Jun Zhang · Liqing Liu

Abstract Although pruning is important to obtain highquality, large-diameter timber, the effects of pruning on nonstructural carbohydrates (NSC) in aboveground organs of many timber species are not well understood. Three intensities of pruning (none, moderate and severe) were tested on poplars ( Populus alba × P. talassica) in the arid desert region of northwest China to compare the concentrations of soluble sugar (SS), starch (ST) and total nonstructural carbohydrate (TNC) in leaves, branches and trunks during the growing season. The concentration of NSC components after different pruning intensities varied similarly in seasonal patterns, increasing slowly at the beginning of the growing season, continuously declining in the middle, then gradually recovering by the end of the growing season. The monthly mean NSC concentration in poplar differed significantly among the three pruning intensities ( p < 0.05). The SS concentration in pruned trees was higher than in unpruned trees ( p < 0.05). For moderately pruned trees, the concentrations of ST and TNC in trunks and branches were higher than in unpruned and in severely pruned trees ( p < 0.05). Compared with no pruning, pruning changed the seasonal variation in NSC concentration. The orders of SS and TNC concentrations in aboveground organs were leaf > branch > trunk, while the order of ST concentration was trunk > leaf > branch, which was related to functional differences of plant organs. The annual average growth in height of unpruned, moderately pruned, and severely pruned poplars was 0.21 ± 0.06, 0.45 ± 0.09 and 0.24 ± 0.05 m, respectively, and the annual average growth in DBH were 0.92 ± 0.04, 1.27 ± 0.06 and 1.02 ± 0.05 cm, respectively. Our results demonstrate that moderate pruning may effectively increase the annual growth in tree height and DBH while avoiding damage caused by excessive pruning to the tree body. Therefore, moderate pruning may increase the NSC storage and improve the growth of timber species.

Keywords Pruning intensity · Nonstructural carbohydrate · Populus alba × P. talassica · Seasonal pattern

Introduction

Carbohydrates can be divided according to their functions into structural carbohydrates (SC) and nonstructural carbohydrates (NSC) (Song et al. 2016). NSC in plant tissues mainly consist of soluble sugar (SS) and starch (ST), which are the result of the balanced relationship between carbon supply and carbon demand (i.e., carbon assimilation and consumption) (Quentin et al. 2015). Thus, NSC plays a major role in the growth and metabolism of plant (Zhang et al. 2014), and further exploration of NSC concentration will deepen our understanding of the mechanisms underlying plant physiology, carbon budgeting, responses to environmental changes, and ultimately, ecosystem processes.

NSC concentrations in trees vary by season and organ (Schaberg et al. 2000; Hoch et al. 2003; Landh?usser and Lieffers 2003; Spann et al. 2008). As the main sites of photosynthesis, Leaves are the primary carbon sources for trees, and branches, trunks and roots are the main carbon sinks for the photosynthetic products (Mei et al. 2015). Because branches both store and transport photosynthates, branch growth is conducive for increases in leaf area and photosynthetic yield (Ishii et al. 2000). Branches first receive carbohydrates needed for growth and storage before excess carbohydrates are transported to other organs, while stored NSC provide energy for the growth of leaves and new shoots in the early growing season (Sch?del et al. 2009). Trunks not only function to support the canopy, but also to transport soluble carbohydrates. Although the concentration of NSC in the trunk is relatively low, the trunk accounts for a large proportion of the total biomass of the tree and stores a large amount of NSC (Mei et al. 2015). NSC concentrations in the trunk and branch vary asynchronously and are lower in the trunk than in branches during the growing season (Hoch et al. 2003).

Plants are vulnerable to external disturbances during growth, including herbivores, trampling (Song and Wang 2013), pests (Vanderklein and Reich 1999; Anderegg and Callaway 2012; Atkinson et al. 2014), and fires (Wiley et al. 2013). When wounded, plants quickly mobilize stored NSC for protection (Song and Wang 2013) and activate defense responses (León et al. 2001). After Reichenbacker et al. ( 1996) defoliated Populus saplings to simulate damage by leaf-feeding insects, tree vitality, as measured by total amount of nonstructural carbohydrates (TNC), was only slightly affected when the amount of defoliation increased. After herbivory, trees sprout new leaves and adopt other coping strategies, such as selective restriction of growth (Honkanen et al. 1994) and rapid mobilization of carbon reserves (Li et al. 2002), which lead to different response strategies in various organs. Other types of destruction to leaves are also likely to affect the NSC.

Pruning is an important management practice to produce high-quality, no-section timber with large diameters and regulate the distribution of photosynthates among organs (Wang and Zeng 2016). In Camellia sinensis, Bore et al. ( 2003) found that the NSC concentration in the leaves, stems, and roots decreases soon after pruning, then gradually increases over the next 30 days. Chesney and Vasquez ( 2007) adopted different pruning intensities for Gliricidia sepium and Erythrina poeppigiana and found that pruning could lead to a large consumption of starch in stem tissues. In the branches and trunks of Aer saccharinum and Acer platanodies during the growing season, Ramirez et al. ( 2018) found that pruning has no effect on the concentrations of SS and ST in the trunks of the two species; However, the concentrations of SS and ST in the branches of A. platanoides is higher in April, decreases in June, and peaks in October. In contrast, in A. saccharinum, SS and ST concentrations increase slowly throughout the growing season. At present, relatively little is known about the effect of pruning in poplar plantations on the dynamics of NSC reserves.

Poplar ( Populus alba × P. talassica; Salicaceae), a deciduous tree species that is resistant to cold, drought, wind, and salt, is widely planted in arid desert regions in Northwest China and is an important afforestation tree species for soil improvement, desertification control, and water and soil conservation. Since the establishment of a shelter forest in 1999, the lack of forest management practices in poplar plantations has led to poor ventilation and light transmittance, so it is necessary to adopt pruning measures of reasonable intensity to improve the quality of tree. Here, we sample leaves, branches, and trunks of a poplar subject to different pruning intensities and explore the following hypotheses: (1) Severe pruning causes greater depletion in carbohydrate reserves than does moderate pruning; (2) NSC concentrations in different organs respond differentially to pruning intensities.

Materials and methods

Study area

The research site is located in the Linzhi base of the agricultural comprehensive development zone in Karamay City (45°22′–45°40′ N, 84°50′–85°20′ E) to the southeast of Mount Gayle and Genghis Khan in the western mountainous area of Junggar. The terrain elevation varies little, with a high in the southwest of 275 m a.s.l. and a low in the northeast of 259 m a.s.l. The average annual precipitation is about 157.4 mm (Fig.1) and is mostly concentrated from June to August, which accounts for 12.5–25.2% of the annual total. The annual potential evaporation is 1492 mm, about 9.5 times the annual precipitation, and the annual average temperature is 8.9 °C. The annual sunshine duration is about 2704 h, the annual average wind speed is about 3.2 m/s, and the frost-free period is 180–220 days. The region is a typical continental arid desert, and the soil in the forest belt of the study area is sandy loam with a depth of about 35 cm, and the groundwater depth is about 8.85 m (Zhang et al. 2013).

Sample area

The poplar plantation was established in 1999 with 2-year-old saplings and row spacing of 2 × 4 m. The

Fig.1 Air temperature, humidity, and precipitation at the research site in Northwest Chinastand age was 12 when sampled. The branches of poplar are dense with poor ventilation and light transmission in the forest belt. The height of natural pruning is less than 3.5 m. Low groundcover plants such as Ceratocarpus, Halogeton arachnoideus, Halogeton glomeratus and Malcolmia africana are grown in the poplar plantation.

Table 1 Survey of poplar plantation with different pruning intensities

In early March 2012, pruning was adopted in a 20 m × 40 m space in the plantation with three intensities: no pruning (control, CK), moderate pruning (pruning branches to 1/3 of tree height from the ground, MP), and severe pruning (pruning branches to 2/3 of tree height from the ground, SP). Each pruning intensity was replicated three times. Pruning was done by cutting branches even with the trunk to ensure smooth incisions and minimize damage to the bark around the incision. After pruning, the wound was painted to prevent wound infection. A wireless weather station (Vantage Pro2; American Davis) was set up approximately 10 m away from the study area, approximately 2.5 m off the ground, to continuously observe and record meteorological factors such as air temperature, air humidity and rainfall. The information of the poplar plantation is listed in Table 1.

Tree sampling

Canopy density, DBH, and total height were measured at the end of the 2011 and 2012 growing seasons (Table 3). Leaves, branches, and trunks were sampled from five standard trees every month from May to September; sampling was completed within 2 days. Canopy branches and leaves were obtained by climbing to the crown of the tree and using high branch scissors to remove branches randomly from the upper and lower canopy of the south-facing side of the crown. Branches and leaves were evenly mixed before making measurements. Growth cones with an inner diameter of 5 mm were used to drill tree cores at chest height and the middle of the crown on south-facing side of the trunk, and were likewise evenly mixed. After drilling the tree core, the resulting hole was smeared with butter and filled in quickly to avoid the invasion of diseases and pests. Samples were placed into self-sealing bags and temporarily kept in a lowtemperature refrigerator. On the same day, all samples were taken to the laboratory, heated in an 800-W microwave oven for 90 s (Hoch et al. 2003), dried to constant mass in an oven at 65 °C, pulverized with a high speed pulverizer, and passed through a 100-mesh screen for NSC analysis.

Data and statistical analyses

Samples were analyzed for SS and ST. The sum of SS and ST was referred here as TNC. SS and ST were measured using a modified phenol–sulfuric acid method (Buysse and Merckx 1993; Zhang et al. 2014). The NSC concentration is reported as a percentage of dry mass. Analysis of variance (ANOVA) and Tukey–Kramer honestly significant difference (HSD) test were used to compare the significance of differences in NSC concentrations among different treatments, sampling periods and organs. SPSS version 18.0 (SPSS Inc., Chicago) was used for all test, and SigmaPlot 10.0 software (SYSTAT, San Jose, CA, USA) to plot all graphs.

Results

Seasonal dynamics of NSC concentrations

The SS, ST and TNC concentrations in aboveground organs fluctuated during the growing season regardless of the pruning intensities of poplars (Fig.2). Regardless of pruning intensity, the concentrations of NSC components in leaves of poplars had similar seasonal patterns; ST and TNC in leaves rose early in the growing season and began to decline in June. As the growth rate of poplars increased, ST and TNC of leaves declined, reaching the lowest value in July. When the growth rate of poplars slowed, ST and TNC in leaves recovered, with the greatest rebound observed in severely pruned trees. SS in leaves decreased in the early growth stage to a minimum in July. Similarly, SS in leaves also began to recover as growth slowed, and the severely pruned trees showed the largest rebound. The concentrations of NSC components in branches of poplars among different pruning intensities showed similar seasonal pattern changes. SS in branches decreased early to a minimum in June, recovered to a peak value in August, and then decreased slowly. ST also peaked in August before declining. TNC in branches began to increase early in the year and peaked 1 month earlier (July) in severely pruned trees than in trees with the other treatments (August). NSC patterns in trunk were qualitatively similar across treatments: NSC increaseduntil July and then declined relatively abruptly in August and maintained or slightly increased in September. Compared with unpruned poplars, moderately and severely pruned trees showed a great magnitude of seasonal variation in NSC concentrations in leaves, branches, and trunks to some extent.

Fig.2 Nonstructural carbohydrates in leaves, branches, and trunks of poplars during the growing season after different pruning intensities. ( SS soluble sugars, ST starch, TNC total nonstructural carbohydrates)

NSC concentrations in different organs

In addition to its seasonal variation (Fig.2), NSC also varied across treatments and between organs (Table 2, Fig.3). Except for SS concentrations in trunks, the mean concentration of NSC components in leaves, branches, and trunks differed significantly ( p < 0.05, Table 2), and NSC concentrations of poplars with moderate and severe pruning were significantly higher than that of unpruned trees ( p < 0.05, Fig.3). The mean concentrations of ST and TNC in trunks differed significantly between treatments, and generally in the order MP > CK > SP, as did SS, ST, and TNC in branches. The patterns were different in the leaves: mean SS concentrations, and the mean concentrations of ST and TNC were in the order CK > MP > SP ( p < 0.05, Fig.3). Within pruning treatments, SS and TNC concentrations in aboveground organs were in the order leaf > branch > trunk, while ST concentrations were generally in the order trunk > leaf > branch.

Effects of different pruning intensities on tree growth

We measured canopy density, tree height, and DBH of trees within each treatment at the end of the growing season (Table 3). There were significant differences in the average growth of tree height and DBH between moderate and severepruning at the end of the growing season ( p < 0.05), but the average growth in tree height and DBH did not differ significantly between the severe pruning and no pruning treatments ( p > 0.05). Due to the greater canopy opening after pruning, nutrient area, ventilation, and light transmittance were improved. Thus, moderate pruning apparently promoted poplar growth.

Table 2 ANOVA of concentrations of nonstructural carbohydrate components

Fig.3 Comparison of seasonal mean values of nonstructural carbohydrates in leaves, branches, and trunks of poplar after different pruning intensities. Errors bars are standard errors of the mean. Bars labeled with the same letter within each index are not significantly different (Tukey’s test at p < 0.05). SS soluble sugars, ST starch, TNC total nonstructural carbohydrates

Table 3 Effect of pruning intensities on tree growth

Discussion

Effects of pruning on carbohydrate concentrations

As we expected, carbohydrate reserves in branches of poplars that were severely pruned were more depleted than in those of trees that were moderately pruned (Fig.2). The stasis of carbohydrate reserves after pruning may be explained by the intensity of the perturbation, which modulates the response of carbohydrates (Atkinson et al. 2014; Eyles et al. 2009). In contrast to severe pruning, moderate pruning did not reduce the percentage of biomass enough to mobilize the carbohydrate reserves to maintain metabolic demand and compensatory growth. Poplars with severe pruning transferred more NSC from the branches early in the growing season—for growth (i.e., new shoots and foliage)—than did the other pruning intensities (Fig.2). This result may indicate a high carbon loading of trees, and supports the idea that trees tend not to be limited by carbon supply (Hoch et al. 2003). Additionally, new foliage produced after pruning could have contributed to the recovery of the pruned trees (carbon autonomy of branches, Landh?usser and Lieffers 2012). Indeed, 1 year after pruning, trees had recovered their crown entirely without any sign of a reduction in growth (Lecigne 2013). These results were surprising because the moderately pruned treatment was close to the pruning limits proposed by the American National Standards Institute to maintain the health of planted forests (Johnson 2007). Current guidelines suggest that poplar plantations should not be pruned more than 30%, because disease, insect attacks, or even death may occur due to inappropriate conditions for growth in pure poplar stands (ANSI 2001). It remains unknown whether and how repeated pruning, such as done on target-trees near our research site, may affect trees over a long period, which would have implications for the growth of large diameter timber.

This first study of NSC dynamics in trees in the arid desert region of Northwest China showed that, despite the high external disturbances to which they are exposed (Gillner er al. 2014; Ramirez et al. 2018), seasonal dynamics of trees with different pruning intensities reflected what had been documented previously in forest trees (Martinez-Vilalta et al. 2016; Maurin and Desrochers 2013). Whatever the pruning intensity, SS concentrations decreased in the middle of the growing season, then reached high levels by the end of the growing season, where they remained until the end of dormancy. In contrast, ST after all pruning intensities increased continuously through the middle of the growing season, then declined to low levels by the end of the growing season, where they remained until the end of dormancy. The initial decrease in sugar concentrations may result from photosynthates being mobilized to meet metabolic and growth demands, rather than being stored early in the growing season (Carbone et al. 2013). In the middle of summer, the photosynthes are allocated to reserves, and NSC concentrations increase because of the reduction in sink strength (Gaucher et al. 2005).

Effects of pruning on NSC concentrations in organs

In contrast to our expectation, the NSC concentrations of different organs did not respond to pruning intensities. NSC concentrations in leaves, branches, and trunks clearly differed across pruning intensities. We found consistencies in the relative magnitudes of NSC components regardless of pruning intensity; for example, the order of concentrations of ST was trunk > leaf > branch. Here, the concentration of SS in leaves was higher than in branches and trunks, consistent with previous findings (Landh?usser and Lieffers 2003). The trunk is an important carbon storage organ and carbon sink, and its lignification degree is higher than other organs. In the trunk, NSC is mainly stored in the form of starch, which is maintained at higher concentrations than in the leaves and branches.

Conclusion

The dynamics of carbohydrate reserves have been evaluated widely in trees grown under natural conditions. To our knowledge, this is the first study that evaluates the dynamics of tree NSC in the arid desert region of Northwest China and, additionally, the first study to evaluate carbohydrate concentrations in three plant organs (leaves, branches, and stems) of severely pruned, moderately pruned and unpruned trees. The concentrations of NSC in aboveground organs had similar seasonal variation regardless of pruning intensity; indicating that the amplitude, rather than the patterns of seasonal variation in NSC are not affected by pruning. We further found that the monthly mean values of NSC concentrations in the aboveground organs of poplars varied according to pruning intensity. The concentration of SS in trunks of pruned poplars was higher than unpruned trees, and the concentrations of ST and TNC in trunks and branches of moderately pruned poplars were higher than those ofother treatments. Regardless of pruning intensity, the order of concentrations of SS and TNC in poplars was leaf > branch > trunk, and ST was trunk > leaf > branch, which may reflect the functional differences of plant organs. Therefore, moderate pruning can both increase NSC storage and improve the growth of poplars and may effectively increase growth in tree height and DBH, while avoiding the damage caused by excessive pruning to the tree body.

AcknowledgementsWe thank Ian Gilman at Yale University for his assistance with the English.

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