of the sap flow velocity in P. szechuanica and P. beijingensis were 0.005 17 cm·s^-1 and 0.002 21 cm·s^-1, respectively. The sap flow velocity of P. beijingensis was only 40% of that of P. szechuanica. During the dry season, the daily averages of the sap flow velocity of P. szechuanica and P. beijingensis were drastically reduced (0.001 74 cm·s^-1 and 0.000 49 cm·s^-1, respectively). The sap flow velocity of P. szechuanica and P. beijingensis during the dry season were only 33.7% and 22.3% of that during the wet season, respectively. The daily maximum of sap flow velocity showed a similar trend compared with the daily average. During the dry season, the daily maximum for P. beijingensis was approximately 31.7% of that of P. szechuanica, whereas this ratio was 48.4% during the wet season. In addition, for P. szechuanica and P. beijingensis, the daily maximum of the sap flow velocity during the wet season was approximately 2.26 times and 3.45 times that during the dry season, respectively.

Mean value and SD. In the same column the different capital letters indicate statistically significant differences among different species in the same season, and the different lowercase letters indicate statistically significant differences among the same tree species in different seasons at the 0.05 probability level, respectively.

As Fig. 4 shows, significant differences existed in the daily averages of the stem sap flux density between the two species as well as between the two seasons for each species. The daily average of the stem sap flux density for P. beijingensis was significantly lower than that of P. szechuanica during both the dry and wet seasons. During the wet season, the daily average of the sap flux density of P. szechuanica was 11 222.85 g·h^-1, whereas that of P. beijingensis was 4 641.08 g·h^-1 was 58% lower than P. szechuanica. During the dry season, the daily average of the sap flux density of P. szechuanica was 3 893.93 g·h^-1, whereas that of P. beijingensis was 1 098.88 g·h^-1, which was 71% lower than that of P. szechuanica. Compared with the wet season, the stem sap fluxes of both poplars were drastically reduced during the dry season. During the dry season, the daily averages of the stem sap flux density of P. szechuanica and P. beijingensis were 65% and 76% less than those during the wet season, respectively.

Mean value and SD. In the same column the different capital letters indicate statistically significant differences among different species in the same season, and the different lowercase letters indicate statistically significant differences among the same tree species in different seasons at the 0.05 probability level, respectively.

2.4 Sap flow velocity and the relationship with environmental variables in the wet and dry seasons

During the dry and wet seasons, a significant correlation was found between Q and the sap flow velocity of the two poplars (Fig. 5). As the determination coefficient shows, differences were found between the two poplars, as well as between the two seasons. The coefficients of determination associated with Q of P. szechuanica were 91.5% and 79.4% during the wet and dry seasons, respectively. The coefficient of determination associated with Q of P. beijingensis was less than that of P. szechuanica, the coefficients were 83.1% and 67.2% during the wet and dry seasons, respectively. The influence of Q on the sap flow velocity was greater during the wet season than during the dry season, and this influence was more apparent on P. beijingensis.

During the dry and wet seasons, a significant correlation was found between the sap flow velocity of the two poplars and the VPD (Fig. 6). During the wet season, the coefficients of determination associated with the VPD for the sap flow velocity of P. szechuanica and P. beijingensis were 90.1% and 78.4%, respectively. The coefficient of determination associated with the VPD for P. szechuanica was approximately 15% higher than that for P. beijingensis. During the dry season, the coefficients of determination associated with the VPD for the sap flow velocity of P. szechuanica and P. beijingensis were significantly increased, which were 94.4% and 89.5%, respectively. This result indicates that Ta and RH have greater influences on the sap flow velocity of the two poplars during the dry season. Regarding the introduced tree species, VPD had less influence on the sap flow velocity of P. beijingensis than on that of P. szechuanica.

Fig. 6 Along with a multivariate statistical analysis, a stepwise multivariate regression analysis was performed on the environmental factors driving transpiration as well as the sap flow velocity of the two poplars during the dry and wet seasons. The regression equations are provided in Table 3. The major environmental factors that influenced the sap flow velocity of the two poplars differed during the dry and wet seasons. Although a regression of all of the environmental factors on the sap flow velocity reached significance, SWC was not included in the regression equation for P. beijingensis during the dry season. The coefficients of determination associated with the environmental factor regression equation on sap flow velocity of P. szechuanica during the wet and dry seasons were 0.949 1 and 0.949 8, respectively, whereas those associated with P. beijingensis were 0.913 6 and 0.855 1, respectively. Therefore, these equations might reveal the dependence of the sap flow velocity on the factors that drive transpiration.

3 Discussion

The daily change trends in sap flow for both poplars during the dry and wet seasons were approximately the same. An apparent diurnal rhythm was observed. These results are similar to those obtained in previous studies (Mo et al., 2014; Ni et al., 2015; Yan et al., 2015; Prior et al., 2013). At nighttime, although the stomata of the plants were closed, sap flow was present. These results might be attributed to the intense transpiration of plants in the semi-arid Lhasa area during the wet season. These plants experienced excessive water loss, thus the sap flow at night was needed to replenish the water lost. Furthermore, the cells damaged during excessive transpiration might be recovered to enhance drought tolerance. The daily changes in stem sap flow showed monomodal, polymodal, and broad-peak patterns (Bauerle et al., 2002; Xu et al., 2008). The two poplars showed polymodal curves during the wet season and a smoother monomodal curve during the dry season. This distribution might be attributed to the physiological factors of the trees or the "napping" phenomenon (Zang et al., 2010; Zhang et al., 2003; Chang et al., 2007). The polymodal pattern of the stem sap flow of the two poplars might be attributed to the intense Q resulting from the thin air in the Tibetan Plateau where the air density is approximately half of that of a typical plain. The significant seasonal and daily changes in weather might also be a factor. Therefore, the stem sap flow of the two poplars varied with the meteorological factors that showed greater fluctuation and resulted in a polymodal curve for the daily changes.

During the dry and wet seasons, the daily maximum and daily average of stem sap flow of P. szechuanica were significantly greater than those of P. beijingensis. The daily maximum and daily average of stem sap flow of P. beijingensis were approximately 70% and 30% that of P. szechuanica during the wet and dry season, respectively. These results are consistent with those on the stem sap flow of Albizia kalkora reported by Wang et al. (2013). During the dry and wet seasons, the starts of the sap flow of P. beijingensis occurred approximately 30 min after those of P. szechuanica. During the wet season, the sap flow rates of both poplars reached their maximum between 1:30 and 2:00 pm; the time was approximately the same for both poplars. During the dry season, a greater difference was observed in the time that the sap flow reached its maximum between the two poplars, the P. szechuanica reached its maximum approximately 3 h earlier than P. beijingensis. The differences in the biological structure of the tree species (e.g., conifers vs. broadleaf trees) might cause the different sap flow rates (Chen et al., 2015). Additionally, P. szechuanica and P. beijingensis belong to the same genus and grow under the same environmental conditions. The differences in maximum sap flow and daily average might be because P. szechuanica (as a native species) is more adapted to growing in the semi-arid Lhasa area. On the other hand, although P. beijingensis has apparent advantages as an introduced hybrid species, these advantages might not be fully expressed because of the limitations on its physiological functions due to the drought and soil impoverishment of the plateau.

In response to various environmental factors, the time lags of the two poplars differed during the dry versus wet season. As the main environmental factors, Q and VPD showed significant time lags with regard to the two poplars. The time lag during the dry season was 30 min briefer than that during the wet season. No time lag was found between the sap flow rate of P. szechuanica and VPD during the wet seasons. During the dry season, the sap flow of P. beijingensis reached its maximum before VPD but later than Q. These results indicate that Q is the primary environmental factors influencing the sap flow of the two poplars. On the other hand, during the dry season, the function of VPD on sap flow rate was enhanced, nevertheless, Q influenced the sap flow velocity.

The changes in plant stem sap flow are influenced by factors such as the biological structure of the plant, meteorological environment, and SWC (Sun et al., 2000). The meteorological environment is the key factor that causes instantaneous changes in plant stem sap flow (Tang et al., 2011). Because of the great difference in the site condition, meteorological environment, and physiological structure of the trees, the results of studies addressing the relationship between meteorological factors and stem sap flow have differed (Chi et al., 2013; Yang et al., 2012). This current research primarily focused on the influence of environmental factors on the instantaneous changes in the sap flow rate. This study indicates that the major meteorological factors that influence the sap flow rate of the two poplars are Q and the VPD, and the SWC had less influence on stem sap flow. However, other studies have indicated that the SWC determines the overall level of the transpiration of trees (Luo et al., 2016). In this study, the SWC measurement was taken 30 cm beneath the surface. For megaphanerophytes, additional studies are needed to determine whether the SWC that influences the overall transpiration is recorded from shallow soil water or ground water. The influences of the environmental factors on the two poplars during the dry and wet seasons differed. Q had greater coefficient of determination on the sap flow rate during the wet season, whereas VPD was the leading factor affecting the sap flows of the two poplars during the dry season. The stepwise regression analysis found that the regression equation of the environmental factors on the sap flow rate of the two poplars during the wet and dry seasons was significant. The R² values associated with P. szechuanica during the wet and dry seasons were both 0.94, whereas those of P. beijingensis were 0.85 and 0.91 during the wet and dry seasons, respectively. The results suggest that these equations better reveal the variation patterns between the sap flow rate and environmental factors.

4 Conclusions

In summary, greater differences exist in the meteorological factors of the Lhasa river valley area during the dry and wet seasons. The average of Q, T_a and VPD values during the wet season were around about 60% of those in wet season. Plants in the area face more severe water stress during the dry season. Compared with the wet season, the stem sap flow rate and sap flux of the two poplars were drastically reduced during the dry season. In both seasons, the stem sap flow velocity and sap flux of P. beijingensis were less than those of P. szechuanica. As the main environmental factors, Q and VPD had less influence on the stem sap flow of P. beijingensis than on that of P. szechuanica.