Black locust (Robinia pseudoacacia L.) ecophysiological and morphological adaptations to drought and their consequence on biomass production and water-use efficiency
© Mantovani et al.; licensee Springer. 2014
Received: 8 February 2014
Accepted: 11 November 2014
Published: 5 December 2014
Successful plantation efforts growing Robinia pseudoacacia L. (black locust) in the drier regions of Hungary and East Germany (Brandenburg), have demonstrated the potential of black locust as an alternative tree species for short-rotation biomass energy plantations.
The response of black locust to water limitation was investigated in a lysimeter experiment. Plants were grown under three different soil moisture regimes, with values set at 35%, 70%, and 100% of the soil water availability, namely WA35, WA70, and WA100. Their morphological adaptation and productivity response to water constraint were assessed together with their water-use efficiency. Furthermore, the ecophysiological adaptation at the leaf level was assessed in terms of net photosynthesis and leaf transpiration.
During the growing season, plants in the WA35, WA70, and WA100 treatments transpired 239, 386, and 589 litres of water respectively. The plants subjected to the WA35 and WA70 treatments developed smaller leaves compared with the plants subjected to the WA100 treatment (66% and 36% respectively), which contributed to the total leaf area reduction from 8.03 m2 (WA100) to 3.25 m2 (WA35). The total above-ground biomass produced in the WA35 (646 g) and WA70 (675 g) treatments reached only 46% and 48% of the biomass yield obtained in the WA100 (1415 g). The water-use efficiency across all treatments was 2.31 g L−1. At vapour pressure deficit (VPD) values <1.4 kPa trees growing under the WA35 soil moisture regime showed a stomatal down-regulation of transpiration to 5.3 mmol m−2 s−1, whereas the trees growing under the WA100 regime did not regulate their stomatal conductance and transpiration was 11.7 mmol m−2 s−1, even at VPD values >2 kPa.
Black locust plants can adapt to prolonged drought conditions by reducing water loss through both reduced transpiration and leaf size. However, under well-watered conditions it does not regulate its transpiration, and therefore it cannot be considered a water-saving tree species.
The production of biomass as a renewable resource for bioenergy has become increasingly important in Germany during recent decades. This had led to the promotion of an environmentally sustainable economy and increasing reliance on carbon-neutral renewable energy along with policies for reducing fossil fuel use and CO2 emissions. However, the traditional use of woody biomass as firewood is changing to a versatile source for larger biomass power plants. Short-rotation forestry (SRF) has great potential to contribute to such increased demands for growing woody biomass (Mitchell et al. ; Weih ; Grünewald et al. ). The planting of fast-growing trees for bioenergy can be an alternative land-use option on marginal land, where economically effective crop production is limited (Sinclair et al. ). Furthermore, interest in the ecological benefit of SRF for the restoration of ecosystem function (Lockwell et al. ) has increased considerably for recultivated post-mining areas (Šourková et al. ; Quinkenstein et al. ; Keskin and Makineci ). Water limitation and drought conditions in spring and summer are quite common in many regions, including in Brandenburg (Eastern Germany), where this experiment was carried out. Regional climate models for the next few decades are predicting changes to seasonal precipitation distribution and a summer rainfall decrease of 10-30% (Cubasch and Kadow ; Schaller ). Moreover, the intensification of extreme events will expand also across Europe over the next few decades, affecting ecosystem functioning (Jentsch and Beierkuhnlein ), tree distribution, growth rate, and productivity (Hickler et al. ). Successful plantation efforts growing Robinia pseudoacacia L. (black locust) in the drier regions of Hungary and East Germany (Brandenburg) (Rédei ; Rédei et al. ; Grünewald et al. ), with an annual mean precipitation lower than 600 mm yr−1, have demonstrated the potential of black locust as an alternative tree species for short-rotation biomass energy plantations. As a pioneer species, black locust is fast-growing and able to fix nitrogen from the atmosphere in considerable amounts (Xiao-rong et al. ). For example, Veste et al. () estimated an annual nitrogen fixation by black locust of 47.9 - 84.9 kg N ha−1 yr−1 on reclaimed post-mining land in Lusatia (East Germany). Furthermore, this tree species is known to be relatively drought tolerant compared with other temperate, deciduous tree species (Mantovani et al. , Veste and Kriebitzsch ). However, the native range of black locust in North America, humid to sub-humid climate, with a required annual precipitation of 1020 to 1830 mm (Schütt ). Until now, most studies on black locust have focused mainly on ecophysiological adaptations of this species to drought conditions (Veste and Kriebitzsch ; Liu et al. ; Zhang et al. ), emphasising its high ecophysiological plasticity. However, at the whole-plant level, biomass production sensitivity to water limitation is more related to plant growth performance and cell formation, rather than to carbon uptake and photosynthesis (Körner ). Consequently, a deeper understanding of the intertwined processes at both levels is needed in order to identify correlations between growth performance, biomass production, and transpiration of the whole tree under different soil water availability regimes and atmospheric boundary conditions. To study the consequences of water shortage, the number of variables involved in the soil-plant-atmosphere system was reduced by performing an investigation in lysimeters, under controlled environmental conditions. The aim of this study was to evaluate the impact of ecophysiological and morphological adaptation to water limitation on the biomass production and water use efficiency of black locust. Specifically, variation among water treatments at the whole-plant level was assessed in terms of a) transpiration, b) growth rate, c) leaf traits, and d) primary production. The results of this study provide detailed information on the physiology and biomass production capacity of black locust across a range of soil water conditions, which is essential for guiding future management strategies for short-rotation forestry.
Two-year-old saplings were collected from a short-rotation plantation in the post-mining area of Welzow-Süd, Brandenburg, Germany (N 51°36′14″, E 14°19′51″). The climate at the collection site is transitional between oceanic and continental. The mean annual rainfall is 556 mm and the mean annual temperature is 9.3°C (Meteorological Station Cottbus 1951–2003). Trees were selected in order to have a comparable trunk diameter (approximately 16 mm) and height (approximately 280 mm). To reduce variation in crown structure, clones presenting only three primary branches were chosen and these were cut back at 100 mm from the trunk before they were transplanted. The nine selected trees were planted directly in 15 L pots and over-wintered under a light-transmissive shelter to avoid frost damage. In March 2011, the young plants were transplanted into wick lysimeters (three trees per lysimeter; Mantovani et al. ; Ben-Gal and Shani ) and fertilised with 1045 mL of Hoagland standard solution (Hoagland and Arnon ) and 3.18 g of potassium dihydrogen phosphate (KH2PO4). The trees were well-watered in the lysimeters during the establishment phase until the start of the experiment in June 2011.
The nine wicked lysimeters used for water balance and growth performance evaluations were constructed as follows: polyethylene drums (1968 cm3, 25 cm radius × 50 cm depth) were filled with sandy loam soil at bulk density of 1.3 kg m−3, low in carbon (1.33%) and nitrogen (0.08%) Bulk density was estimated by using the thermo-gravimetric method (Jury and Horton ) while the total C and total N were estimated with the dry combustion method by using an elemental analyzer (Elemental Vario EL, LT Scientific, Inc. Nevada, USA). Water was supplied from an automatic drip-irrigation system, installed at the soil-atmosphere interface, only when the soil moisture reached values lower than the predefined values. Uncontrolled water input was avoided by installing the system under a light-transmissive roof and the evaporation was minimised by covering the soil with two separate geotextile layers. To control the irrigation amount and frequency, the soil moisture was measured at 20 cm depth with a Frequency Domain Reflectometry (FDR) probe (SM-200, Frequency Domain Reflectometry, Soil Moisture Sensor Delta-T Devices, Cambridge, UK). A supplementary FDR probe was installed at 40 cm depth to monitor the soil moisture gradient along the profile. To measure the soil matric potential, two gypsum tensiometers (SIS, UMS, München, Germany) were installed at 20 and 40 cm depth. Solar radiation and wind speed were recorded using a photosynthetically active radiation (PAR) sensor (QS2, Delta-T Devices, Cambridge, UK) and a switching anemometer (A100R, 119 Vector Instruments, Rhyl, UK) respectively) All measurements were logged at hourly intervals. The data were stored on data loggers (GP1, Delta-T Devices, Cambridge, UK) and transferred using a Global System for Mobile Communications (GSM) wireless data transmission system to an internet platform (WEBVis, Umweltanalystische Produkte GmbH, Cottbus, Germany). The daily mean vapour pressure deficit (VPD) was calculated from the daily mean temperature and relative humidity, measured from 9:00 to 18:00. The variation in water storage requirements for the weekly water budget calculation was obtained by measuring the soil moisture at four depths (10, 20, 30, and 40 cm) with a portable FDR profile probe (PR2/4w-02, Delta-T Devices, Cambridge, UK) on a weekly basis. Water use for a single plant during the growing season was evaluated from the experimental water balance. Water use efficiency (WUE) was calculated at harvest by the ratio between the total above-ground dry biomass (defined and determined below) produced from each tree and its cumulative water use. The economic water-use efficiency was calculated taking only the economically relevant woody biomass into account, since only the only the wood is harvested.
Water regime treatments
Description of the soil water availability conditions of the treatments
Number of trees
Number of lysimeters
Relative soil water availability
Soil water content
Soil matric potential
Biomass and leaf area
Net photosynthesis and transpiration
The gas exchange of fully expanded leaves was measured in situ employing a CMS400 minicuvette system (Heinz Walz GmbH, Effeltrich, Germany) (Midgley et al. ; Veste and Herppich ). Gas exchange measurements were carried out with ambient CO2 concentrations and the H2O and CO2 concentrations were determined with an infra-red gas analyser (BINOS 100-4P, Rosemount, Hanau, Germany). Each portion of leaf (couple of leaflets) was placed in the minicuvette for 5–6 minutes until a constant H2O signal was reached. Transpiration and CO2 exchange were calculated according to Koch et al. (). Leaf conductance for water vapour (gH2O) was calculated using the method of von Caemmerer and Farquhar (), with software DIAGAS 2.0 (Heinz Walz GmbH, Effeltrich, Germany), and all fluxes were calculated in relation to the projected leaf area. Each portion of leaf was scanned and its area measured by using the same digital image processing technique described in the previous section. During the measurements, the air temperature and relative humidity in the cuvette were kept constant and corresponded closely to the actual ambient VPD. Three days with different temperature and humidity conditions were selected: I) 20°C, VPD 0.7 kPa, II) 25°C, 1.4 kPa, and III) 32°C, 2.3 kPa, that represented typical summer days in July and August, and the minicuvette was adjusted to these actual temperature and humidity conditions. The illumination was set to a constant value of 1100 μmol m−2s−1 using an external halogen lamp to ensure the light-saturation of the photosynthesis.
This work involved investigation of plants at two levels: I) plant level for transpiration and growth performance and II) the leaf level for transpiration and net photosynthesis. As a result, the statistical analysis required the use of different analytic tools. Before performing the statistical tests, the data were tested for normality by the Shapiro-Wilk test. Regression analysis was used to correlate cumulative water use with soil water availability, and water use with biomass production. The non-parametric Spearman’s rho (α = 0.01) test was used to correlate transpiration rate, growth rate and VPD at the individual-leaf level and at the whole-plant level. A non-parametric analysis using the Mann–Whitney U-Test (α = 0.05) was performed to compare the treatments in terms of cumulative transpiration, total leaf area, trunk diameter, biomass production and WUE. For branch diameter and length increase, a parametric ANOVA, Post-Hoc analysis Tukey HSD (α = 0.05), was performed and a parametric Robust Test, Post-Hoc Games-Howell (α = 0.05), was used for the leaf traits. All the analyses were executed using IBM SPSS software, version 21 (SPSS Inc. Chicago, IL).
Plant growth rate
Relative trunk diameter and secondary branches diameter and length increases, recorded from the beginning of the experiment (1 June 2011) to the end (8 November 2011)
Trunk diameter increase1(%)
Secondary branches diameter increase2(%)
Secondary branches length increase2(%)
Leaf gas exchange
Increases in leaf transpiration for the WA70 and WA100 trees were not accompanied by an increase of the net CO2 exchange. The CO2 flux remained constant at all values of transpiration tested. Instead, there was linearity between the transpiration rate and the CO2 exchange rate for the trees from the WA35 treatment (r2 = 0.92), where the Spearman’s rho value was significant (r s = 0.857). At the leaf level, the WUE of the WA35 plants was more than 50% lower, compared with the plants from the two treatments with higher soil water availability (WA70 and WA100). However, this difference was statistically not significant due to the large within-treatment variation.
Various studies conducted on the drylands of China (Hu et al. ) and under the extreme edaphic conditions of post-mining sites in Bulgaria (Filcheva et al. ) and Eastern Germany (Böhm et al. ) have emphasised the growth potential of black locust on marginal land. The results presented here show how black locust responds to water limitation by reducing transpiration at both the individual-leaf level and at the whole-plant level, in relation to the climatic conditions. The differences in transpiration rates among the treatments were most pronounced during mid-summer and less significant in autumn, when the VPD was very low and leaves had senesced. The linear relationship between transpiration and biomass (wood and total above ground) production found in the current study is well supported at the whole-plant level by the homogeneity of the WUE among the treatments, i.e. 2.31 ± 0.46 g L−1 when total above-ground production was considered and 1.63 ± 0.39 g L−1 when only wood production was taken into account.
However, lower WUE values (0.32 to 0.71 g L−1) were obtained for black locust in a field experiment under semi-arid conditions on the Loess Plateau in Inner Mongolia (Hu et al. ). In another field study, Raper et al. () reported extremely low WUE values of 0.03 to 0.09 g L−1 in Georgia, USA. Higher WUE values have been found in other common tree species used for short-rotation For example Salix viminalis L. growing in northern Europe had WUE values in the range 4.1-5.5 g L−1 (Lindroth et al. ) while WUE values at different soil moisture regimes for Populus simonii Carrière, growing in the northwest region of the Loess Plateau (a highland area in north-central China) had ranged from 4.76 to 6.09 g L−1 (Liang et al. ). All these results are in line with the typical values estimated for a range of tree species growing in temperate climate zones where the water-use efficiency range lies between 1.42 and 6.66 g L−1 (Penka ). Comparable results were also found for well-watered Populus przewalskii Maximowicz and Populus cathayana Rehder plants with 4.08 and 4.6 g L−1 respectively, in an indoor experiment (Yin et al. ). Transpiration of black locust at both the individual-leaf level and at the whole-plant level was not limited by the stomata when soil water supply was optimal under the climatic conditions the current investigation. However, a limited soil water supply under the same climatic conditions resulted in a reduced transpiration rate, in order to minimise water loss. Similar behaviour has been observed for other broad-leaved trees (Gollan et al. ; Sperry ). That explains why towards the end of the growing season (October) the weekly transpiration mean was comparable between the treatments, even though the transpiring surfaces of the trees was significantly different. This confirms earlier findings about the leaf transpiration under well-watered conditions, where the leaf transpiration increased concomitantly with the VPD, while the net CO2 was nearly constant (Veste and Kriebitzsch ). As reported from other studies (Tipton and White ; Rashidi et al. ; Schurr et al. ; Niu et al. ), adaptation to water limitation also implies morphological changes. Among them, reduction in the dimensions of individual leaves (and consequently total leaf area) due to a water shortage are important morphological adaptations in order to control water loss (Xu et al. , Veste and Kriebitzsch ). The slow but constant growth of drought-stressed plants (WA35) in the current study indicates an adaptation to minimise water loss in a water limited environment. The drought-related decline in the area of individual leaves may be a consequence of a low turgor pressure impairing cell growth and expansion (Jaleel et al. ). Further limited transpiration had severe repercussions on the growth rate, as was shown here by reduced growth of the trunk and secondary branches. The recorded reduction in primary production at the whole-plant level was explained at the individual-leaf level by the linear relation between the transpiration and the CO2 exchange rate shown by the drought stressed plants (WA35). The well-watered plants (WA100) fluxes (CO2 and H2O) could only be limited by metabolic requirements of the plants and the atmospheric concentrations, rather than the constraints imposed by stomatal regulation, as already reported in literature (Körner ; Muller et al. ). Consequently, the identification of the combined effect of soil water availability and atmospheric evaporative demand as driving factors for the water use efficiency variability is crucial to understanding the response of the plants to different environmental conditions in terms of production.
The plants showed a high plasticity to water shortage, since drought stress at values close to the wilting point did not affect the plants’ functionality although it did affect their growth. Black locust has lower WUE than other species grown in short-rotation coppice species so is certainly not a low water-use tree species. Thus, growing black locust in a plantation setting may affect ground-water recharge and the local water budget. However, its ability to grow under adverse edaphic conditions plus other traits not studied here (such as high wood density and rot resistance) makes it a suitable species for marginal lands. Growth performance and morphological adaptations were more sensitive than the photosynthesis across the range of soil water availabilities tested, and hence growth is limited by factors other than photosynthetic C gain.
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