Architectural plasticity and growth responses of Hippophae rhamnoides and Caragana intermedia seedlings to simulated water stress

ARTICLE IN PRESS

Journal of Arid Environments 69 (2007) 385–399

Journal of Arid Environments www.elsevier.com/locate/jaridenv

Architectural plasticity and growth responses of Hippophae rhamnoides and Caragana intermedia seedlings to simulated water stress W. Guoa,b, B. Lia, X. Zhanga,c,, R. Wangb a

Key Laboratory of Environmental Change and Natural Disaster of Ministry of Education, College of Resources Science, Beijing Normal University, Beijing 100875, PR China b College of Life Science, Shandong University, Jinan 250100, PR China c Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, PR China Received 4 July 2006; received in revised form 19 September 2006; accepted 12 October 2006 Available online 28 November 2006

Abstract The objective of this controlled experiment was to compare the ability of Hippophae rhamnoides L. (Sea buckthorn) and Caragana intermedia Kuang & H.C. Fu (Intermediate peashrub), both perennial temperate deciduous shrubs, to acclimate to a water deficit by architectural plasticity and growth responses. Their changes in branching pattern parameters, and in dry matter accumulation and allocation, were recorded after 2 years of exposure to four different water supply levels: normal precipitation, slight drought, drought and extreme drought. Their branching patterns showed that H. rhamnoides tended to expand horizontally, with more, shorter, thinner branches and a larger branch angle, whereas C. intermedia tended to grow perpendicularly with fewer, longer, thicker branches and a smaller branch angle. The overall bifurcation ratio and stepwise bifurcation ratio R1:2 of H. rhamnoides were comparatively steady; in contrast, those of C. intermedia increased markedly with an increase in water supply. The different adaptation strategies in biomass distribution pattern under different water supply treatments indicated that C. intermedia made a relatively high investment in root growth, especially in deeper roots, and in its changes in bifurcation ratio under water stress. H. rhamnoides grown under ample water supply was distinguished by its fast growth and

Corresponding author. Key Laboratory of Environmental Change and Natural Disaster of Ministry of

Education, College of Resources Science, Beijing Normal University, Beijing 100875, PR China. Tel./fax: +86 10 58808555. E-mail addresses: [email protected] (W. Guo), [email protected] (X. Zhang). 0140-1963/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2006.10.003

ARTICLE IN PRESS 386

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

relatively high investment in branches and leaves. The study revealed the ability of C. intermedia to adapt to a wider range of water stress by architectural plasticity and growth responses. r 2006 Elsevier Ltd. All rights reserved. Keywords: Branching pattern; Biomass allocation; Intermediate peashrub; Plant architecture; Sea buckthorn; Water deficit

1. Introduction Plasticity is one solution to the problem of adaptation to heterogeneous environments. Plant morphological plasticity (i.e. ability to alter growth) enables a plant to change its growth pattern as it encounters different soil conditions (Hutchings, 1988). Because of the importance of heterogeneous environments in the ecology and evolution of most species, plasticity has been of great interest to ecologists and evolutionary biologists for many years (e.g. Derner and Briske, 1999; Gautam et al., 2003; Sultana, 2004; Via et al., 1995). Plasticity in growth rate increases the variety in architecture within a species (Takahashi, 1996; Wu and Hinckley, 2001); as a result, architectural variation in different environments may to some extent reflect different adaptation strategies (Ho et al., 2004; Horn, 1971, 1979; Klich, 2000; Salemaa and Sieva¨nen, 2002; Schnitzler and Closset, 2003). In the modular plant models growth results from the interaction of plant organs and their environment (Eschenbach, 2005; Jones, 1985; Middelhoff and Breckling, 2005) and plant productivity is limited by water availability in most terrestrial ecosystems (Ho et al., 2004). However, the architectural plasticity of modular plants in response to water stress has been studied relatively little. The Yellow River brings great quantities of muddy sand into the Bohai Sea, and the river’s middle reaches pass through an easily eroded plateau called the Loess Plateau (Guo et al., 2003). In the north of the Loess Plateau and the middle of the farming-pastoral ecotone of North China, which is sensitive to climatic variation, particularly to precipitation change, lies Huangfuchuan watershed, which is the fixed research site of the ‘Eco-productive Paradigm’ project representing the landscape type of Sediment-Rock zone of the Yellow River valley (Zhang and Shi, 2003). Here, the main problems for plants are the scant precipitation and severe soil erosion. Hippophae rhamnoides L. (Sea buckthorn) and Caragana intermedia Kuang and H.C. Fu (Intermediate peashrub) are perennial, temperate, deciduous shrubs with a high degree of drought tolerance. Both are widely planted in an agro-pastoral transition zone in the semiarid area of northern China for afforestation, water and soil conservation, and desertification control and prevention, in recognition of their early successional nitrogen fixing, varied adaptability and economic importance. In particular, H. rhamnoides has on average been planted on 60 000 h m2 of the Loess Plateau every year since 1985, but at the same time many problems have arisen. For example, H. rhamnoides grows quickly when water is abundant and rapidly covers the ground. Its high consumption of water in the plant community has led to the continual decline of the soil water content. There was severe drought for the 3 years from 1999 to 2001 in Huangfuchuan watershed, with an annual precipitation of less than 300 mm, which resulted in the successive death of H. rhamnoides in large areas, and even extinction at some sites, whereas C. intermedia survived.

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

387

On account of this, water relations have to be taken into consideration if planting H. rhamnoides or C. intermedia in natural ecosystems and on restoration sites of arid areas. However, up to now, there still exist controversies over their drought-resistance mechanisms and adaptive strategies, and few researches have been reported on the effects of precipitation changes and water stress on H. rhamnoides or C. intermedia (Guo et al., 2004; Li et al., 2005; Zhang, 2005). Therefore, in this study, an artificially controlled water gradient experiment was carried out, based on four levels of water supply: mean precipitation, slight drought, drought and extreme drought. The main objective of the present study was to compare the ability of H. rhamnoides and C. intermedia to acclimate to a water deficit by architectural plasticity and growth responses. 2. Materials and methods 2.1. Study site and species The experiment site was at the ecological field experiment station of Beijing Normal University in Huangfuchuan watershed (39145.100 N, 111107.490 E, 1099 m a.s.l.). Huangfuchuan River, a tributary of the Yellow River, originates from an easily eroded plateau called the Loess Plateau. In Huangfuchuan watershed, a typical semi-arid area, the terrain consists mainly of exposed arsenic sandstone. The annual average temperature is 6.2–7.2 1C. The annual average precipitation for 40 years (1961–2000) in Huangfuchuan watershed was 389.75 mm, of which 77% falls during June to September, most of it in the form of rainstorms. A runoff experiment done locally (Jin et al., 1992; Wang et al., 1999) showed an approximate 20% loss of precipitation in the forms of runoff and seepage under the same natural conditions as in the present experiment. Few natural forests or grasslands remain. The only trees (such as Pinus tabulaeformis Hort. ex K. Koch, Populus simonii Carrie`re and Pinus sylvestris L. var. mongolica Litvin) have been planted, as have shrubs including C. intermedia and H. rhamnoides along with artificial grassland. H. rhamnoides (Elaeagnaceae) is a perennial, temperate, deciduous shrub, with stout thorn. It is widely distributed in the temperate zone of Eurasia, which in China is distributed in northeastern, northwestern and northern China (Editorial Committee for Flora of China, 1983). C. intermedia (Leguminosae) is also a perennial, temperate, deciduous shrub. It is widely distributed throughout northwestern China and usually establishes itself in sandy shrubland or brushy grassland communities (Editorial Committee for Flora of China, 1993). 2.2. Experimental design and materials We built a fixed field experiment station with cement pools in order to conduct a controlled experiment to simulate variable water stress during 2 years. Sixteen separate cement pools (0.6 m depth, 2 m length and 1 m width) were constructed in the station. There was a pipe on the bottom of each pool in order to drain unwanted water from the pools. All pools were below the great greenhouse. During the experiment, the top of the greenhouse was exposed to sunshine, and was covered with waterproof cloth to exclude the effect of natural rains; the surrounding sides of the canopy were open in order to make the other environmental factors similar to natural conditions.

ARTICLE IN PRESS 388

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

Each cement pool was filled with uniform sandy loess to a depth of 0.5 m on May 7, 2002. Its saturated water content was 23% by mass, the largest volumetric water content 35% and porosity 35%. One hundred and sixty 1-year-old H. rhamnoides seedlings from the Shagedu Nursery near the Experiment Station, all of approximately the same size, were randomly divided into eight groups. These eight groups were then planted into eight cement pools. Eight groups of C. intermedia seedlings, divided in the same way, were then planted into the other eight cement pools. All sand pools were managed well, weeded regularly and sprayed with insecticide during the growing season. 2.3. Water supply treatment and the measurement of soil water content Water was supplied from the last half of May 2002. The National Climate Center of China recognizes a climatological scale as follows: if the precipitation is 50% higher than a multiple-year mean value, it is called a high year; if 20% higher, a slightly high year; if 50% less, a low year; and if 20% less, a slightly low year. These years are regarded as abnormal years, and if the precipitation deviates within 720%, it is a normal year. On the basis of these criteria, the annual average precipitation for 40 years in Huangfuchuan watershed, and the runoff experiment done locally, we used an artificial water supply of 315, 227.5, 167, and 115 mm, designated W4, W3, W2, and W1, respectively, in order to simulate normal conditions of annual precipitation, slight drought, drought and extreme drought. Each water treatment was replicated. The proportion of the water supply to be allocated each month was determined on the basis of the mean precipitation in every month during 1961–2000 in the study area; the mean monthly precipitation (%) is 0.6, 0.9, 2.7, 4.6, 7.6, 11.4, 26.0, 26.7, 12.6, 5.0, 1.6 and 0.3 from January to December, respectively. During the experimental period, every cement pool was installed with an FDR (Frequency Domain Reflectometry) ATS1 PR1/4 tube (Delta-T Devices Ltd., UK). Volumetric soil water content (y) at four levels, i.e. at 10, 20, 30 and 40 cm depth, were determined by using a FDR Profile Probe on 5 consecutive days every mid-month. Calibration was done according to oven measurement. Regression analysis from 180 pairs of FDR readers (x) and oven values (y) measured in phase, was accomplished with the regression equation y ¼ 0:01 þ 0:36x ðR2 ¼ 0:80; r ¼ 0:88; n ¼ 180; po0:001Þ.

ð1Þ

2.4. Architectural and growth characteristics Branch orders were determined by the Strahler method (McMahon and Kronauer, 1976). At the end of the experiment, total branch number, primary branch number, secondary branch number and leaf number were counted on each shoot. Shoot height and each branch length were measured by ruler, stem and branch diameter by an electronic vernier caliper, branch angles by protractor. Crown area (p  shoot vertical projection length  vertical projection width/4) was determined. The overall bifurcation ratio, Rb, was measured by the formula Rb ¼ ðN T  N S Þ= ðN T  N 1 Þ (Steingraeber and Waller, 1986; Whitney, 1976), where NT is the total branch

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

389

number, NS is the branch number of the highest order, and N1 is the branch number of the first order. The stepwise bifurcation ratio, Ri:i+1, was measured by the formula Ri:iþ1 ¼ N i : N iþ1 (Fisher, 1986), where Ni is the branch number of the order i, and Ni+1 is the branch number of the order i+1. All plants were harvested and separated into roots, stems and leaves. The root material was divided into levels 1, 2, 3 and 4, which corresponded with depths of 0–15, 15–25, 25–35 and 35–50 cm. All harvested material was oven-dried at 85 1C for 48 h and then weighed. Dry matter biomass allocation parameters were calculated, such as root:shoot ratio (root biomass/branch and leaves biomass), photosynthetic biomass ratio (leaf biomass/total biomass), non-photosynthetic biomass ratio (branch and root biomass/total biomass), ratio of photosynthetic to non-photosynthetic biomass (leaf biomass/ branch and root biomass), and ratio of level i to root biomass (root biomass at level i/root biomass). In addition to the dry matter biomass, the fresh weight of the leaves from each shoot was determined soon after harvesting. Subsequently, saturation leaf weights were measured after immersion in water for at least 24 h. Water saturation deficit (g g1) was calculated as described by Beadle et al. (1993). Leaf area was measured by Laser Area Meter CI-203 (CID, Inc., USA). Leaf area ratio was calculated by leaf area/total biomass, according to Hughes and Freeman (1967). 2.5. Statistical analyses Calculations and statistical analyses were performed with MS Excel 2000 and SPSS 10.0 for Windows. The above-mentioned characteristics were tested with analysis of variance (ANOVA) and Duncan’s multiple range test, marked by letters, where the values sharing the same letters are not significantly different at the p ¼ 0:05 level. 3. Results 3.1. Soil water content ANOVA indicated a significant effect of water gradient on soil water content. Although, soil water content tended to increase along with the water gradient, the soil water content of the highest water gradient, W4, was not the largest (Fig. 1). 3.2. Shoot height, stem diameter and crown area Water supply had a marked effect on shoot height, stem diameter and crown area; these characteristics all increased significantly as water supply increased. Compared with C. intermedia, the crown area of H. rhamnoides was more sensitive to water stress, decreasing more markedly with increasing water stress. 3.3. Branching pattern characteristics Different branching pattern parameters responded to water supply differently. Almost all of them increased significantly along with the increase in water supply, except for mean branch length, mean branch diameter and mean branch angle (Fig. 2).

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

390

Soil water content (%)

7

a

6

a b

5

d

ab

b c

c

4 3 H. rhamnoides W1

W2

C. intermedia W3

W4

a b

90 c

60

a

d 30 c

b

b

Mean branch length (cm)

0 a

a

15

a

12 9

a

6

b

b

2.5

a

3

a

a 2.0

b

1.5

a

1.0

ab

a

b

b

a

b

0.5 0.0 60

a

Mean branch angle (°)

Total branch number

120

Mean branch diameter (mm)

Fig. 1. Changes in soil water content of H. rhamnoides and C. intermedia plots with gradient in water supply. Boxes represent means and error bars represent7SE of the means (n ¼ 40). Values with different letters are significantly different at the 0.05 level (Duncan’s multiple range test).

b

50

a

40

a bc c ab

30 20 10 0

0 H. rhamnoides W1

W2

C. intermedia W3

W4

H. rhamnoides W1

W2

C. intermedia W3

W4

Fig. 2. Changes in branching patterns of H. rhamnoides and C. intermedia with gradient in water supply. Boxes represent means and error bars represent7SE of the means (n ¼ 40). Values with different letters are significantly different at the 0.05 level (Duncan’s multiple range test).

Between H. rhamnoides and C. intermedia, there were marked differences in almost all branching pattern parameters. Total branch number, primary branch number, secondary branch number, total branch diameter, total branch length, total branch angle and mean branch angle of H. rhamnoides were all more than those of C. intermedia, whereas mean branch diameter and mean branch length were less (Fig. 2). The response of bifurcation ratio to water supply differed significantly between H. rhamnoides and C. intermedia. Overall bifurcation ratio and stepwise bifurcation ratio R1:2 of H. rhamnoides were comparatively steady; the stepwise bifurcation ratios R2:3 under W2, W3 and W4 conditions were coincident generally but they were all significantly larger

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

391

than that of W1. Overall bifurcation ratio and stepwise bifurcation ratio R1:2 of C. intermedia improved significantly with the improvement of water supply, while the response of stepwise bifurcation ratio R2:3 to water supply is nearly a curve of converse bell (Fig. 3). 3.4. Leaf characteristics

8

a a

6

a

a a

bc

4

b

c

2

Stepwise Bifurcation ratio R1: 2

0 8

Stepwise Bifurcation ratio R2: 3

Overall Bifurcation ratio Rb

Leaf number, and leaf area ratio of H. rhamnoides were larger than those of C. intermedia, and water saturation deficit was similar in the two species (Fig. 4). Different water supplies had significant effects on leaf characteristics. Along with the enhancement of water supply, leaf number, leaf area and leaf area ratio increased, while water saturation deficit fell significantly (Fig. 4). Water supply and plant species interacted in terms of leaf number, leaf area, leaf area ratio and water saturation deficit, at the 0.001, 0.001, 0.05 and 0.01 levels, respectively.

25

6

a a

a

a

bc

a

4

b

c

2 0 a a

20 15

a

b

10 ab 5

b

a

a

0 H. rhamnoides W1

W2

C. intermedia W3

W4

Fig. 3. Changes in bifurcation ratio of H. rhamnoides and C. intermedia with gradient in water supply. Boxes represent means and error bars represent7SE of the means (n ¼ 40). Values with different letters are significantly different at the 0.05 level (Duncan’s multiple range test).

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

392

a b

800 c 400

d

Water Saturation Deficit (g g−1)

d

a

b

c

Leaf area (cm2)

1200

1600 b

40 a c

b d

0.4

c

c

0.2 0.0 H. rhamnoides W1 W2

c

c

400

0.8 b

b

800

0

a

a

1200

0

0.6

a

2000

Leaf area ratio (cm2 g−1)

Leaf number

1600

d

d

bc

ab

a

30

a

20

c

a

a

b

10 0

C. intermedia W3 W4

W1

H. rhamnoides W2

W3

C. intermedia W4

Fig. 4. Changes in leaf characteristics of H. rhamnoides and C. intermedia with gradient in water supply. Boxes represent means and error bars represent7SE of the means (n ¼ 40). Values with different letters are significantly different at the 0.05 level (Duncan’s multiple range test).

There was a reduction in Leaf Area Index (LAI; the ratio of total leaf area to the area of ground covered by the plant) due to a decrease in total leaf number with decreasing levels of water supply, as well as poor expansion of individual leaves. The LAI of H. rhamnoides from W1 to W4 was 0.101, 0.345, 0.815 and 1.755; the LAI of C. intermedia was 0.091, 0.360, 0.776 and 1.231, respectively. 3.5. Biomass There was no statistically significant difference in branch biomass between H. rhamnoides and C. intermedia. Leaf biomass of H. rhamnoides was greater than that of C. intermedia, while root biomass, total biomass and root biomass at each soil layer level were less. Water supply had significant effects on all parameters of biomass, such as branch biomass, leaf biomass, root biomass, total biomass and root biomass at each soil layer level, all of which increased with the increase in water supply. The response of plant biomass to water supply was very similar to those of shoot height, crown area, stem diameter and leaf number. 3.6. Biomass allocation There was a significant difference in biomass allocation between H. rhamnoides and C. intermedia. Photosynthetic biomass ratio, ratio of photosynthetic to non-photosynthetic biomass, and ratio of level 1 to root biomass of H. rhamnoides were higher than those of

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

a

1.2 0.8

1.0 b

a

ab

b

b

bc c

0.4

Non-photosynthetic biomass ratio

Root to shoot ratio

1.6

a

a a

b

b b

a

c

0.1 0.0 0.8 a b b

b

a

b

0.4

c

c

0.2 0.0 0.2 a b

a ab ab

c

a

b

0.1

0.0 H. rhamnoides C. intermedia W1 W2 W3 W4

Ratio of photosynthetic Ratio of level 2 to root biomass to non-photosynthetic biomass

0.3

Ratio of level 4 to root biomass

Photosynthetic biomass ratio Ratio of level 1 to root biomass Ratio of level 3 to root biomass

0.4

0.6

b

0.8

b b

c

b b

0.6 0.4 0.2 0.0

0.0

0.2

a

a

393

0.4

a

a a

0.3 b

0.2

a

b b c

0.1 0.0 0.5 0.4

a

a

a

a a

b

ab b

0.3 0.2 0.1 0.0 0.2 a

a

a 0.1

b

b

b b

b

0.0 W1

H. rhamnoides C. intermedia W2 W3 W4

Fig. 5. Changes in biomass allocation of H. rhamnoides and C. intermedia with gradient in water supply. Boxes represent means and error bars represent7SE of the means (n ¼ 40). Values with different letters are significantly different at the 0.05 level (Duncan’s multiple range test).

C. intermedia, whereas root:shoot ratio, non-photosynthetic biomass ratio, and the ratios of levels 2, 3 and 4 to root biomass of H. rhamnoides were lower under the same water supply conditions (Fig. 5). This indicated that H. rhamnoides is a comparatively shallowrooted shrub.

ARTICLE IN PRESS 394

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

Water supply had significant effects on biomass allocation in these species. In general, more intense water stress was accompanied by greater root to shoot ratio, nonphotosynthetic biomass ratio, and ratio of level 1 to root biomass, but by smaller photosynthetic biomass ratio, ratio of photosynthetic to non-photosynthetic biomass, and the ratios of levels 3 and 4 to root biomass (Fig. 5). 3.7. Interactive effects As shown in Table 1, different water supplies and plant species had no significant interactive effects upon shoot height, stem diameter, branch biomass, total biomass, root biomass at levels 1 and 4, and all biomass allocation parameters except for root to shoot ratio; however, they had significant interactive effects upon crown area, all branching pattern characteristics except for mean branch length and mean branch angle, leaf characteristics in terms of leaf number, leaf area, leaf area ratio and water saturation deficit, leaf biomass, root biomass, and root biomass at levels 2 and 3. 4. Discussion Water limitation is one of the most general types of stress experienced by plants and is a main factor limiting plant growth. The survival of the plants to adverse conditions requires plasticity responses and plants may develop stress avoidance mechanisms by an adequate architectural plasticity (Gautam et al., 2003; Ho et al., 2004; Klich, 2000; Sultana, 2004; Wu and Hinckley, 2001). The parameters of branch architecture include branch number, length, diameter, angle and bifurcation ratio. Among them, stem development and elongation are the critical components of the growth process (Schulze and Matthew, 1993). Bifurcation ratio, a term derived from river bifurcation in geography (Whitney, 1976), indicates the ability of a branch to produce bifurcations, and also expresses quantitatively the distribution conditions among every branch order of a branch population (Fisher, 1986). The stepwise bifurcation ratio reflects the growth condition at different developmental stages. H. rhamnoides and C. intermedia are both temperate perennial deciduous shrubs; in both, the leaves all grow from new branches. The stepwise bifurcation ratio R1:2 indicates directly branching conditions in the current year, whereas the stepwise bifurcation ratio R2:3 denotes branching conditions in the previous vegetation season, that is, the effects of water stress on branching ability in the first year of this experiment. Branching pattern differed significantly between H. rhamnoides and C. intermedia, which reflected their architectural variations. Whether plant architecture and branching pattern are steady or not has been hot issues of plant architecture research since Modular Theory put forward by Harper (1977, 1978). The result of this controlled experiment showed that plant architecture could be varied with different environments, for example, changes of water supply in this experiment; in different development stages, as demonstrated by Stepwise bifurcation ratio R1:2 and R2:3. Their branching patterns showed that H. rhamnoides tended to expand horizontally, with more, shorter, thinner branches and larger branch angle; while C. intermedia tended to grow perpendicularly with less, longer, thicker branches and smaller branch angle. Overall bifurcation ratio and stepwise bifurcation ratio R1:2 of H. rhamnoides were steady comparatively, but on the contrary, those of C. intermedia enhanced largely with the

Significance level: ***po0.001, **po0.01, *po0.05,

p40.05.

ns

Shoot height (cm) Stem diameter (mm) Crown area (cm2) Branch number (no.) Mean branch diameter (mm) Mean branch length (cm) Mean branch angle (1) Overall bifurcation ratio Rb (no. no.1) Stepwise bifurcation ratio R1:2 (no. no.1) Stepwise bifurcation ratio R2:3 (no. no.1) Leaf number (no.) Leaf area (cm2) Leaf area ratio (cm2 g1) Water saturation deficit (g g1) Branch biomass (g) Leaf biomass (g) Root biomass (g) Total biomass (g) Root biomass at level 1 (g) Root biomass at level 2 (g) Root biomass at level 3 (g) Root biomass at level 4 (g) Root to shoot ratio (g g1) Photosynthetic biomass ratio (g g1) Ratio of photosynthetic to non-photosynthetic biomass (g g1) Ratio of level 1 to root biomass (g g1) Ratio of level 2 to root biomass (g g1) Ratio of level 3 to root biomass (g g1) Ratio of level 4 to root biomass (g g1)

Characteristics

81.595 167.764 83.069 95.160 3.814 2.132 9.377 5.283 5.195 8.041 120.344 135.002 52.092 47.230 152.202 136.753 130.802 178.168 136.352 122.856 103.656 25.365 16.130 28.864 22.934 13.594 4.138 7.695 23.589

0.000*** 0.000*** 0.000*** 0.000*** 0.010** 0.096ns 0.000*** 0.001*** 0.002** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.007** 0.000*** 0.000***

2.311 0.003 1.794 244.309 209.717 192.852 877.060 0.649 0.497 266.233 398.410 7.044 54.021 2.538 0.071 15.657 69.468 6.618 41.331 81.84 81.065 17.810 156.991 135.665 135.368 52.513 2.371 12.487 76.978

F

F Sig.

Species

Water supply

Table 1 Effects of plant species and different water supply treatments on architectural and growth characteristics

ns

0.129 0.953ns 0.181ns 0.000*** 0.000*** 0.000*** 0.000*** 0.421ns 0.481ns 0.000*** 0.000*** 0.008** 0.000*** 0.112ns 0.789ns 0.000*** 0.000*** 0.011* 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** 0.125ns 0.000*** 0.000***

Sig. 0.736 0.197 6.790 17.060 3.757 2.219 2.592 2.976 3.633 5.723 53.813 5.978 4.899 3.773 2.130 6.005 5.786 1.864 2.219 6.588 11.653 2.130 3.176 0.969 1.763 0.569 0.530 2.057 1.204

F

0.531ns 0.898ns 0.000*** 0.000*** 0.011* 0.086ns 0.053ns 0.032* 0.013* 0.001*** 0.000*** 0.001*** 0.002** 0.011* 0.096ns 0.001*** 0.001*** 0.136ns 0.086ns 0.000*** 0.000*** 0.096ns 0.024* 0.408ns 0.154ns 0.636ns 0.662ns 0.106ns 0.309ns

Sig.

Water supply  species

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

ARTICLE IN PRESS 395

ARTICLE IN PRESS 396

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

enhancement of water supply. This study contrasted with the suggestions propounded by Whitney (1976), and Lynda and Ford (1978) that branching pattern was steady within a species and an individual. Plant architecture could be varied with different environments (Ho et al., 2004; Planchais and Sinoquet, 1998; Salemaa and Sieva¨nen, 2002; Steingraeber et al., 1979; Takahashi, 1996) such as the changes of water supply in this experiment, in different development stages (Borchert and Tomlinson, 1984; Schnitzler and Closset, 2003), as demonstrated by stepwise bifurcation ratios R1:2 and R2:3. There is an ecological implication among character expressions of architectural plasticity. There were higher investments in branch growth when water supply increased. There could be some tradeoff between branch length and bifurcation ratio. Under water stress, more investment in branch growth at the cost of the reduction of bifurcation ratio, and a subsequently steady branch length, may capture more resources in order to adapt to an arid environment. A high degree of branching is an unnecessary luxury under water stress because it would be wasteful of soil moisture (Keim and Kronstad, 1981). The inhibition of branching under water stress conditions observed here in H. rhamnoides and C. intermedia could therefore be considered an adaptive mechanism to conserve water that could be needed in more critical stages of development. The bifurcation ratio of C. intermedia reduced gradually along with the intensification of water stress, whereas that of H. rhamnoides was relatively steady; this difference probably reflected a better adaptation to the variation of the water stressed environment by architectural variation in C. intermedia than in H. rhamnoides. Leaf growth is the most sensitive of plant processes to water deficits (Bradford and Hsiao, 1982; Hsiao, 1973; Jones, 1985). Reduction in leaf area with increasing water stress demonstrates the ability of a species to tolerate and acclimate to a broad range of water levels by morphogenetic plastic responses (Kozlowski et al., 1991). In this experiment, water stress adversely affected leaf number, leaf biomass, leaf area and LAI, owing to poor leaf expansion and defoliation, and in turn reduced the amount of light intercepted. A reduction in the total number of leaves with decreasing levels of soil moisture, as well as poor expansion of individual leaves, resulted in a reduction in leaf area, a reduction more marked in C. intermedia than in H. rhamnoides. Water stress significantly reduced biomass accumulation in all components of H. rhamnoides and C. intermedia investigated, namely, the leaf, branch, root, root biomass at every level and, consequently, total biomass. It can therefore be presumed that water stress would decrease the efficiency with which solar radiation is used to accumulate biomass. This efficient drought avoidance mechanism was at the expense of biomass accumulation. Root architecture can vary between and among species and plays an important role in belowground resource acquisition (Ho et al., 2004). Several studies have shown that root systems that have optimal architectures should allocate carbon to root deployment patterns that are the most effective for acquisition of limiting soil moisture (Gautam et al., 2003; Ho et al., 2004; Middelhoff and Breckling, 2005). Plant root morphological plasticity enables a plant to change its root growth pattern as it encounters different soil conditions (Hutchings, 1988). High root to shoot ratios are generally a response to water stress in the rooting zone. Root growth depends on the supply of carbohydrate from the shoot, and reduction in leaf area usually reduces root growth (Gautam et al., 2003; Ho et al., 2004; Kramer, 1983); this would have been the case with H. rhamnoides and C. intermedia. C. intermedia made a relatively high investment in root growth, especially in deeper rooting, for high survival capacity under water stress; this strong deep-rooted system

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

397

reaches water and nutrients from deep soils and therefore adapts well to a comparatively arid environment. In contrast, H. rhamnoides, a shallow-rooted shrub, made a relatively high investment in branch and leaf growth under ample water supply in order to capture more light energy for growth, and thereby to occupy the habitat rapidly under favorable conditions. On the basis of these results, we found that water stress had negative effects on plant growth and architectural characteristics of H. rhamnoides and C. intermedia, and furthermore, that drought tolerance in plants varies widely among species. In addition, the seedlings adapt to different water resource environments by several synergistic strategies. The growth of H. rhamnoides was greatly reduced by slight drought and by drought, and completely inhibited by extreme drought. Throughout the growing season, C. intermedia grew well under normal precipitation, and reasonably well under slight drought conditions, with the ability to acclimate to a wide range of water stress intensity by architectural plasticity and growth responses. In planting H. rhamnoides or C. intermedia in natural ecosystems and on restoration sites of arid areas, the compromise between economic development and environmental protection in the region, and the water tolerance of the population as a whole, have to be taken into consideration. And further studies appear to be necessary to serve as a basis for modeling approaches to forecast future plant growth with global warming and local drying. Acknowledgments The research was supported by the State Key Basic Research and Development Plan of China (No. G2000018607) and the Outstanding Young Scientists Foundation Grant of Shandong Province (No. 2005BS08010). Thanks are due to Dr C. Welham at the University of British Columbia, Canada, for his constructive suggestions and to Asia Science Editing Compuscript Ltd. for their efficient help in language revising. References Beadle, C.L., Ludlow, M.M., Honeysett, J.L., 1993. Water relations. In: Hall, E.O., Scurlock, J.M.O., BolharNorderkampf, H.R. (Eds.), Photosynthesis and Production in a Changing Environment: A Field and Laboratory Manual. Chapman & Hall, London, pp. 113–128. Borchert, B., Tomlinson, P.B., 1984. Architecture and crown geometry in Tabebuia rasea (Bignoniaceae). American Journal of Botany 71, 958–969. Bradford, K.J., Hsiao, T.C., 1982. Physiological responses to moderate water stress. In: Lange, O.L., Nobel, P.S., Osmond, C.B. (Eds.), Encyclopedia of Plant Physiology, Vol. 12B: Physiological Plant Ecology II: Water Relations and Carbon Assimilation. Springer, Berlin, pp. 263–324. Derner, J.D., Briske, D.D., 1999. Does a tradeoff exist between morphological and physiological root plasticity? A comparison of grass growth forms. Acta Oecologica 20, 519–526. Editorial Committee for Flora of China, 1983. Flora of China, vol. 52(2). Science Press, Beijing. Editorial Committee for Flora of China, 1993. Flora of China, vol. 42(1). Science Press, Beijing. Eschenbach, C., 2005. Emergent properties modeled with the functional structural tree growth model ALMIS: computer experiments on resource gain and use. Ecological Modelling 186, 470–488. Fisher, J.B., 1986. Branching patterns and angles in trees. In: Givnish, T.J. (Ed.), On the Economy of Plant Form and Function. Cambridge University Press, London, pp. 493–523. Gautam, M.K., Mead, D.J., Clinton, P.W., Chang, S.X., 2003. Biomass and morphology of Pinus radiata coarse root components in a sub-humid temperate silvopastoral system. Forest Ecology and Management 177, 387–397.

ARTICLE IN PRESS 398

W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

Guo, W.H., Wang, R.Q., Zhou, S.L., Zhang, S.P., Zhang, Z.G., 2003. Genetic diversity and clonal structure of Phragmites australis in the Yellow River delta of China. Biochemical Systematics and Ecology 31, 1093–1109. Guo, W.H., Li, B., Huang, Y.M., Zhang, X.S., 2004. Effects of severity of water stress on gas exchange characteristics of Caragana intermedia seedlings. Acta Ecologica Sinica 24, 2716–2722. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London. Harper, J.L., 1978. The demography of plants with clonal growth. In: Freysen, A.H., Wouldendrop, J.W. (Eds.), Structure and Functioning of Plant Populations. North-Holland Publishing Company, London, pp. 27–48. Ho, M.D., McCannon, B.C., Lynch, J.P., 2004. Optimization modeling of plant root architecture for water and phosphorus acquisition. Journal of Theoretical Biology 226, 331–340. Horn, H.S., 1971. The Adaptive Geometry of Trees. Princeton University Press, Princeton. Horn, J.S., 1979. Adaptation from the perspective of optimality. In: Solbrig, O.T., et al. (Eds.), Topics in Plant Population Biology. Columbia University Press, New York, pp. 48–61. Hsiao, T.C., 1973. Plant responses to water stress. Annual Review of Plant Physiology 24, 519–570. Hughes, A.P., Freeman, P.R., 1967. Growth analysis using frequent small harvest. Journal of Applied Ecology 4, 553–560. Hutchings, M.J., 1988. Differential foraging of resources and structural plasticity in plants. Trends in Ecology and Evolution 3, 200–204. Jin, Z.P., Shi, P.J., Hou, F.C., 1992. Soil Erosion Systematical Model and Administrant Pattern in Huangfuchuan Watershed of Yellow River. Oceanic Press, Beijing. Jones, M., 1985. Modular demography and form in silver birch. In: White, J. (Ed.), Studies on Plant Demography: A Festschrift for John L. Harper. Academic Press, London, pp. 223–237. Keim, D.L., Kronstad, W.E., 1981. Drought response of winter wheat cultivars grown under field stress conditions. Crop Science 21, 11–14. Klich, M.G., 2000. Leaf variations in Elaeagnus angustifolia related to environmental heterogeneity. Environmental and Experimental Botany 44, 171–183. Kozlowski, T.T., Kramer, P.J., Pallardy, S.G., 1991. The Physiological Ecology of Woody Plants. Academic Press, San Diego. Kramer, P.J., 1983. Water Relations of Plants. Academic Press, New York. Li, C.Y., Yang, Y.Q., Junttila, O., Palva, E.T., 2005. Sexual differences in cold acclimation and freezing tolerance development in sea buckthorn (Hippophae rhamnoides L.) ecotypes. Plant Science 168, 1365–1370. Lynda, A.C., Ford, E.D., 1978. Growth of a sitka spruce plantation: analysis and stochastic description of the development of the branching structure. Journal of Applied Ecology 15, 227–244. McMahon, T.A., Kronauer, R.E., 1976. Tree structures: deducing the principle of mechanical design. Journal of Theoretical Biology 59, 443–466. Middelhoff, U., Breckling, B., 2005. From single fine roots to a black alder forest ecosystem: how system behavior emerges from single component activities. Ecological Modelling 186, 447–469. Planchais, I., Sinoquet, H., 1998. Foliage determinants of light interception in sunny and shaded branches of Fagus sylvatica (L.). Agricultural and Forest Meteorology 89, 241–253. Salemaa, M., Sieva¨nen, R., 2002. The effect of apical dominance on the branching architecture of Arctostaphylos uva-ursi in four contrasting environments. Flora—Morphology, Distribution, Functional Ecology of Plants 197, 429–442. Schnitzler, A., Closset, D., 2003. Forest dynamics in unexploited birch (Betula pendula) stands in the Vosges (France): structure, architecture and light patterns. Forest Ecology and Management 183, 205–220. Schulze, H.R., Matthew, M.A., 1993. Growth, osmotic adjustment, and cell-wall mechanics of expanding grape leaves during water deficits. Crop Science 33, 287–294. Steingraeber, D.A., Waller, D.M., 1986. Non-stationarity of tree branching patterns and bifurcation ratios. Proceedings of the Royal Society of London B 228, 187–194. Steingraeber, D.A., Kascht, L.J., Franck, D.H., 1979. Variation of shoot morphology and bifurcation ratio in sugar maple (Acer saccharum) saplings. American Journal of Botany 66, 441–445. Sultana, S.E., 2004. Promising directions in plant phenotypic plasticity. Perspectives in Plant Ecology, Evolution and Systematics 6, 227–233. Takahashi, K., 1996. Plastic response of crown architecture to crowding in understorey trees. Annals of Botany 77, 159–164. Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S.M., Schlichting, C.D., Van Tienderen, P.H., 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology and Evolution 10, 212–217.

ARTICLE IN PRESS W. Guo et al. / Journal of Arid Environments 69 (2007) 385–399

399

Wang, X.D., Xie, S.N., Chen, H.C., 1999. Study on mathematical model of runoff sediment yield and analysis on reasons for changes of runoff and sediment yields in Huangfuchuan Watershed. Journal of Sediment Research 10, 56–66. Whitney, G.G., 1976. The bifurcation ratio as an indicator of adaptive strategy in woody plant species. Bulletin Torrey Botanical Club 103, 67–72. Wu, R., Hinckley, T.M., 2001. Phenotypic plasticity of sylleptic branching: genetic design of tree architecture. Critical Reviews in Plant Sciences 20, 467–485. Zhang, J.T., 2005. Succession analysis of plant communities in abandoned croplands in the eastern Loess Plateau of China. Journal of Arid Environments 63, 458–474. Zhang, X.S., Shi, P.J., 2003. Theory and practice of marginal ecosystem management—establishment of optimized eco-productive paradigm of grassland and farming-pastoral zone of North China. Acta Botanica Sinica 45, 1135–1138.