Growth and water relations of riparian poplar forests under pressure in Central Asia's Tarim River Basin

The riparian forests in the Tarim Basin (NW China) are mainly composed of poplar species (Populus euphratica, Populus pruinosa). In the hyper‐arid climate of this region, the trees are phreatophytes, which rely on access to groundwater. Essential ecosystem services (ESS) of these forests comprise provisioning, regulating, and cultural services. The ESS of the forests are threatened by overuse and a continuous decrease in the groundwater level due to excessive use of water for agriculture, which resulted in a severe reduction of the poplar forest area during the past decades.

originate from the Kunlun Mountain range and end up farther north in the desert.
Forests along those river shores grow in a climate that, according to the UNESCO-based definition of the ratio of average annual precipitation (P) to evapotranspiration (ET; Whitford, 2002), is hyper-arid (P/ET < 0.03 mm mm −1 ). Under these conditions and at an annual precipitation that, in some regions, is lower than 50 mm, the perennial plant species generally are phreatophytes in the sense of Meinzer (1923), which-for survival and growth-rely on temporary or even permanent access to groundwater for the uptake of water and mineral nutrients (Thomas, 2014). Euphrates poplar (Populus euphratica Oliv.; syn. P. diversifolia Schrenk) and pruinose poplar (P. pruinosa Schrenk) are the dominating tree species (Walter & Box, 1983), whereas the widely distributed co-occurring Tamarix ramosissima grows as a shrub.
In Xinjiang and other Central Asian regions, the rapidly growing human population and the pressure to produce cash crops such as cotton that are competitive on the global market even increase the pressure on the (near-)natural ecosystems. Thus, in many parts of Central Asia, ESS of the riparian forests are threatened by overuse, by a continuous decrease in the groundwater level, and by salinization. In the Tarim Basin, changes in the land use have resulted in a severe reduction of the poplar forest area during the past decades (Geist, 2005;Wang et al., 1996). At the northern rim of the Tarim Basin, excessive use of water for agricultural areas has led to a drastic drop of the groundwater level and to the decline of poplar forests particularly in the lower reaches of the Tarim River (Feng et al., 2005). Natural impacts such as the outbreak of insect herbivores in the mostly monospecific tree stands (cf. Gärtner, Förster, & Kleinschmit, 2016;Zheng et al., 2014) and sand storms (Hai et al., 2006;Xia et al., 1993), which might be aggravated through anthropogenic action, can exacerbate the pressure on the forests. The distance to the groundwater also affects phytodiversity (Zhang, Chen, & Pan, 2005). After degradation, possible recovery or new establishment of the forests seems to be dependent on controlled flooding (Tao, Gemmer, Song, & Jiang, 2008;Westermann, Zerbe, & Eckstein, 2008) or on the presence of a shallow groundwater table (Khamzina, Lamers, & Vlek, 2008). Therefore, a water release programme was launched in 2000 to supply the lower reaches of the Tarim River with additional ("ecological") water.
This article aims at reviewing recent studies on biomass production and water relations as crucial compounds of the tugai forests' functions and the responses of these functions to the principal pressures, with a focus on the past two decades of research in the Tarim River Basin. On that basis, we formulate management recommendations for the conservation of the forests against the background of climate change and dwindling resources. These recommendations may also be relevant for poplar-dominated riparian forests suffering from decreases in water supply in other (semi-)arid regions of Central Asia, for example, along the Amu Darya of Uzbekistan (Schlüter et al., 2013;Treshkin, 2001), and along the Syr Darya river system and in the Ili-Balkhash basin of Kazakhstan against the background of the prospected climate change (Nurtazin et al., 2019;Sorg et al., 2014).

| LIFE HISTORY AND REJUVENATION OF RIPARIAN POPLAR FORESTS
The tugai forests of the Tarim Basin cover an area of~352,000 ha and, thus, make up for some 54% of the world's Populus euphratica forests (Hai et al., 2006). At the river shores, P. euphratica can germinate from seeds only after intense flooding when the soil is sufficiently moist (Cao et al., 2012;Xu, Ye, & Li, 2009) and sufficient open space without competing vegetation is available (for comparable results on Salicacean species of the Northern Hemisphere, cf. González et al., 2018 andKarrenberg, Edwards, &Kollmann, 2002).
A continuously wet substrate also provides the most favourable condition for seed germination and seedling survival of other poplar species in temperate regions of Europe and North America (Guilloy- can grow rapidly down to the capillary fringe of the water table if the distance to the groundwater is not larger than 2 m (Thevs et al., 2008). Throughout the temperate zone of the Northern Hemisphere, Populus and Salix species of the Salicacean family are known to be particularly successful in rapidly colonising sediments on river shores after flooding (Karrenberg et al., 2002). During the life history of the trees and stands, the distance of the trees' aboveground parts to the groundwater often increases ( Figure 1) as a result of lowering of the groundwater level (upon changes in the course of the river, for example, Li, Yu, Brierley, Wang, & Jia, 2017;Thevs et al., 2008); of anthropogenic withdrawal of water from the river for extensive irrigation of agricultural land (Feng et al., 2005;Thevs, Peng, Rozi, Zerbe, & Abdusalih, 2015;Yimit, He, Halik, & Giese, 2006); or by wind-driven sand accumulation (Wang & Jia, 2013;Xia et al., 1993). To a certain extent, P. euphratica trees are capable of keeping pace with sand encroachment through height increment of the stem (cf. Gries et al., 2003). At larger distances to the groundwater, where seeds cannot germinate due to the absence of inundation, regeneration is only possible vegetatively through "root suckers." These are shoots emerging from horizontally running underground root sections (spacers) connected to the "parent" plant. Such shoots are initiated in soil depths down to~0.6 m and reach distances of up to 40 m from the "parent" tree (Wiehle, Eusemann, Thevs, & Schnittler, 2009). Thus, large clones can develop that cover areas of up to 121 ha (Vonlanthen, Zhang, & Bruelheide, 2010). However, the trees' capability to regenerate vegetatively through suckers decreases with increasing distance to the water table and is limited to a maximum groundwater distance of 8 m (Zerbe & Thevs, 2011). Therefore, P. euphratica stands growing at a large distance to the groundwater often are relatively old and sparse, whereas dense poplar stands containing a large fraction of young trees generally are only found at sites with a relatively small distance to the water table or to the riverbed .
When the distance of the trees to the groundwater becomes too large, the stand declines ( Figure 1). This life history of P. euphratica stands leads to the assumption that the percentage of clones in a given stand increases with an increase in the distance to the water table because sexual reproduction decreases. In recent studies, however, no straightforward relationships were found between the groundwater distance on one hand and the percentage of clones, the survival and the age of the stands on the other hand. Those studies were conducted at the middle reaches of the Tarim River (Eusemann, Petzold, Thevs, & Schnittler, 2013) and across a larger gradient of site conditions from the lower and the middle reaches of the Tarim River to the Aibi Lake (Ebinur) in the western part of north-eastern Xinjiang (Kramp et al., 2018). These results indicate that the genetic pattern of P. euphratica is not easily predictable even over small distances, but is a result of a complex interplay of stand history and dispersal of propagules (pollen, seeds, and vegetative diaspores) by wind and water. Thus, for the stand structure including its age distribution and the spatial and genetic relationships among the trees, the site history and, in particular, the pace of the decrease in the groundwater level may be at least as important as the lowering of the water table itself. Overall, the genetic diversity of P. euphratica across its distribution in north-western China is high (Wang, Li, Guo, Ren, & Wu, 2011). However, pure clonal stands can occur at sites where a high salt concentration of the upper soil prevents germination of the seeds (cf. Zhang et al., 2019) and establishment of the seedlings although the distance to the groundwater is relatively small (1.4-2.7 m; Kramp et al., 2018).
The understorey of the riparian forests harbours only some few shrub and herb species, whose number and abundance mainly depend on the distance to the river and to the groundwater and, thus, on the availability of water: species richness and abundance decrease with decreasing water supply (Thevs et al., 2008; Table S1 of the Supporting Information). In general, the alpha diversity of plant species is low along the Tarim River: up to only~30 vascular plant species have been found in a given plant community on flooded plots at the river's middle (Thevs et al., 2008) and lower reaches (Ling, Zhang, Xu, & Zhao, 2015) with P. euphratica and the shrub Tamarix ramosissima being the most abundant species. However, some species are important for medicinal use (Li et al., 2016; Table S1 of the Supporting Information).
F I G U R E 1 Schematic life history of Populus euphratica stands at the Tarim River (northern fringe of the Taklamakan Desert) across a sequence of groundwater distances and development stages from flooding and the germination of seeds (➀) to exclusively vegetative regeneration (➂) and the ultimate decline of the stand at large distances to the groundwater (➄)

| GROWTH AND BIOMASS PRODUCTION OF RIPARIAN POPLAR FORESTS
In young, dense, and highly productive stands in the Tarim Basin, the total above-ground wood biomass of P. euphratica can reach 56 Mg ha −1 -similar to the value of 58 Mg ha −1 determined at the middle reaches of the Amu Darya under comparable conditions-but is smaller at larger distances to the groundwater and to the river (Aishan, Betz, Halik, Cyffka, & Rouzi, 2018;Thevs et al., 2012;Thomas et al., 2017; Table 1). Although, in general, vigour (assessed through the extent of defoliation) and growth of P. euphratica trees decrease with increasing distance to the groundwater and the river at the stand level Halik, Aishan, Betz, Kurban, & Rouzi, 2019;Ling et al., 2015; Table 1), individual mature trees growing at larger distances to the groundwater (up to 12 m) can reach a similar annual productivity as trees of the same age class thriving at shorter distances to the water table . Attaining values of up to~3.3-3.4 Mg ha −1 yr −1 in a young (22 years, originated from clonal growth after clear-cutting; Gries et al., 2005) and a middle-aged stand (Wang et al., 1996) and 2.8 Mg ha −1 yr −1 in a mature stand (Table 1) Along gradients of water supply (distance to the groundwater or supply with additional "environmental flow" for restoration purposes) at two sites (middle and lower reaches of the Tarim River), the average tree-ring width and basal area increment (BAI) during four decades  were significantly higher in stands with the amplest water supply than in the stands with larger distances to the groundwater or smaller water supply (Lang et al., 2016). However, a more thorough analysis of productivity data revealed that, according to the life history of the trees (see section Life history and rejuvenation of riparian poplar forests), AAWP per unit soil-surface area was much closer related to the age and the density of the stands than to groundwater distances .
Around the year 2000, wood harvesting from living P. euphratica trees has been banned in any form in several regions of Xinjiang (cf. Bruelheide et al., 2003;Mamat et al., 2019), but in the past, forest productivity has distinctly decreased by intense wood harvesting through stem cutting or pollarding, that is, cutting of branches or large twigs. However, the trees are capable of (partly) compensating the loss of biomass through a more intense gas exchange and formation of secondary branches (Lang et al., 2015). In contrast, a moderate intensity of pollarding does not result in significant growth reduction and should be permitted to let the local population make use of this renewable resource (Lang et al., 2015). In a 22-year-old coppice stand, harvesting of 44-49% of the stems did not lead to a reduction in stem diameter increment, but even to enhanced growth in the subsequent year (Gries et al., 2005). Aboveground biomass productivity can be reduced by complete defoliation upon infestation with larvae of Lepidopteran species, which occurs every few years, and can result in a loss of~44% relative to years of high productivity at ample water supply (Schäfer, Saleh, Yu, Zhang, & Thomas, 2017).
Supply with additional ("ecological") water resulted in a marked increase in tree growth (Gärtner, Förster, Kurban, & Kleinschmit, 2014;Lang et al., 2016). Interannual fluctuations in the water supply led to distinct alterations in BAI in trees that grew at a short distance to the water table or were supplied with additional water. At the Tarim River's middle reaches, in the time period 1971-2011, when the course of the river was relatively constant, tree-ring increment and BAI exhibited a significantly positive relationship with the river discharge of the preceding year (which occurs in late summer and autumn, when the annual increment of the trees is already completed [Thomas et al., 2008] and, therefore, exerts no effect on the tree growth in the same year). However, this correlation was restricted to the stand growing at the shortest distance to the groundwater (2 m) and to the river's main course (Lang et al., 2016).
T A B L E 1 Structure of riparian poplar stands, above-ground wood biomass (AWB), and soil surface-related annual above-ground wood productivity (AAWP; 3-year average) on plots differing in groundwater distance or water supply at the upper, middle, and lower reaches of the Tarim River (means ± 1 standard error, where applicable) Notes: Different lower case letters indicate statistically significant differences among plots in a given region (Kruskal-Wallis test followed by post-hoc multiple pairwise Dunn's tests; data from Lang et al., 2015;Lang et al., 2016;Thomas, Jeschke, Zhang, & Lang, 2017). n.d., not determined. a EW, supply with additional "ecological water" in most years since 2000. b Determined from xylem sap flow according to Granier, Biron, Bréda, Pontailler, and Saugier (1996).

| WATER USE AND WATER USE EFFICIENCY OF RIPARIAN POPLAR FORESTS
Corresponding to the trees' permanent access to the groundwater, the annual water use of P. euphratica stands at the lower reaches of the Tarim River (up to 150 mm yr −1 ; Table 1)  According to the relatively high transpiration rates, the water use efficiency of above-ground productivity (biomass produced per unit water transpired) is rather low and, in the 22-year-old coppice stand, does, on average, not exceed 1.6-2.3 g dry matter (DM) per kg H2O (Thomas et al., 2006), which is markedly lower than in broad-leaved trees of temperate regions (3-5 g DM kg H2O −1 ; Larcher, 2003).

| MANAGEMENT MEASURES AND RECOMMENDATIONS FOR TUGAI FORESTS
Withdrawal of water, mainly for irrigation of agricultural fields along the upper and middle reaches of the Tarim River, as well as water retention through construction of reservoirs in the mountain areas (Chen, Ye, & Shen, 2011) are the main causes of the decline of the riparian forests, particularly at the lower reaches (Chen, 2014;Li, Zhou, Fu, & Chen, 2013;Zu, Gao, Qu, & Qiang, 2003). Therefore, a long-term programme has been launched in 2000 to divert additional ("ecological") water to the river's lower reaches to protect and con- Along the lower reaches of the Tarim River, forests cover an area of 33,700 ha (Chen, Li, Xu, Ye, & Chen, 2015). Mature P. euphratica stands growing at a groundwater distance of~5 m and supplied with "ecological water" transpire up to 150 mm yr −1 in that region (Table 1), amounting to 50.6 million m 3 yr −1 for the entire forest area.
This value is similar to the water consumption of 58.6 million m 3 yr −1 by forests of that region calculated by Chen et al. (2015) Chen et al., 2015), and very old and sparse stands with an assumed groundwater distance of 6.6 m (cf. Table 1), only 9.4 million m 3 yr −1 (or 13.2 million m 3 yr −1 according to Chen et al., 2015) when related to the entire forest area. Nevertheless, according to measurements and calculations, an amount of 160-300 million m 3 is being recommended to meet the water demand of these P. euphratica forests, that is, to lift the water table to a distance of 2-4 m below the soil surface (Chen et al., 2010(Chen et al., , 2015Ling et al., 2015), which is considered ecologically suitable for the growth of P. euphratica forests (Li et al., 2013 to regenerate from seeds upon flooding instead of diverting large quantities of water to stands with large distances to the groundwater, which are foredoomed to die off due to a dwindling ability to regenerate. Moreover, successful establishment of seedlings of typical riparian trees depends on the occurrence of bare, moist surfaces protected from disturbance, as has been shown for P. deltoides in western North America (González et al., 2018;Scott, Friedman, & Auble, 1996).
Along the Tarim River, concentrating additional water supply on forest stands with a short distance to the groundwater gains even more importance by the fact that during the past decades, the course of the river has become more constant due to lower rates of discharge (Thevs et al., 2008) and by embankment upon a large-scale construction of dykes . This results in progressively smaller zones along the riverbanks in which regeneration from seeds is possible.
Therefore It is recommended that • a moderate extent of wood harvesting by pollarding (cutting twigs and branches from trees) is allowed in case of P. euphratica growing at a short distance to the groundwater (up to 2 m); • a continuous and sufficient water supply to P. euphratica forests growing at short distances to the groundwater (up to 5-6 m) is ensured instead of diverting water to stands located at large distances to the groundwater.
These suggestions may be integrated in water management schemes that aim at protecting and conserving the unique riparian forest ecosystems in the Tarim River Basin and, simultaneously, allow a sustainable use of the forests. Such a strategy, which also might include active introduction of poplar trees (cf. González et al., 2018), is particularly important against the background of substantial mass losses of the Tian Shan glaciers, which constitute the source of the Tarim River water, due to the current climate change (Farinotti et al., 2015).

DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analysed in this study. Available references can be obtained by request to the corresponding author (FMT).