Summary We determined the response of Betula pendula Roth. trees to a restricted water supply, and quantified the interactions between tree N and water status on leaf demogra-phy and internal N cycling. In April 1993, 3-year-old trees were planted in sand culture and four treatments applied: high-N supply (56 mg tree−1 week−1) with either 2 dm3 water week−1 (HN+) or 0.9 dm3 water week−1 (HN−), or low-N supply (14 mg tree−1 week−1) with 2 dm3 (LN+) or 0.9 dm3 (LN−) water week−1. Until 1994, the N supplied to trees was enriched with 15N to 5.4 atom %.
During 1993, there were few differences in the growth or leaf demography of trees in the LN+ and LN− treatments, but the high-N treatment increased tree growth. Leaf mass and area were initially similar in trees in the HN+ and HN− treatments, but the trees in the HN− treatment had a smaller root system. Net assimilation rate under saturating light was higher in trees in the HN+ treatment than in trees in the LN+ treatment. There was an N × water supply interaction as a result of trees in the HN− treatment closing their stomata by the beginning of August. However, there was no difference in gas exchange characteristics of leaves in the LN+ and LN− treatments. Al-though leaf senescence and abscission started in the HN− treatment by mid-August and continued for about 90 days, whereas leaf abscission in the other treatments did not start until the beginning of October and only lasted 25--30 days, the trees in the HN+ and HN− treatments remobilized similar amounts of 15N for leaf growth in the spring of 1994. There were no differences in predawn water potential among treat-ments and no evidence of osmotic adjustment. We conclude that B. pendula trees avoid rather than tolerate drought. The interaction between the effects of nitrogen and water supplies on leaf demography and internal cycling of N are discussed. Keywords: birch, internal cycling, leaf senescence, remobiliza-tion, water relations.
Introduction
Much of the nitrogen (N) used by deciduous trees for growth each year can come from the internal cycling of stored reserves (Weinbaum et al. 1987, Millard and Proe 1991, Sanchez et al.
1991). A key process in such internal cycling is the withdrawal of N from leaves during senescence (May and Killingbeck 1992) for storage in shoots and roots during the winter, often as storage proteins in bark cells (Stepien et al. 1994). Remobi-lization of N from these storage proteins can contribute the majority of N used for leaf growth in the spring (Millard and Neilsen 1989, Millard and Proe 1991). However, the efficiency of N use by trees for growth may be regulated by environ-mental factors, including the availability of water (del Arco et al. 1991, Raison and Myers 1992).
Trees can respond to a shortage of water in several ways. First, drought can cause reallocation of assimilates thereby stimulating root growth (Khalil and Grace 1992, Lansac et al. 1994) and proliferation deep into the soil profile (Pallardy and Rhoads 1993). Second, in response to drought, some species maintain open stomata and leaf turgor by osmotic adjustment (Kleiner et al. 1992, Vivin et al. 1993). A third mechanism is drought avoidance, either by closing stomata (Gowing et al. 1990, Pereira et al. 1992), or, in the longer term, by leaf abscission (Escudero and del Arco 1987, Pallardy and Rhoads 1993). Premature leaf abscission caused by water stress may, in turn, result in a reduction in the amount of N withdrawn prior to leaf fall (del Arco et al. 1991), with consequent effects for N storage and remobilization.
Betula pendula Roth. is a pioneer species capable of growth on a wide range of sites, including sites of low fertility (Evans 1984). Under low-N conditions, over half the N used for leaf growth can be supplied by remobilization (Millard 1993). However, compared with other Betula species, B. pendula is less able to withstand dry sites and shows no capacity for osmotic adjustment (Ranney et al. 1991). Therefore, we tested the hypothesis that the response of B. pendula to drought is an alteration in root growth or leaf demography. We examined the effects of a restricted water supply on the growth, physiology and leaf abscission of B. pendula seedlings grown in sand culture for 2 years. Two rates of N were supplied, labeled with 15N during the first year, to determine: (1) if N availability influences the response of trees to a restricted water supply, and (2) if the response to drought affects the capacity of trees to store and remobilize N for leaf growth the following spring.
Impacts of water and nitrogen supplies on the physiology, leaf
demography and nitrogen dynamics of
Betula pendula
RENATE WENDLER
1and PETER MILLARD
1,2 1 Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB9 2QJ, U.K.2
Author to whom correspondence should be addressed
Received March 2, 1995
Materials and methods
Experimental design
Two hundred 2-year-old B. pendula saplings were lifted from a nursery while dormant and placed in cold storage until planted in pots (55 cm diameter × 45 cm deep) containing sand on April 6, 1993. The trees had previously received a moderate N supply. At planting, the saplings had a mean dry weight of 2.1 ± 0.3 g tree−1 and an N concentration of 14.7 ± 1.8 mg g−1 dry weight (DW). The pots were arranged in five randomized blocks in a greenhouse and watered to field capacity every 2 days with nutrient solution containing either 8.0 mol N m−3 (HN) or 2.0 mol N m−3 (LN) as NH4NO3. Other nutrients supplied were as described by Millard and Proe (1991). Trees designated for harvest in 1993 received N at natural abun-dance, whereas trees to be harvested in 1994 were given NH4NO3 enriched with 15N to 5.35 atom %. From early June, half the trees received 300 cm3 of the appropriate nutrient solution three times each week (HN− and LN− trees); the remaining trees also received the nutrient solution as described plus 550 cm3 of deionized water twice a week (HN+ and LN+ trees). At each of six harvests during 1993, one tree of each treatment was selected randomly from each block. In late summer, the trees were netted to ensure that no leaves would be lost during senescence. During winter, the dormant trees were kept frost-free and moist, and in February 1994, the trees were repotted in clean sand and kept moist until early March. Thereafter, trees were given a nutrient solution containing either HN or LN at natural 15N abundance. Four more harvests were taken during the spring and early summer of 1994. Harvested trees were removed from their pots and separated into leaves, stem, current stem, stem extension, tap root and fine roots. All plant samples were freeze dried, weighed and milled before analysis.
Measurements
Plant water status was assessed by measuring predawn water potential with a Scholander pressure chamber. Leaf gas ex-change (net CO2 assimilation and transpiration) was measured on fully expanded leaves with an open minicuvette system (H. Walz, Effeltrich, Germany) at ambient CO2 and relative hu-midity (ranging between 28.4 and 79.6%), 20 °C and saturat-ing light conditions (PFD between 1200 and 1400 µmol m−2 s−1). Measurements were taken between 1000 and 1600 h, because measurements of diurnal cycles showed no changes in gas exchange throughout the day. Plants were monitored for leaf abscission from July 22, 1993. From the start of leaf abscission, leaf litter was collected daily and the leaves counted. Leaf abscission was modeled as described by Dixon (1976). The numbers of fallen leaves each day were summed to give a cumulative distribution that was represented by the following model:
W(t)= LFt
exp((2.2/LF10--50)(LFmax−t)) ,
where W is the cumulative leaf fall (numbers), LFt is the total
annual leaf fall (numbers), LFmax is the time of maximum rate of leaf fall (days from January 1, 1993), LF10--50 is the time between 10 and 50% total leaf fall (days), and t is the time (days) from January 1, 1993. Genstat software was used to perform the analysis.
Total N plus 15N and total N were determined by ANA-SIRA mass spectrometry (VG IsoGas, Middlewich, Cheshire, U.K.), as described by Millard and Neilsen (1989). The 15N enrich-ment of tissue was used to calculate the uptake of labeled N (Millard and Neilsen 1989). During 1994, recovery of labeled N in leaves gave a direct measurement of N that had been taken up the previous year and remobilized from perennial tissues. Statistical analysis
To test for effects of nitrogen treatment, water supply and harvest dates, a three-way ANOVA was carried out. Because the assumption of equal variance was broken for dry weights and N contents, these values were log transformed.
Results
Tree growth
Dry weights of all organs (leaves, stem, current-year stem and total roots) were greater in HN trees than in LN plants (P < 0.001) (Figure 1). Increased leaf biomass in the HN trees was the result of both a greater number of leaves and a larger area per leaf. The total leaf area of HN trees was almost twice that of LN trees (Table 1). No increase in plant dry weight occurred after the end of September, indicating that trees were dormant over the winter. The reduced water supply had no effect on tree growth in the LN treatment, except for a decrease in leaf
growth in June and July (Figure 1), which was reflected in a reduction in both leaf number and total leaf area (Table 1). Reduced water supply had no effect on the dry weight of stem or current-year stem of plants in the HN treatment. However, the reduced water treatment resulted in a marginally lower dry weight of leaves (P < 0.05) when considered across all harvest dates and both N supplies, and in a smaller root system in HN− plants compared with the well-watered plants (P < 0.001, Figure 1). The reduction in total root dry weight of HN− plants was achieved by reductions in both tap root (P < 0.01) and fine roots (P < 0.05). On September 22, the dry weight of tap roots was 9 ± 1.4 and 6 ± 1.2 mg tree−1 and of fine roots were 58 ± 0.9 and 32 ± 2.4 mg tree−1 in the HN+ and HN− treatments, respectively.
Nitrogen content
The nitrogen content of all compartments was significantly greater in HN plants than in LN plants (P < 0.001, Figure 2). The water supply treatment had no effect on the N content of LN trees or on the N content of leaves and roots of HN trees; however, plants in the HN− treatment had a greater N content in the stem (P < 0.001) and current-year stem (P < 0.01) than plants in the HN+ treatment (Figure 2). On October 21, the maximum N contents of the plants were 985 ± 89 and 1024 ± 88 mg tree−1 in the HN+ and HN− treatments, respectively, and 315 ± 29 and 333 ± 26 mg tree−1 in the LN+ and LN− treatments, respectively, indicating that water supply had no effect on the rate of N uptake, even though root growth was reduced in trees in the HN− treatment compared with trees in the HN+ treatment (Figure 1).
Although N supply had a large effect on tree mass, it only had a small effect on leaf N concentrations. On August 25, before leaf senescence, leaf N concentrations were 22.3 ± 1.2 and 28.1 ± 0.4 mg gDW−1 in trees in the HN+ and HN− treatments, respectively, and the corresponding values for LN trees were 16.7 ± 3.2 and 19.3 ± 1.1 mg gDW−1. Trees in the HN− treatment also had a higher root N concentration than trees in the HN+ treatment, because their rate of N uptake was similar but root growth was less. The N concentrations in tap
roots were 5.7 ± 0.9 and 11.1 ± 0.6 mg gDW−1 in trees in the HN+ and HN− treatments, respectively, whereas fine roots of trees in the HN+ and HN− treatments had N concentrations of 8.8 ± 0.8 and 11.9 ± 0.6 mg gDW−1, respectively.
Leaf water potential
Leaf predawn water potential decreased in all treatments dur-ing the summer. The only significant treatment effect observed was in trees in the HN− treatment, which showed a less negative predawn water potential during the late summer and autumn than trees in the other treatments (Table 2).
Table 1. Effects of nitrogen and water supply on leaf number and area (cm2 plant−1) during the 1993 growing season. Values are the mean and standard error of five replicates.
Date HN+ HN− LN+ LN−
Leaf number
June 11 113 ± 3.2 119 ± 24.8 89 ± 11.6 59 ± 13.2
July 16 152 ± 13.4 201 ± 18.7 161 ± 37.0 118 ± 20.7
August 25 215 ± 10.0 164 ± 22.0 98 ± 16.0 116 ± 6.0
September 22 205 ± 15.7 162 ± 12.4 114 ± 18.6 104 ± 10.2
October 21 159 ± 13.2 140 ± 28.5 89 ± 9.8 96 ± 14.7
Leaf area
June 11 790 ± 51 808 ± 118 437 ± 67 304 ± 17
July 16 1316 ± 200 1661 ± 62 879 ± 226 572 ± 26
August 25 1700 ± 78 1368 ± 227 736 ± 82 734 ± 26
September 27 1742 ± 126 1262 ± 87 691 ± 48 725 ± 90
October 21 1449 ± 83 1051 ± 335 651 ± 63 643 ± 69
Assimilation and transpiration rates
Overall there was no statistically significant effect of N supply on net carbon assimilation rates (P > 0.05) (Table 3). However, there was an interaction between water and N supply such that trees in the HN− treatment had a significantly (P < 0.01) lower carbon assimilation rate per unit leaf area than trees in the HN+ treatment from August 12 onward. When the data were ex-pressed on a whole-tree basis, carbon assimilation rates were significantly lower (P < 0.01) in trees in the HN− treatment than in trees in the HN+ treatment from August 25 onward. No such effect was seen in LN plants (Table 3). Transpiration rates were also lower in trees in the HN− treatment compared with
trees in the other treatments from July 29 onward (P < 0.05).
Leaf abscission
Total annual leaf fall of HN plants was approximately double the number of leaves shed by LN plants (Table 4, Figure 3). The effect of N on the final number of shed leaves is consistent with the observed effect of N on leaf mass (Figure 1). Plants in the HN− treatment started leaf senescence earlier (end of August) than plants in the other treatments (early October) (Figure 3). The timing of maximum leaf fall was also earlier (6--8 days) in trees in the HN− treatment compared with trees in the other treatments (Table 4). A greater difference in the
Table 2. Effects of nitrogen and water supply on the predawn water potential (MPa) of Betula pendula at selected dates during 1993. Values are the mean and standard error of three determinations.
Date HN+ HN− LN+ LN−
June 11 −0.3 ± 0.02 −0.5 ± 0.08 −0.3 ± 0.02 −0.3 ± 0.04
July 17 −0.4 ± 0.04 −0.6 ± 0.07 −0.6 ± 0.07 −0.8 ± 0.1
August 4 −1.1 ± 0.15 −0.5 ± 0.13 −1.2 ± 0.14 −1.0 ± 0.18
September 1 −1.4 ± 0.13 −0.5 ± 0.11 −1.3 ± 0.12 −1.6 ± 0.21
October 9 −1.6 ± 0.14 −0.9 ± 0.13 −1.6 ± 0.12 −1.7 ± 0.2
Table 3. Effects of nitrogen and water supply on the gas exchange characteristics of Betula pendula at selected dates during 1993. Values are the mean and standard error of six replicates.
Date HN+ HN− LN+ LN−
Gas exchange per unit leaf area: Carbon assimilation (mmol m−2 s−1)
June 9 13.7 ± 4.0 12.0 ± 1.2 11.0 ± 1.9 8.5 ± 0.7
July 29 13.2 ± 0.6 11.3 ± 0.8 12.7 ± 0.7 12.8 ± 1.2
August 12 16.6 ± 0.9 4.2 ± 1.1 13.9 ± 1.2 13.3 ± 1.4
August 25 17.2 ± 1.7 8.6 ± 1.4 13.1 ± 1.5 14.8 ± 2.1
August 31 12.2 ± 1.4 5.4 ± 1.2 10.0 ± 1.3 8.9 ± 2.2
September 14 14.5 ± 1.0 8.5 ± 1.2 10.7 ± 0.5 8.5 ± 0.5
September 21 11.8 ± 1.4 7.4 ± 0.7 13.2 ± 2.5 11.1 ± 2.9
Transpiration (mmol m−2 s−1)
June 9 2.9 ± 0.8 2.9 ± 0.5 2.4 ± 0.3 2.5 ± 0.3
July 29 2.4 ± 0.2 1.4 ± 0.2 3.3 ± 0.2 3.8 ± 0.3
August 12 2.5 ± 0.3 0.3 ± 0.1 2.8 ± 0.4 2.0 ± 0.2
August 25 1.9 ± 0.4 0.4 ± 0.8 2.1 ± 0.4 1.7 ± 0.5
August 31 2.4 ± 0.2 0.5 ± 0.2 2.9 ± 0.4 1.8 ± 1.5
September 14 3.5 ± 0.4 1.1 ± 0.1 3.2 ± 0.3 2.1 ± 0.2
September 21 2.2 ± 0.3 1.1 ± 0.1 2.1 ± 0.2 2.5 ± 0.4
Gas exchange per tree:
Carbon assimilation (mmol s−1 tree−1)
June 9 0.7 ± 0.4 1.0 ± 0.1 0.3 ± 0.1 0.3 ± 0.1
July 29 1.7 ± 0.1 1.9 ± 0.1 1.1 ± 0.1 0.7 ± 0.1
August 25 3.0 ± 0.3 1.2 ± 0.2 1.0 ± 0.1 1.1 ± 0.2
September 22 2.1 ± 0.3 1.2 ± 0.1 0.9 ± 0.2 0.8 ± 0.1
Transpiration (mmol s−1 tree−1)
June 9 0.2 ± 0.06 0.2 ± 0.04 0.1 ± 0.01 0.1 ± 0.01
July 29 0.3 ± 0.02 0.2 ± 0.02 0.3 ± 0.01 0.2 ± 0.02
August 25 0.3 ± 0.06 0.1 ± 0.01 0.2 ± 0.03 0.1 ± 0.03
date of initial senescence than in dates of maximum leaf fall for HN− trees compared to the other treatments is reflected in a greater LF10--50 value for trees in the HN− treatment (Table 4).
Remobilization of N
The 15N recovered in the leaves during 1994 represented N taken up by the roots during the previous year, stored during the winter, and remobilized in the spring. Remobilization was complete by June 10, with HN trees remobilizing more N than LN trees (P < 0.001). However, the final amount of N remo-bilized in the spring of 1994 was unaffected by the water supply the previous year (Figure 4). Therefore, differences in leaf demography between trees in the HN+ and HN− treat-ments (Figure 3) had no effect on the amount of N stored during the winter and subsequently remobilized for leaf growth.
On June 10, 1994, the unlabeled N contents of leaves, derived from all sources, were 429 ± 32 and 409 ± 14 mg tree−1 for trees in the HN+ and HN− treatments, respectively. The
corresponding values for trees in the LN+ and LN− treatments were 217 ± 18 and 168 ± 17 mg tree−1, respectively. Therefore, remobilization had provided between 50 and 54% of the total N in the leaves by June 10.
Discussion
The results show that B. pendula trees avoid rather than toler-ate drought. When grown in the HN treatment, the response to a restricted water supply was stomatal closure to reduce tran-spiration and eventually premature leaf senescence. There was no evidence of osmotic adjustment, confirming the findings of Ranney et al. (1991). The main effect of the responses of HN trees to a restricted water supply was a reduction in root growth. A similar water-stress response has been reported for Betula seedlings by Osonubi and Davies (1981).
Abrams (1988) hypothesized that high nutrient availability enhanced a tree’s ability to withstand drought by maintaining physiological processes. Myers and Talsma (1992) found that predawn needle water potential of field-grown Pinus radiata D. Don could be independent of soil water content, but in-creased with both soil temperature and foliar N concentrations. However, in a study of two Quercus species, Kleiner et al. (1992) showed that fertilization did not ameliorate a drought-induced reduction in several measurements of physiological performance, including net photosynthetic rates, water use efficiency and leaf water potential, and furthermore, the re-sponse to drought was greater in fertilized trees than in unfer-tilized trees because rates of water depletion were faster. We found that the response to a restricted water supply was de-pendent on tree N status. Water supply had no significant effects on net assimilation or transpiration rates of LN trees; however, both of these physiological parameters were greater in LN trees than in trees in the HN− treatment from August 12 onward. Furthermore, the pattern of leaf abscission was similar in trees in the LN+ and LN− treatments, whereas trees in the HN− treatment exhibited leaf abscission sooner and over a longer period than trees in the other treatments. We conclude,
Table 4. Effects of nitrogen and water supply on the total annual leaf fall (leaf numbers) (LFt), the time of maximum rate of leaf fall from
January 1, 1993 (LFmax ), and the time between 10 and 50% total leaf
fall (LF10--50).
Treatment LFt LFmax LF10--50
HN+ 200.2 ± 13.7 303.5 ± 1.8 12.11 ± 2.0 HN− 223.5 ± 25.0 295.5 ± 3.4 27.00 ± 6.0 LN+ 104.5 ± 10.5 301.3 ± 1.2 10.73 ± 2.2 LN− 126.0 ± 12.6 301.8 ± 1.7 10.91 ± 2.5
Figure 3. Effects of N and water supply on leaf abscission of Betula pendula. The values are cumulative numbers of fallen leaves and represent the mean ± standard error of ten replicates. The best fitted curves of the model of Dixon (1976) are also presented (j) for HN+ (A), HN− (B), LN+ (C) and LN− (D) trees.
therefore, that HN trees grew more but were less able to withstand a restriction in their water supply than LN trees, because the N-induced increases in leaf number and area in HN trees resulted in a greater transpirational loss of water by the whole canopy compared with the LN trees.
In a study of a range of species, including B. pubescens J.F. Ehrh., del Arco et al. (1991) found an inverse relationship between the duration of leaf abscission and the proportion of N withdrawn. However, we conclude that the premature leaf abscission exhibited by trees in the HN− treatment in 1993 had no effect on the amount of N stored during the winter and remobilized for leaf growth in 1994, because the amount of 15N remobilized for leaf growth in the spring of 1994 was deter-mined by N supply alone and was unaffected by the amount of water supplied during 1993. The lack of response of the timing of leaf abscission on N remobilization was probably because the predominant source of N stored in the HN trees during winter was from N uptake by roots in the autumn, despite a reduction in the root growth of HN trees. Nitrogen uptake by tree roots can be rapid during canopy senescence (Millard and Proe 1991). Under conditions of generous N supply, which delayed leaf senescence of Malus domestica Mill., Millard and Thomson (1989) showed that root uptake of N compensated for the reduction of N withdrawal from leaves in augmenting N storage over the winter. In addition, Weinbaum et al. (1984) found that Prunus dulcis (Mill.) D.A. Webb trees retained 15N absorbed in the late summer and autumn in the roots and the more proximal, aboveground perennial tissues during winter, and suggested that late-season uptake of N was important in providing N for internal cycling. We found that, in trees in both the HN+ and HN− treatments, increases in the N contents of the roots and stems, and stem extension between October 21 and January 18 were sufficient to account for the majority of N remobilized the following spring.
We have shown that B. pendula trees avoid rather than tolerate drought stress by premature leaf abscission. The re-sponse of the trees to summer drought was dependent on N supply. Trees well supplied with N were less able to withstand a restricted water supply because of their greater leaf area. However, drought-induced leaf abscission is unlikely to affect internal N cycling and growth the following year, provided that N uptake can occur during the autumn and early winter.
Acknowledgments
We thank Sandra Galloway for skilled technical assistance, and the Scottish Office of Agriculture and Fisheries Department and the Euro-pean Commission (Contract STEP-CT90-0037) for funding.
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