Wood harvest by pollarding exerts long-term effects on Populus euphratica stands in riparian forests at the Tarim River, NW China

Forest Ecology and Management 353 (2015) 87–96

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Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco

Wood harvest by pollarding exerts long-term effects on Populus euphratica stands in riparian forests at the Tarim River, NW China Petra Lang a,⇑, Michael Jeschke a, Tobias Wommelsdorf a, Tobias Backes a, Chaoyan Lv b, Ximing Zhang c, Frank M. Thomas a a b c

University of Trier, Faculty of Regional and Environmental Sciences, Geobotany, Campus II, D-54296 Trier, Germany Xinjiang Cele National Field Scientific Observation and Research Station of Desertification and Grassland Ecosystem, Cele 848300, Xinjiang, China Chinese Academy of Sciences, Xinjiang Institute of Ecology and Geography, 40 South Beijing Road, 830011 Urumqi, China

a r t i c l e

i n f o

Article history: Received 14 January 2015 Received in revised form 8 May 2015 Accepted 11 May 2015 Available online 30 May 2015 Keywords: Dendroecology Euphrates poplar Forest management Non-timber products Taklamakan Desert Tree morphology

a b s t r a c t Populus euphratica (Euphrates poplar) is the dominant tree species of the riparian (‘‘tugai’’) forests of Central Asia, which provide important ecosystem services to a rapidly growing population. However, overuse of the forests by wood harvest (pollarding) contributes markedly to their destabilisation. At the upper reaches of the Tarim River (Xinjiang, NW China), we investigated the effects of past pollarding (in the 1970s and 1980s) on the stand structure, tree morphology, stem diameter increment and intrinsic water use efficiency (iWUE) of poplars with different pollarding intensities in the past (‘No Use’, ‘Moderate’, ‘Intense’) growing on three adjacent plots with the same distance to the groundwater level. Compared to the non-used trees, the pollarded poplars (in particular, the intensely used trees) exhibited smaller figures of the following morphological variables: ratio of tree height to diameter at breast height, vertical crown extension, crown projection area, crown volume, and tree-ring width as well as basal area increment (BAI) during the past 24 years; but a higher number of secondary shoots, a higher percentage of hollow stems and a higher degree of hollowness of the stems. The pollarded trees were capable of regenerating to a certain extent, which was obvious from the formation of secondary shoots and, in the intensely pollarded trees, from a lower iWUE (inferred by more negative d13C isotopic ratios of the tree rings; most probably due to higher rates of gas exchange) as well as from their capability of re-establishing a crown efficiency similar to non-pollarded trees. However, the BAI of the main trunk and the secondary branches of the pollarded trees decreased continuously during the last 24 years of investigation. Whilst moderate intensities of pollarding seem to be sustainable for the riparian P. euphratica forests, intense pollarding reduces the growth increment of the trees and, even more importantly, results in a distinct increase in the percentage of hollow stems, which can render the trees less stable and more susceptible to secondary damaging factors. The significant correlations between BAI and morphological variables of crown projection area and crown volume are promising for developing approaches to assess the productivity of P. euphratica stands on a landscape level using methods of remote sensing. Ó 2015 Elsevier B.V. All rights reserved.

1. Introduction The Taklamakan Desert in the Tarim Basin of North-western China, the second largest sandy desert on Earth, can be assessed as hyperarid (ratio of mean annual precipitation to mean annual evapotranspiration of less than 0.03; Whitford, 2002). Its extremely hostile environment supports only sparse vegetation. Forests can solely establish along the banks of the Tarim River. ⇑ Corresponding author. Tel.: +49 651 201 3395; fax: +49 651 201 3808. E-mail addresses: [email protected] (P. Lang), [email protected] (M. Jeschke), [email protected] (T. Wommelsdorf), [email protected] (X. Zhang), thomasf@ uni-trier.de (F.M. Thomas). http://dx.doi.org/10.1016/j.foreco.2015.05.011 0378-1127/Ó 2015 Elsevier B.V. All rights reserved.

The type of riparian forests found along river systems in Western and Central Asia (Wang et al., 1996; Thevs, 2005; Thevs et al., 2008a) is known as ‘tugai forest’ (Thevs, 2005, 2006a), which harbours only few woody species. The predominant tree species is Euphrates poplar (Populus euphratica Oliv. [syn. Populus diversifolia Schrenk]) (Thevs et al., 2008a). Stands of P. euphratica can be found in arid and semi-arid areas from Northern Africa to India, but the largest natural population (>50% of the global population; Wang et al., 1996) occurs in the Tarim Basin in the Xinjiang Uygur Autonomous Region of China. The tugai forest is a highly threatened ecosystem (e.g., Thevs, 2006a). Water from the Tarim River as well as P. euphratica are

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used by the local population and form an important resource for the livelihood of many people. During the past century, population increased dramatically within this region (1953: 4.9 million; 2000: 19 million; National Bureau of Statistics and State Ethnic Affairs, 2003), leading to massive disturbances of this fragile ecosystem. The natural resources were over-exploited and the change from a traditional land use to industrialized cotton farming with large-scale irrigation resulted in even bigger problems (Hoppe et al., 2006): the groundwater levels decreased drastically and missing floods, caused by an uncontrolled overuse of Tarim River water, as well as deforestation of tugai forest led to an extensive decline of P. euphratica stands (Thevs et al., 2008a). As a typical phreatophyte, P. euphratica relies on permanent access to the groundwater (Wang et al., 1996; Thevs, 2005; Thomas et al., 2006; Thomas, 2014). The formation of xylem conduits with large diameters facilitates a high hydraulic conductivity (Rzepecki et al., 2011) and allows for high rates of biomass production (Gries et al., 2005; Thomas et al., 2006). Excess water loss is prevented by a delicate response of the stomata to an increase in the water vapour pressure deficit of the surrounding atmosphere (Thomas et al., 2008). Pollarding is a traditional way of using tree biomass for fuel, construction wood or fodder. Local farmers used to cut down the thickest stems at a stem height of 2–3 m every few years, mainly in August, which resulted in a disturbed growth of the trees. To our knowledge, there is no study focusing on pollarding effects on P. euphratica. Within the framework of the present study, which is part of the joint German-Chinese project SuMaRiO (‘‘Sustainable Management of River Oases along the Tarim River’’, Cyffka et al., 2013), P. euphratica trees, representative of the intensity of use (no, moderate and intense pollarding), were investigated with regard to stand structure, tree morphology, radial stem increment and d13C isotopic ratios in tree rings. To make sure that the effects are not superimposed by different distances to the water table, plots were selected that did not differ in their groundwater level. On a first inspection of the study site, the pollarded trees seemed to show reduced growth and were hollower than non-pollarded trees. Upon these field observations and theoretical considerations, we tested the following hypotheses: (i) Tree height, tree-ring width and basal area increment (BAI) decrease with increasing pollarding intensity. (ii) Crown morphology (crown area and volume) correlates with growth increment; if so, such relationships could be used as a basis for developing methods to predict growth using remote sensing data. (iii) As a compensatory response, trees respond to pollarding with higher rates of carbon assimilation, which should become evident through a lower intrinsic water use efficiency, indicated by more negative d13C isotopic ratios in the tree rings. Because P. euphratica forests provide important ecosystem services (provisioning services: wood for fuel, construction and handicraft as well as fodder for livestock; regulating services: protection from sand drift and soil erosion), conservation of the forests is of crucial importance for maintaining the livelihood of the human population. Nowadays, the poplar forests of Xinjiang are totally protected by law (which also prevents tree cutting or felling for quantifying the amount of biomass harvested by pollarding and establishing allometric relationships). However, the growing human population still has a huge demand for natural resources from the forests. Therefore, information is needed on the extent of use that still is sustainable in the long term. Our study aims at contributing to providing a scientific basis for developing

sustainable management schemes for the P. euphratica forests in Xinjiang and other regions of Central Asia. 2. Material and methods 2.1. Study area and plot selection Our study was conducted at the upper reaches of the Tarim River near the village of Gezkum (Plot ‘No Use’ 40°560 6500 N; 82°510 1600 E; 966 m a.s.l. see Supplementary Material Fig. S1). The study site is situated in the Tarim River Basin at the northern fringe of the Taklamakan Desert in the Uighur Autonomous Region of Xinjiang in North-western China. The Tarim River runs from west to east and is mainly fed by snow and glacier melting water from the surrounding high-altitude mountains (Tian Shan, Pamir, Kunlun Shan). The Taklamakan Desert is characterized by a hyperarid continental climate. In the region of the study site, the mean annual temperature is 11 °C (January: 8 °C; July: 25 °C) with a mean annual precipitation of 62 mm (meteorological station at Alar near the Tarim River, approx. 140 km to the west of the study area). A total amount of 285 poplar trees were selected in order to represent the different pollarding intensities. The pollarding categories are based on morphological traits, as callus formation and tree morphology generally are clearly linked to pollarding intensity. If trees are repeatedly cut at the same height, only tree-ring data can provide information about pollarding duration. Pollarding was conducted by local farmers, who always completely removed the largest branches of the trees. Interviews with local farmers and shepherds confirmed that pollarding was done every year in August, but not on every tree. Exact data on pollarding events, dating back more than three decades in our case, do not exist because neither forestry nor other local authorities were involved in pollarding at that time. Neither the Tarim Watershed Bureau nor the forest administration could provide data on pollarding intensities and the beginning of pollarding. The pollarding ended – at least at a large scale – with the prohibition of pollarding by law. The trees were concentrated on three plots. The distance between the individual plots was at least 370 m to avoid spatial autocorrelation (cf. Fig. S1 of the Supplementary Material). All plots exhibited a similar distance to the groundwater level (2.0– 2.2 m on average; measured at seven spots per plot with a hand-driven soil auger). Each plot covered an area with a radius of 50 m around a central tree. The plots contained at least 23 trees with a diameter at breast height (dbh; measured at 130 cm above ground, including the bark) between >15 cm and 40 cm. The trees of the first plot (n = 95) had not been subjected to pollarding (‘No Use’). These trees showed a normal growth pattern (Fig. 1a). The poplar trees (n = 102) on the second plot were characterized by a moderate pollarding intensity (‘Moderate’). Wood removal from the crown was clearly visible through the formation of at least one secondary stem (Fig. 1b). The trees (n = 88) of the last plot (‘Intense’) were affected by several pollarding events over a longer period of time. Their crowns were subdivided into several parts and wood removal from the crown was clearly evident by the existence of multiple secondary stems (Fig. 1c). 2.2. Tree morphology and stand structure On each plot, we recorded the dbh, tree height, crown height and the position of all trees. Using a sighting tube, we calculated the crown projection area as the sum of eight triangles, which resulted from eight vertical projections of the crown onto the horizontal plane (Johansson, 1985; Röhle, 1986). At pollarding height,

P. Lang et al. / Forest Ecology and Management 353 (2015) 87–96

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Fig. 1. Typical growth patterns of Populus euphratica on the three study plots with different pollarding intensity; (a) no pollarding, (b) moderate pollarding and (c) intense pollarding.

the numbers of stems and branches with a diameter of >2 cm were recorded. Stand density (number of trees per unit soil surface area), basal area and tree cover as well as the percentage of hollow trees and the degree of hollowness were determined for each plot. The degree of hollowness was calculated by subtracting the increment core length from the corrected stem radius at breast height. The corrected stem radius was estimated by taking the shrinking of the dried cores as well as the mean bark thickness into account (Wessolly, 1998). 2.3. Tree-ring analyses Increment cores were taken from 23 trees (representative of one type of pollarding intensity; dbh >15 cm) per plot with an increment borer (5 mm of diameter, length 400 mm; Suunto, Vantaa, Finland). Two cores per tree were sampled from the main trunk at breast height. To determine the date of pollarding, 33/36 (‘Moderate’/’Intense’ use) secondary stems with a diameter >10 cm that had been formed after pollarding were sampled with an increment borer (Table 1). The age of the trees and the secondary stems was determined with a moveable object table (Lintab 5, Rinntech, Heidelberg, Germany) and a stereo microscope (Carl Zeiss, Jena, Germany) with an accuracy of 10 lm. As many trees were hollow, we estimated the tree age by adding missing years. The missing years were

Table 1 Sampling of tree increment cores: total number of trees/secondary stems, increment cores, hollow and damaged cores and cores eliminated from further analysis after cross-dating; numbers in brackets = percentage of all cores within each group.

‘No Use’ main trunk ‘Moderate’ main trunk ‘Moderate’ secondary stems ‘Intense’ main trunk ‘Intense’ secondary stems

Trees/ secondary stems

Hollow cores

Damaged cores

Eliminated cores

23

4 (8.7)

1 (2.2)

6 (13.0)

23

15 (32.6)

1 (2.2)

14 (30.4)

33

15 (22.7)

6 (9.1)

0

23

20 (43.5)

0

6 (13.0)

36

16 (22.2)

4 (5.6)

0

calculated by dividing the area of the hollow core by the mean annual basal area increment of the intact outer surface for each tree separately. Further analysis of the tree-ring data was conducted with TSAP-Win Professional 0.55 software (Rinntech, Heidelberg, Germany). Cross-dating followed the standard methods in dendrochronology (Fritts, 1976; Schweingruber, 1983). Damaged cores and cores that were below the cross-dating thresholds were left out from further analysis. To avoid age-related effects on the growth rate, tree-ring width data were detrended by standardization. According to Fritts (1976), the trend was eliminated by converting the original tree-ring data (measured ring width, Wt) into ring-width indices (It) by subtracting the expected annual growth (Yt) from the original value at the time t (Eq. (1)). For fitting the curve, a 13-year moving average was used as a reference for the expected annual growth. Due to the mode of calculation, the age-detrended series are scattered around 0. Therefore, an offset (o) was added (Eq. (1)), which results in a shift towards the positive or negative range. For analysis we used the mean of the respective trend series as an offset to enhance the contrast between the plots.

It ¼ W t  Y t þ o

ð1Þ

While analysing tree-ring data, we observed a strong increase in mean tree-ring width on plot ‘No Use’ after 1970. Logging activities, indicated by a large amount of tree stumps within this plot, might have caused this sudden increase in the late 1960s. We determined the age of the logged trees by taking each one tree disc per stump from six stumps. To estimate the date of logging, the chronologies of the stumps were related to the chronologies of the increment cores. 2.4. Basal area increment and crown morphology From the individual tree-ring widths, we computed the annual basal area increment (BAI) for each tree on the assumption of circular cross-sectional areas of the stem and related the BAI to crown area and crown volume. We assumed an elliptical crown area and an ellipsoidal crown volume according to

V ellipsoid ¼ 4=3p a b c

ð2Þ

with a, longest axis of the ellipse; b, shortest axis of the ellipse; c, crown length. For calculations, we used the image processing package Fiji (Ferreira and Rasband, 2012).

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As the relationship between tree increment and crown morphology might be influenced by tree growth, we weighted crown area and crown volume by different morphological variables of the tree. Three different weighting approaches were used by multiplying crown area and volume with: (1) ratio of the vertical crown extension (VCE) to total tree height, (2) ratio of CBD to tree height, where CBD is the distance of the crown base to the soil surface; (3) ratio of CBD to VCE. To compare the growth rates of the trees across the different types of pollarding intensity we calculated the crown efficiency (tree growth per unit crown size) using the following formula (e.g., Fichtner et al., 2013):

CE ¼ BAI=mean crown surface area

ð3Þ

with CE, crown efficiency and BAI, mean BAI of the years 1987–2010 and 2000–2010. Mean crown surface area was calculated according to equation:

crown surface area ¼ pCR=6CL2 ½ð4CL2 þ CR2 Þ

3=2

 CR3 Þ

ð4Þ

where CR is crown radius and CL is crown length (Kramer, 1988). We calculated the mean BAI for the years 1987–2010 to cover the time span after the last pollarding event in 1983 plus an estimated immediate recovery period of three years. In addition, we calculated the crown efficiency for the time span 2000–2010, which should be representative for a period after a putative recovery from pollarding. To assess the capability of the trees to recover from pollarding, we determined an index of resilience for moderately and intensely pollarded poplars, which represents the ratio of post-pollarding to pre-pollarding growth (Pretzsch et al., 2013). To define the year of pollarding, we used the year with the lowest mean basal area increment within the time-span 1975–1983 (the period in which pollarding took place) for each tree separately. We assumed that a clear drop in BAI, which was detected in every pollarded tree during this time span, indicates strong pollarding activity. The index of resilience was calculated tree-wise as the ratio of the three-year averages of the annual basal area increments after and before the pollarding event. An index of resilience >1 indicates full recovery or even an increase in growth, whereas a value <1 is indicative of a decline in growth after pollarding (Pretzsch et al., 2013). 2.5. d13C isotopic ratios and iWUE The stable carbon isotope ratios (d13C) of the individual tree rings formed during the past 66 years were determined on the plots ‘No Use’ and ‘Intense’ in cores of six trees per plot. After combusting the samples in an element analyser (Flash EA 112, Thermo Finnigan, Bremen, Germany), the d13C isotopic ratios were measured in a continuous-flow isotope ratio mass spectrometer (Delta V Advantage, Thermo Finnigan) with IAEA-CH-3 (Coplen et al., 2006) as a standard. To remove the direct effect of the increase in the CO2 concentration of the atmosphere and the physiological reaction of the trees to higher atmospheric CO2 concentration, the data were adjusted by adding the difference between the atmospheric value for each year (Dphys) and a standard value (Datm) (McCarroll and Loader, 2004):

d13 Ccorr ¼ d13 Cmeasured þ Dphys þ Datm

ð5Þ

The intrinsic water use efficiency (iWUE) was obtained by (according to McCarroll and Loader, 2004):

iWUE ¼ ca =1:6  ðdb  d13 Cair þ d13 Ccorr Þ=ðdb  da Þ;

ð6Þ

where ca is the atmospheric CO2 concentration, da is the discrimination against 13CO2 during diffusion through the stomata (4.4‰) and db is the net discrimination due to carboxylation (27.00‰).

2.6. Statistical analyses Results are presented as mean values ±1 standard deviation. The program SPSS Statistics 21 (IBM, Armonk, NY, USA) was used for statistical analyses if not stated otherwise. Due to our plot selection (large distance between the plots; see Section 2.1), we could exclude spatial autocorrelation. Differences among the three tree groups (i.e. intensities of use) and plots were tested on statistical significance using the Kruskal–Wallis-Test, followed by pairwise post-hoc comparisons using the Mann–Whitney-U-Test and the Bonferroni–Holm-correction for multiple testing. The Friedman-Test in combination with the post-hoc Wilcoxon-signed-rank-Test was used for comparisons of the tree-ring chronologies among the plots. The relationships between BAI and crown morphology as well as tree age and degree of hollowness were tested by calculating Pearson correlation coefficients. The non-parametric Wilcoxon-signed-rank-Test was conducted to test if resilience differs significantly from the hypothetical median = 1. To test the effect of tree age on the degree of hollowness, we conducted an analysis of covariance (ANCOVA; SigmaPlot for Windows Version 13.0, Systat Software, Erkrath, Germany) with use intensity as the independent factor, the percentage of hollowness related to the stem cross-sectional area as the dependent variable and the tree age (estimated values in the case of hollow trees) as the covariate. All results were assumed to be statistically significant at P < 0.05.

3. Results 3.1. Stand structure and tree morphology Tree cover was highest and the basal area lowest on plot ‘No Use’ (Table 1). In contrast, the numbers of trees per plot as well as the stand densities were similar on all plots. Mean tree age was 47–90 years (Table 2; cf. Fig. S2A in the Supplementary Material). Significant differences in tree morphology were found among the pollarding intensities. The dbh was significantly smaller in the non-pollarded trees (‘No Use’) than in the pollarded ones (Table 3). Non-pollarded trees were tallest, and intensely pollarded trees were smallest. Thus, the intensely pollarded trees exhibited the lowest height/dbh ratio and the smallest vertical crown extension, crown projection area and crown volume. When calculated for the period 2000–2010, the crown efficiency (CE) did not differ among the plots. In contrast, the crown efficiency (CE) of the intensely pollarded trees was significantly higher than CE of the other tree groups when calculated for the period 1987–2010. For both time-spans, the intensely pollarded poplars also exhibited a significantly lower BAI than the non-pollarded specimens. The indices of resilience did not differ significantly between moderately and intensely pollarded trees and were not significantly different from the hypothetical median of 1, thus indicating that pre- and post-pollarding BAI values were similar. Furthermore, intensely pollarded trees had a significantly higher number of secondary

Table 2 Stand structure of the plots dominated by trees with different pollarding intensities. Pollarding intensity

‘No Use’

‘Moderate’

‘Intense’

Tree cover [%] Basal area [m2 ha1] Number of trees per plot [radius = 50 m] Stand density [trees ha1; without stumps] Tree age (all trees) min/mean/max [years]

20 5.94 95 121

13 13.72 102 130

7 14.73 88 112

35/47/ 91

25/66/159

53/90/ 142

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Table 3 Morphological parameters of the trees differing in the intensity of pollarding (means ±1 standard deviation); CBD, distance of the crown base to the soil surface; dbh, diameter at breast height; different letters indicate significant differences among the plots (post hoc Mann–Whitney-U-Test, with Bonferroni–Holm-correction; P < 0.05). Pollarding intensity

‘No Use’

‘Moderate’

‘Intense’

Mean dbh [m] Mean tree height [m] Height/dbh Mean vertical crown extension [m] Mean CBD [m] Mean crown projection area [m2] Mean crown volume [m3] Mean BAI (1987–2010) [cm2 year1] Mean BAI (2000–2010) [cm2 year1] Crown efficiency (1987–2010) Crown efficiency (2000–2010) Index of resilience [cm2 year1 (cm2 year1)1] Mean number of secondary stems and branches per tree Degree of hollowness [% of stem area] Degree of hollowness [% by radius] Percentage of hollow trees

0.24 ± 0.08 b 9.8 ± 2.1 a 43.3 ± 10.5 a 6.8 ± 1.2 a 4.3 ± 1.1 a 18.7 ± 8.4 a 80.8 ± 42.0 a 13.8 ± 5.5 a 15.6 ± 6.7 a 0.20 ± 0.04 b 0.22 ± 0.06 a – 1.5 ± 0.5 b 0.6 ± 1.7 b 3.1 ± 7.5 b 17.4

0.35 ± 0.11 a 8.2 ± 2.2 b 25.7 ± 9.6 b 5.9 ± 1.3 a 2.7 ± 0.7 b 11.2 ± 5.6 b 42.7 ± 25.8 b 10.7 ± 3.8 ab 9.4 ± 4.1 b 0.21 ± 0.03 b 0.20 ± 0.08 a 0.79 ± 0.36 a 2.0 ± 1.0 ab 20.8 ± 22.2 a 35.0 ± 29.9 a 65.2

0.39 ± 0.14 a 7.6 ± 1.8 c 21.1 ± 5.9 c 4.3 ± 0.9 b 3.1 ± 0.9 b 7.8 ± 2.7 b 21.8 ± 10.0 c 9.1 ± 3.6 b 5.6 ± 1.9 c 0.34 ± 0.14 a 0.20 ± 0.06 a 0.91 ± 0.40 a 2.7 ± 1.1 a 34.3 ± 22.6 a 52.3 ± 26.9 a 87.0

stems and branches than non-pollarded trees and exhibited the highest percentage of hollow stems and the highest degree of hollowness. On average, hollow trees were older than non-hollow specimens (Fig. S2B in the Supplementary Material), and tree age was significantly correlated with stem hollowness (r = 0.63, P < 0.001 for regressions of radius- or diameter-related stem hollowness (dependent variables) on tree age (independent variable)). However, ANCOVA revealed that the differences in the cross section area-related stem hollowness (brought about by different use intensities) did not depend on tree age, and that there was no significant interaction between stem hollowness and tree age (F = 0.751, P = 0.477). In the non-pollarded trees, the degree of hollowness (adjusted means) was still significantly lower than in both groups of pollarded poplars when tree age as the covariate was included (P 6 0.01). 3.2. Stem diameter increment The mean tree-ring width of non-pollarded trees was significantly higher than that of the moderately and intensely pollarded trees, which exhibited similar mean growth rates (Table 4). Hollow trees, which have been considered in calculating the chronologies, generally showed smaller ring widths than non-hollow trees. In the group of the non-pollarded poplars, the number of hollow stems was smaller than in the groups of the moderately and intensely used trees (Table 4). From the tree-ring chronologies (1911–2010), differences in the growth rate among the pollarding intensities became even more obvious. The mean indexed tree-ring widths of moderately and intensely pollarded trees were significantly lower than the indexed tree ring width of the chronology of the non-pollarded trees throughout the years (Fig. 2a). A strong increase in the tree-ring width of non-pollarded trees was observed after 1970, where the

highest values had been found (Fig. 2a). There was also a slight increase in the tree-ring width of the moderately and the intensely pollarded trees between 1970 and 1977, but the growth rate clearly dropped in 1978 (Fig. 2a). After 1980, the mean indexed tree-ring width slightly increased in these two tree groups, with higher radial increment rates of the moderately pollarded trees (Fig. 2a). In contrast, the increment of the non-pollarded trees slightly decreased after 1976 and increased after 1999, but still was higher than in the other two categories of pollarding intensity. For the same 100-year period, the mean basal area increment (Fig. 2b) showed slightly different chronologies without significant differences among the plots. The BAI of plot ‘No Use’ was even lower until the beginning of the 1970s than on the other two plots, but displayed the largest BAI during the time-span when pollarding took place (1975–1983). The BAI of the moderately and the intensely pollarded poplars clearly dropped within this time-span (Fig. 2b). 3.3. Formation and growth of secondary stems As there were no secondary stems >10 cm in non-pollarded trees, chronologies of such stems were only documented for moderately and intensely pollarded poplars. The age could be determined for 18 stems (out of 33) of moderately pollarded trees and for 23 stems (out of 36) of intensely used trees. The oldest secondary stem of moderately used poplars exhibited an age of 35 years (formed in 1975), and of the intensely used trees, of 43 years (formed in 1967). The majority of secondary stems was formed from the mid-70s to the mid-80s (Fig. 2b). Between 1988 and 2010, the growth rates of secondary stems from moderately and intensely used trees strongly decreased (Fig. 3). The growth rates of stems and main trunks of moderately and intensely used trees were similar, in particular after the year 1995 (Fig. 3).

Table 4 Mean tree-ring widths (mm; ±1 standard deviation) of trees subjected to different pollarding intensities (‘No Use’, ‘Moderate’ and ‘Intense’): mean tree-ring width of all trees (TRW), minima and maxima of the tree-ring width and mean tree-ring widths of hollow (TRW hollow) and non-hollow trees (TRW non-hollow); number in brackets = number of trees; different letters indicate significant differences among the pollarding intensities within a given type of shoot compartment (main trunk and secondary stem; Friedman-Test and post hoc Wilcoxon-signed-rank-Test; P < 0.05). TRW ‘No Use’ main trunk ‘No Use’ secondary stem ‘Moderate’ main trunk ‘Moderate’ secondary stem ‘Intense’ main trunk ‘Intense’ secondary stem

1.68 ± 1.29 – 1.11 ± 0.68 1.79 ± 0.69 1.19 ± 0.67 1.54 ± 0.42

(20) a (15) (20) (20) (20)

b a b a

Min

Max

TRW hollow

TRW non-hollow

0.36 – 0.26 0.51 0.29 0.73

5.02

1.57 ± 1.32 – 1.05 ± 0.63 1.36 ± 0.60 1.12 ± 0.60 1.42 ± 0.51

1.81 ± 1.28 – 1.18 ± 0.85 2.12 ± 0.56 1.23 ± 0.77 1.64 ± 0.32

2.88 2.93 3.99 2.36

(3) a (11) (15) (17) (16)

b a b a

(17) a (4) (5) (3) (4)

b a b a

P. Lang et al. / Forest Ecology and Management 353 (2015) 87–96 200

3.5

180

3.0 160

a

2.5

60 40

0.5

20 0

0.0

a

(b)

35 30

-1 2

5

2

1.0

-1

80

10

Mean annual BAI (cm yr )

b

100

b

Number of trees

120

2.0 1.5

15

140

25

Mean annual BAI (cm yr )

(a)

20

(a)

20 25

a 15

20

a

15

10 10 5

Number of branches (> 10 cm)

Mean indexed tree-ring width (+ offset) (mm)

92

0

(b)

20

15

10

5

0

5

1990

1995

2000

2005

2010

Year 0

0 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 2010

Year Fig. 2. (a) Radial stem increment (calculated from detrended tree-ring widths with offset according to Eq. (1)) and number of trees considered (graphs in the lower part of the panel); (b) mean annual basal area increment (BAI; lines) and number of newly formed branches (vertical bars) in each year; dotted line, trees without pollarding; black line and black vertical bars, moderately pollarded trees; grey line and grey vertical bars, intensely pollarded trees. Chronologies with the same letter do not differ significantly (Post-Hoc Wilcoxon-signed-rank-Test; P < 0.05).

Fig. 3. Mean annual basal area increment of the main trunk and secondary stems between 1988 and 2010; (a) moderately and (b) intensely pollarded poplars. Black lines, main trunk; dashed lines, secondary stems.

Table 5 Pearson correlation coefficients between mean annual basal area increment (BAI), crown area and crown volume; Pearson correlation was calculated for (i) unweighted crown area and crown volume, (ii) weighted with the ratio of vertical crown extension (VCE) to total tree height (H), (iii) weighted with the ratio of CBD (distance of the crown base to the soil surface) to total tree height and (iv) weighted with the ratio of CBD to VCE.

3.4. Tree increment and crown morphology Significant relationships were found between tree increment and crown morphology. Best results were achieved by multiplying crown area and crown volume with the ratio of vertical crown extension (VCE) to total tree height (Table 5). There was a significantly positive correlation between mean annual basal area increment and crown area (Fig. 4a) as well as crown volume (Fig. 4b).

BAI vs. crown area (i) Not weighted (ii) Weighted with VCE/H (iii) Weighted with CBD/H (iv) Weighted with CBD/VCE ** *

**

0.558 0.626** 0.374** 0.289*

BAI vs. crown volume 0.600** 0.635** 0.470** 0.405**

P < 0.01. P < 0.05.

4. Discussion 3.5. Intrinsic water use efficiency 4.1. Effects of pollarding on tree morphology and growth increment The intrinsic water use efficiency (iWUE), calculated on the basis of d13C values, was significantly higher in the non-pollarded than in the intensely pollarded trees within the time span 1955– 2010 (Fig. 5). In the non-pollarded trees, iWUE markedly increased between 1969 and 1975 and stayed at a high level until 2005. Intensely pollarded trees showed a slightly different trend. The iWUE also increased during 1975–1980, but dropped between 1980 and 1982, one year after the highest number of new stems had been formed (in 1979 and 1981; Fig. 5). Another drop in iWUE was obvious in 2002. There was a significant positive correlation between iWUE and the mean tree-ring widths (non-pollarded trees: r = 0.667, P < 0.01, n = 57; intensely pollarded trees: r = 0.828, P < 0.01, n = 57) as well as BAI (non-pollarded trees: r = 0.834, P < 0.01, n = 57; intensely pollarded trees: r = 0.858, P < 0.01, n = 57).

Our study confirms that pollarding intensity exerts a strong influence on the growth of P. euphratica. Intensely pollarded trees exhibited the lowest mean tree height. The larger dbh of the pollarded trees might have been due to the higher average age of the trees. Nevertheless, significant differences in crown morphology and stand structure were observed among the pollarding categories. In contrast to dense mixed forests in temperate zones (e.g. Pretzsch, 2014; Hajek et al., 2015), interaction among the tree crowns could not have been the cause for the differences in crown morphology due to the sparse cover of the poplar trees in the stands. It is also improbable that root competition plays a major role in the performance of the trees. Upon germination, P. euphratica seedlings gain access to the water table within a few months (Wang et al., 2015), and phreatophytic species growing in the

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Fig. 4. Relationship between mean annual basal area increment (BAI; main trunk) and crown area (a) or crown volume (b), both weighted by the ratio of vertical crown extension to total tree height. Triangles, non-pollarded trees; circles, moderately pollarded trees; squares, intensely pollarded trees. The regression lines have been calculated for all data pairs; ⁄⁄ = significant at P < 0.01.

Fig. 5. Intrinsic water use efficiency (iWUE) (means ±1 standard deviation) for the time span 1955–2010 in non-pollarded (dotted line) and intensely pollarded poplars (grey line). The chronologies differed significantly (Wilcoxon-signed-rankTest, P < 0.05).

Tarim Basin including P. euphratica can meet their nutrient demand by nutrient uptake from the groundwater (Arndt et al., 2004; Zeng et al., 2006). Therefore, competition among the trees at the root level should not play a significant role in plant performance once the poplars have attained access to the groundwater, what is obligatory for this phreatophytic species.

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The detailed analysis of the increment cores confirms our first hypothesis that in the pollarded trees, the indexed tree ring width is significantly lower than in the non-used trees throughout the years. We found a corresponding result for the basal area increment, which decreased significantly with increasing pollarding intensity (time period 1987–2010), or still was significantly smaller in intensely pollarded poplars compared to non-pollarded trees in the most recent period of time (2000–2010). A negative impact of pollarding on tree ring width has not only been found in temperate deciduous trees with a slow growth rate during maturity (Quercus robur; Rozas, 2005), but also in species with a high sprouting capability (Tilia x europaea; Jarvis and Marlow, 2000). Pollarding reduces the biomass and the area of the leaves, leading to a reduction of assimilates which finally causes a decrease in growth (Génard et al., 1998; Li et al., 2001). Between 1978 and 1980, the chronologies of the mean basal area increment of moderately and intensely used trees exhibited a particularly strong decrease. This coincides with the formation of new secondary stems, indicating high pollarding intensities from the end of the 1970s to the early 1980s. Thus, P. euphratica responded with an enhanced formation of secondary stems to a pollarding event. This response can be interpreted as a compensatory reaction, in which at least part of the lost biomass is being replaced (Tschaplinski and Blake, 1995; Gries et al., 2005). Ultimately, this results in the formation of an irregularly shaped crown. The formation of a crown that is subdivided into several parts (instead of forming a uniform crown) seems to be a widespread response of trees that have been subject to periodical removal of branches (Matyssek et al., 2010). In combination with the lower tree-ring and basal area increment of the pollarded trees, the enhanced formation of secondary shoots of these poplars is indicative of an increased allocation of assimilates towards the tree crown, which could – at least in part – compensate for the loss of crown biomass. Nevertheless, when calculated with BAI values averaged for the time period 1987– 2010, the significantly higher crown efficiency (CE) of the intensely pollarded trees (compared to the non- and moderately pollarded poplars) indicates that the crown development of these trees still lagged behind the stem diameter increment as a result of the severe disturbance of the tree crowns. In contrast, the lack of significant differences in CE among the three pollarding intensities in the most recent time period (2000–2010) can be interpreted as a recovery of the crown structure, but at the cost of a continuous reduction in BAI. From 1973 to 1985, the non-pollarded poplars showed a significantly larger mean basal area increment than the pollarded trees. A large amount of tree stumps within that plot indicated that logging had taken place. In theory, this could have caused the increase in growth due to removal of competitors. But the dendrochronological analysis of the tree stumps, whose time series had been synchronized with the chronologies of the main trunk, showed that logging took place not before the time period from 2003 to 2008. Thus, it is improbable that logging has caused the sudden increase in the stem diameter increment. Additionally, all plots are only sparsely covered by trees; therefore, above-ground competition between the poplars can be excluded. Instead, other factors have to be considered. Differences in water supply might have been a decisive factor, but as we have no records of the Tarim River discharge and of changes in the groundwater level for the given study area and time span, we have no evidence for a possible effect of water supply. The inner composition of a stem has a large effect on the stability of trees. Therefore, the degree of hollowness is a good criterion to estimate the tree stability. A ratio of remaining stem wall thickness to stem cross-sectional radius of 0.3 is often used as a critical threshold of stability (Mattheck et al., 1994; Mattheck and Breloer,

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1993; Gaffrey and Kniemeyer, 2002): if this ratio falls below 0.3, the tree stability is at risk (Gaffrey and Kniemeyer, 2002). Hollowness increases the danger of windbreak and hollow trees are more vulnerable to diseases as portals of entry for pathogens and saprophytes have been created. Moreover, the risk of drought damage increases as water can leave the trunk through holes, and water taken up by the roots can seep into the hollow trunk (we observed that water was leaking out when boring the increment cores). During winter, this can lead to frost wedging, which further decreases the stability of the tree. In addition, the stem’s capacity of carbon storage can be reduced if not only the heartwood but also the inner part of the sapwood becomes subject to decay. This can affect the tree’s physiological functioning such as growth and water conductance (e.g. Sala et al., 2012) what, in turn, could also reduce the tree’s capability of regeneration after loss of biomass. We found that the degree of hollowness in P. euphratica increased with pollarding intensity and was significantly higher in pollarded than in non-pollarded trees. This is in accordance with other studies showing that the probability of hollow formation increases with pollarding intensity (Sebek et al., 2013). In our study, intensely pollarded trees, in particular, were strongly affected by hollowness. Eight out of 23 (35%) investigated trees that had been intensely pollarded showed a ratio of wall thickness to cross section radius of less than 0.3, thus being classified as unstable. In the other pollarding categories, none of the investigated trees fell below this critical threshold. Although the degree of hollowness increased with tree age from non-pollarded to intensely pollarded trees, it is improbable that age is the decisive cause of the higher percentage of stem hollowness. Firstly, ANCOVA applied to our data sets revealed that the effect of the different pollarding intensities on stem hollowness was independent of tree age. Secondly, even the maximum age determined in the investigated trees (159 years) was not very high compared to the age that can be reached by these poplars. P. euphratica trees with an age of up to 300 years can easily be found along rivers of NW China (Li et al., 2010), and a maximum age of more than 700 years is documented for a tree found in eastern Xinjiang (Wang et al., 1996). Thirdly, only a very small fraction of trees with a hollow stem (two trees out of 75, belonging to an age class of 100–120 years) was encountered in near-natural P. euphratica stands at the middle reaches of the Tarim River (Westermann et al., 2008). This indicates that without pollarding, the formation of hollow stems is relatively rare under near-natural conditions at a tree age of approximately 100 years. And fourthly, older poplars growing around settlements bear a higher risk of being pollarded several times during their life cycle; thus, the older trees at our study site might have been pollarded more often than the younger trees that exhibited a lower degree of hollowness. Also in this case, pollarding rather than tree age would have been the decisive factor for the formation of hollow trees. For all these reasons, we conclude that the formation of hollow stems in the intensely pollarded trees of our study is mainly a consequence of biomass removal rather than of mere tree age. 4.2. Crown morphology and growth increment Collecting large tree ring data sets, especially from remote areas, is time consuming and costly. Thus, other approaches are to be used for conducting forest inventories on a landscape level. Remote sensing is an efficient method to assess the canopy structure of forest stands, the tree cover and the productivity of ecosystems on large areas (e.g. Sprintsin et al., 2009; Le Polain de Waroux and Lambin, 2012). A tight correlation between tree growth and tree morphology, established in terrestrial observations, would provide a sound basis for estimating the productivity of forest ecosystems on a regional and supraregional level using two- or

three-dimensional images derived from remote sensing. According to our second hypothesis, we found significant relationships between basal area increment and crown area as well as crown volume. This finding is promising for developing strategies to predict biomass production on larger geographical scales using remote sensing data. Such an approach could provide results that are more reliable than methods based on more indirect approaches using the leaf area index or chlorophyll reflectance (Tillack et al., 2014). 4.3. Compensatory response In the moderately and the intensely pollarded trees, the formation of a large number of secondary shoots is indicative of a compensatory response to pollarding. Compensatory biomass formation can be achieved by higher rates of photosynthesis due to wider or prolonged opening of the stomata, as has been detected in coppice shoots of hybrid poplar (Tschaplinski and Blake, 1995). At the leaf level, this would result in an increased influx of CO2 (and, necessarily, in an increased efflux of water vapour) and, at the cell level, in a stronger discrimination of the stable carbon isotope 13C during photosynthesis (Farquhar et al., 1989). In assimilates and in the biomass formed thereof, including wood, this should result in a more negative d13C isotopic ratio and thus lower iWUE (e.g. Scheidegger et al., 2000). Accordingly, we found a lower iWUE in the tree rings of the intensely pollarded trees than in the respective annual rings of the non-pollarded poplars throughout the investigated time period. Because all sampled trees grew under the same climatic and edaphic conditions, we can conclude that those differences in iWUE were due to the different pollarding intensities. It is improbable that changes in the shoot:root ratios upon the removal of shoot biomass by pollarding are the principal cause of the observed differences in iWUE. A previous study has shown that in P. euphratica, the stomatal resistance of the leaves is much closer related to the leaf-to-air difference in the partial pressure of water vapour than to the conductance to water on its flow path from the soil to the leaves (Thomas et al., 2008). On the basis of all these findings, our hypothesis of a compensatory production of secondary stem or branch biomass through increased carbon assimilation, accompanied by an increased use of water, can be maintained. Although the growth of P. euphratica is hampered by severe pollarding, it is capable of regenerating and, to a certain extent, of compensating for the removal of above-ground biomass. The long-term fluctuations in iWUE during the period of investigation may be due to alterations in the ground water table at a local or regional level induced by large-scale temperature changes in the region, which affected the rate of snow and glacier melting in the Tian Shan and, thus, the amount of water in the tributaries to the Tarim River and the Tarim River itself (Yao et al., 2004; Lang et al., 2013). 4.4. Conclusion The decline of P. euphratica stands is an ongoing process in the Taklamakan Desert due to an overuse of the water of the Tarim River, land reclamation by cotton farms and over-harvesting of wood (Hoppe et al., 2006). The population in this region has to deal with massive problems caused by woodland degradation in the course of desertification. It is therefore an important task to stop the further decline of P. euphratica stands. For a sustainable use of the tugai vegetation, the management efforts must be optimized. Several studies have already suggested guidelines for future sustainable management on the basis of the underlying ecological mechanisms (Thomas et al., 2006; Thevs, 2006b; Thevs et al., 2008b; Westermann et al., 2008). But none of these studies analysed the effects of pollarding on P. euphratica. We found that even

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an intermediate extent of pollarding resulted in a significant reduction in height and in diameter and basal area increment of the poplar trees and significantly increased the occurrence of stem rot. However, due to the possible negative effects of stem hollowness on the mechanical stability and physiological functioning of the trees, the increase in the risk of stem rot occurrence upon pollarding most probably is more deleterious to the trees than the removal of biomass itself. On the other hand, the species displayed a strong capability to regenerate from pollarding. This is also obvious from our finding that the crown efficiency did not significantly differ any more among the pollarding intensities when calculated with the BAI values of the most recent time period (2000–2010), and exhibited no significant difference at all between the non-used and the moderately pollarded trees. These results indicate that finally, the pollarded trees are capable of adjusting the growth of the crown to the increment of the main stem due to an increased allocation of assimilates towards the crown. Thus, a sustainable use of the species might be possible under moderate forms of pollarding, i.e. by harvesting only a small number of branches per tree with intervals of several years that allow regeneration of the crown. The exact threshold of injury caused to P. euphratica by pollarding that should not be exceeded in management schemes guided by principles of sustainability still has to be defined. The use of remote sensing on the basis of the relationship between crown dimensions and growth increment might help identifying this threshold on a landscape scale. Acknowledgements The study was funded by the German Federal Ministry of Education and Research (BMBF-Funding Measure ‘Sustainable Land Management’; project number: 01LL0918K). We thank two anonymous reviewers for their helpful comments, which significantly contributed to improving this paper. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2015.05. 011. References Arndt, S.K., Arampatsis, C., Foetzki, A., Li, X., Zeng, F., Zhang, X., 2004. Contrasting patterns of leaf solute accumulation and salt adaptation in four phreatophytic desert plants in a hyperarid desert with saline groundwater. J. Arid Environ. 59, 259–270. Coplen, T.B., Brand, W.A., Gehre, M., Gröning, M., Meijer, H.A.J., Toman, B., Verkouteren, R.M., 2006. New guidelines for d13C measurements. Anal. Chem. 78, 2439–2441. Cyffka, B., Rumbauer, C., Kuba, M., Disse, M., 2013. Sustainable management of river oases along the Tarim River (P.R. China) and the ecosystem services approach. Geogr., Environ. Sustain. 4, 77–90. Farquhar, G.D., Ehleringer, J.R., Hubick, K.T., 1989. Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. 40 (1), 503–537. Ferreira, T., Rasband, W., 2012. ImageJ User Guide – IJ 1.46r. (accessed 21.10.14). Fichtner, A., Sturm, K., Rickert, C., von Oheimb, G., Härdtle, W., 2013. Crown sizegrowth relationships of European beech (Fagus sylvatica L.) are driven by the interplay of disturbance intensity and inter-specific competition. For. Ecol. Manage. 302, 178–184. Fritts, H.C., 1976. Tree Rings and Climate. Academic Press, London, New York. Gaffrey, D., Kniemeyer, O., 2002. The elasto-mechanical behaviour of Douglas fir, its sensitivity to tree-specific properties, wind and snow loads, and implications for stability – a simulation study. J. For. Sci. 48 (2), 49–69. Génard, M., Loic, P., Kervella, J., 1998. A carbon balance model of peach growth and development for studying the pruning response. Tree Physiol. 18, 351–362. Gries, D., Foetzki, A., Arndt, S.K., Bruelheide, H., Thomas, F.M., Zhang, X., Runge, M., 2005. Production of perennial vegetation in an oasis-desert transition zone in NW China – allometric estimation, and assessment of flooding and use effects. Plant Ecol. 181, 23–43.

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