Bot. Bull. Acad. Sin. (2003) 44: 291-296

Ge et al. — Soil water effects on physioecological traits of two endangered species

Effect of soil water status on the physioecological traits and the ecological replacement of two endangered species, Changium smyrnioides and Chuanminshen violaceum

Y. Ge¹, Jie Chang^1,*, C.-X. Fu¹, and G.Y.-S. Chan²

¹The State Key Laboratory of Plant Physiology and Biochemistry, College of Life Science, Zhejiang University, 232 Wensan Road, Hangzhou 310012, P. R. China

²Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Hong Kong, P. R. China

(Received April 21, 2003; Accepted June 9, 2003)

Abstract. Both Changium smyrnioides Wolff and Chuanminshen violaceum Shen et Shan are monotypic species of the family Umbellaceae. They have narrow distribution areas and can only be found in the Yangtze River basin in China. Changium is distributed from the east to middle subtropical zone of China, and Chuanminshen from the middle to the west; they almost meet in the middle of the Yangtze basin. Because the climate varies from humid to semi-humid, an experiment was carried out to find out the two species' demand for soil water and analyze their niche separation by determining changes in their physio-ecological and structural traits in response to different soil water statuses. Results showed that the two species have similar structural characters and functional intensity. Diurnal variations, daily mean values, and relationships of irradiation and temperature to P_N, E and WUE among the three treatments indicate that Chuanminshen has more tolerance to drought than Changium. Changes in morphological traits also suggest that Changium adapts to medium to wet soil conditions while Chuanminshen adapts to drought soil conditions. The differences in the adaptation of physiological and morphological traits to the water environment should be part of the reason these two species have become geographically vicarious species. The results indicate that, at least, the mechanism and the approach to conservation for the two species are similar.

Keywords: Ecological replacement; Endangered species; Growth; Morphology; Photosynthesis; Subtropical zone; Transpiration; Water use efficiency.

Introduction

Both Changium smyrnioides Wolff and Chuanminshen violaceum Shen et Shan are monotypic species of the family Umbellaceae. There are some interesting viewpoints on the relationship between Changium and Chuanminshen, for they were classified as the same species before 1980. Shen et al. (1980) indicated that Chuanminshen violaceum should belong to different genera with a distant relation in systematic development with Changium smyrnioides.

Because their fleshy roots are prized in Chinese medicine, and because of land use, the natural populations of the two species have been seriously disturbed by human activity and have decreased in recent years to the point that they are now endangered species (Qiu et al., 2000). Chuanminshen has been cultivated as a medicinal material on a large scale, but Changium has not yet been cultivated.

The two species have narrow distribution areas and can be found only in the drainage basin of the Yangtze River in China. Changium is distributed in the area from the east

to the middle subtropical zone of China while Chuanminshen is from the middle to the west. The distribution areas of the two species meet in the middle of the Yangtze basin, but barely overlap (Figure 1). Thus, the distribution of the two species shows ecological replacement. They should be geographically vicarious from an ecological viewpoint. Because the climate from east to west of the subtropical zone of China varies from humid to semi-humid (Wu, 1983), we suppose each species should fit into different water environments with different morphological adaptations and physio-ecological requirements, especially different demands for water; i.e. there would be niche partitioning between the two species.

To test the hypothesis, we designed an experiment on the appearance and plasticity of the physioecological and structural traits of the two species in response to different soil water statuses (Rajendrudu et al., 1997), to find out their demands for soil water and analyze their niche separation.

Although there are studies of geographically vicarious species, much of the work is on their systematics, morphology, anatomy, molecular biology, genetics (Liu et al., 2002), or paleobiology (Prado and Gribs, 1993). Some work has been done on the distribution patterns and their relationship to climate and water conditions (Prado and

*Corresponding author. Tel & Fax: +86-571-8797-2193; E-mail: jchang@mail.hz.zj.cn

Botanical Bulletin of Academia Sinica, Vol. 44, 2003

species, and finally determining the distribution. In the period from late autumn to spring, the mean temperatures in the east and the west are similar while the west is significantly dryer with less precipitation (Figure 2).

Research was conducted at the plantation of Zhejiang University in the city of Hangzhou, eastern China (120º10´E, 30º15´N). Both species were cultivated in pots (height 14.5 cm and diameter of upper surface 17.5 cm) in January 2001, after the seeds germinated and the seedlings had reached 5 cm. Experiencing a growth season, Chuanminshen began dormancy in early June while Changium did so in mid-June. Chuanminshen began frondescing in late-September, and the treatments began in October 2001; Changium frondescence in mid-February 2002, and the treatments begin in early March 2002. The aim of the experiment was to provide the two species with the same treatments at the same life history stages. All treatments were carried out in a glass house with an open wall.

There were ten repetitions of three treatments, expressed by the relative soil water contents (RWC), which is the percentage of the soil water holding capacity (WHC) as follows: (1) Constant saturation (SS), replenished until 100% WHC whenever the RWC of samples dropped to 90% WHC due to evapotranspiration; (2) Alterative water (middle moist, AW₅₀), plants were not watered until the RWC dropped to 50% WHC; and (3) Alterative water (drought, AW₂₀), distilled water was added to saturation whenever RWC dropped to 20%. These treatments simulated field soil water conditions in which rainy and dry weather alternate: SS simulated waterside habitat, and AW₅₀ and AW₂₀ simulated soil moisture conditions with more or less intermittent precipitation, respectively.

Measurements of net photosynthetic rate (P_N) and transpiration (E) were carried out from 06:30 to 18:30 on clear days at the beginning of April, every hour in triplicate. P_N was measured using a CO₂ analyzer (GHX305A, Beijing,

Figure 1. Distribution of Changium smyrnioides and Chuanminshen violaceum.

Gribs, 1993); however, little has been known about the physio-ecological reasons for the ecological replacement of the vicarious species. Our work can increase the understanding of the ecological mechanisms of vicarious distributions of the plant species and assist in the development of approaches to conserve the two endangered species.

Materials and Methods

Both species are winter species in the subtropical zone of the Yangtze basin of China, where the climate and soil environmental conditions are not too cool for plants. The main growth periods of the two species are winter and spring, and the seasonal climate should be the main factor limiting the physiological processes and growth of the

Figure 2. Combination of temperature (solid line) and precipitation (dot line) in east (e.g. Hangzhou) and west (e.g. Chengdu) subtropical zones of China, the distribution region of Changium smyrnioides and Chuanminshen violaceum. The drought period occurs when precipitation line falls below temperature line.

Ge et al. — Soil water effects on physioecological traits of two endangered species

China-German cooperation) in the closed system. Diurnal mean photosynthetic rate (P_Nmean) was calculated by average the P_N of every hour from morning to afternoon. E of whole shoots were measured by weighting the whole pots, the upper surfaces of which were covered with plastic film to prevent evaporation from the soil,

E = (W_t-W_t+1)/A

where W_t is the weight of pots the previous time, W_t+1 is the weight the current time, and A is the total area of the leaves in pots. Diurnal mean transpiration rate (E_mean) was calculated by the average of the E of every hour. Water use efficiency (WUE) was calculated as P_N/E. Photosynthetically active radiation (PAR) above the leaf, air temperature (T_a), leaf temperature (T_l), and relative humidity (RH) were measured simultaneously with P_N. An admixture of acetones and ethanol (2:1) was used to distill chlorophyll, and then the absorbency of chlorophyll-a and chlorophyll-b were measured at 663 nm and 645 nm, respectively, with a 751 spectrophotometer (HP, Shanghai). Three individuals of every species were harvested from the three-replication pots. Before drying the samples in an oven at 80°C for at least 72 h, leaf area was determined with a portable area meter. Leaf area per unit leaf mass (specific leaf area; SLA), leaf area per unit of total mass (leaf area ratio; LAR), and leaf mass per unit of total mass (leaf mass ratio; LMR) were determined (Hunt, 1978). The differences between the traits were statistically analyzed with ANOVA in SPSS (8.0).

Results and Discussion

Diurnal Pattern of Photosynthesis, Transpiration and Water Use Efficiency in Response to Soil Water Status

Daily changes of photosynthesis differed between the species in the same soil water status (Figure 3). In SS, the P_N of Changium increased in the morning in response to PAR, peaked at 10:00, then did not respond to the increase of PAR and held steady until 14:00. In Chuanminshen the P_N increased more slowly than Changium and peaked at 13:00, showing a single peak curve. In dry soil (AW₂₀), the P_N of Changium showed double peaks (at 9:00 and 14:00) while the P_N of Chuanminshen fluctuated at midday (the peak was at 13:00). The diurnal curves of P_N of Changium in AW₅₀ were close to those of SS while that of Chuanminshen in AW₅₀ approached AW₂₀.

The diurnal variations of E of both species were similar. The values for Chuanminshen were lower than Changium in SS and AW₅₀ and slightly higher than Changium in AW₂₀.

The E of Changium increased much more slowly than P_N in the morning in SS and AW₅₀, causing an increase in WUE of Changium in the early morning, and the P_N of Changium was not correlated with E (P>0.05). While the E increased simultaneously with P_N for Chuanminshen (P<0.05), that made WUE of Changium higher than Chuanminshen in the morning.

Figure 3. Diurnal variations of the net photosynthetic rate (P_N), transpiration (E), water use efficiency (WUE), photosynthetic photon flux density (PAR), leaf temperature (T_l) and air temperature (T_a) for Changium smyrnioides and Chuanminshen violaceum in different soil water statuses (SS, soil water near saturation constantly; AW₅₀, soil water content altered from saturation to 50% soil water holding capacity; AW₂₀, soil water content altered from saturation to 20% soil water holding capacity).

WUE of the two species had higher values and larger fluctuations in the morning than in the afternoon. The differences were more significant in the morning than in the afternoon among the treatments, especially for Changium.

The diurnal variation of P_N, E and WUE in response to soil water status indicates that the physiological traits of Changium change little when soil water is kept at a wet or medium wet level, but change significantly when water levels varied from medium wet to drought level conditions. In contrast, the physiological traits of Chuanminshen change little when soil water varied from medium wet to drought level conditions; i.e., Chuanminshen can keep a high physiological vigor at drought level conditions.

The differences between P_N and E among the three treatments in Changium outstrip those in Chuanminshen, indicating that Changium is more sensitive in response to soil water than Chuanminshen in photosynthesis and transpiration, while the two species did not show differences in WUE.

Daily Mean Photosynthesis, Transpiration, and Water Use Efficiency Responds to Soil Water Status

The P_Nmean of Changium showed a significant decrease when conditions changed from medium wet to drought level; in contrast, that of Chuanminshen showed an increase with a change from medium wet to drought level

Botanical Bulletin of Academia Sinica, Vol. 44, 2003

conditions. P_Nmean of Changium was similar in SS and AW₅₀, but that of Chuanminshen was similar in AW₅₀ and AW₂₀ (Figure 4). The P_Nmean of Changium was higher than that of Chuanminshen in SS and AW₅₀, but lower in AW₂₀.

The E_mean of two species was SS>AW₅₀>AW₂₀, entirely in response to soil water content. Like P_Nmean, the E_mean of Changium was higher than that of Chuanminshen in wet to medium wet soil, but lower than Chuanminshen in drought.

The highest daily mean WUE of Changium was in AW₅₀ while the highest in Chuanminshen was in AW₂₀, with the smallest in AW₅₀. The WUE of Changium was nearly two times that of Chuanminshen in medium wetness, but was lower than Chuanminshen in drought. This indicates that a medium soil water status suits Changium best and that it has a lower tolerance than Chuanminshen for drought.

The coefficient variation of P_Nmean and E_mean of Changium (56%, 52%) was larger than that of Chuanminshen (30%, 35%) in three treatments, showing that the P_N of Changium had a higher phenotypic plasticity in response to soil water content than Chuanminshen.

Diurnal Pattern of Photosynthesis, Transpiration and Water Use Efficiency in Response to Light and Temperature

An increase in PAR and T_l brought a linear increase in P_N of Changium in wet to medium wet soil (SS and AW₅₀), and the response was AW₅₀>SS (Table 1). However, the P_N of Changium did not respond to PAR or T_l in drought. Subsection analysis showed that the P_N only responds to PAR (R²=0.725**, n=24) below light saturation (PAR<300

Figure 4. Daily mean net photosynthetic rate (P_Nmean), daily mean transpiration (E_mean) and water use efficiency (WUE) of Changium smyrnioides and Chuanminshen violaceum in different soil water statuses (legends as in Figure 3).

Ge et al. — Soil water effects on physioecological traits of two endangered species

the fourth euphylis on, i.e. they are almost the same in the early stages of individual development and differ later. We suggest that the systematic development of both Changium and Chuanminshen is very close.

Changium resides under the forest gap caused by defoliated trees in winter. Individuals finish vegetative growth after re-foliation of deciduous trees, so as to avoid shading and competition with other plants (Busso et al., 2001). Such a pattern of Changium could be seen as a competition-avoidance strategy through temporal niche partition. With higher SLA, LAR, and chloral content (Table 3), Changium uses irradiation fully in carbon accumulation in a short time in compensation for its short growth period. In humid environments, the plant often has a larger SLA and LAR than in drought (Fownes, 1999; Gurnier et al., 2001). The humid climate in Changium's distribution area, the east to middle subtropical zone of China, ensure it a larger SLA and LAR. Chuanminshen has a lower SLA and LAR, adapts to the dryer environment in the west, and has a longer growth period to meet the requirement of carbon accumulation.

Conclusions

The two species, Changium smyrnioides and Chuanminshen violaceum have similar structural charac

µmol m^-2s^-1) and only to T_l (negative correlation, R²= 0.287**, n=28) above light saturation, meaning that temperature stress occurs at higher temperatures in drought conditions.

In contrast to Changium, P_N of Chuanminshen responds to PAR and T_l in all three soil water statuses, and the degree of response was SS>AW₂₀>AW₅₀. It means that P_N of Chuanminshen still functions normally in the dry soil in which the physiological process of Changium has changed.

The E of both species responds to PAR and T₁ (positive) and RH (negative) significantly and the slope of correlation was SS>AW₅₀>AW₂₀. In wet to medium wet conditions, Changium responds to the above three factors more sensitively than Chuanminshen but does just the opposite in drought conditions (Table 2).

The diurnal pattern of the main physiological traits suggests that the P_N of Chuanminshen has a higher tolerance to drought than that of Changium.

Morphology and Growth Traits of the Two Species

Our investigation concluded both species to be nearly identical in morphology from the first to the third euphylis of the seedling, and then the leaves become different from

Botanical Bulletin of Academia Sinica, Vol. 44, 2003

Fownes, A.J.H. 1999. Water supply regulates structure, productivity, and water use efficiency of Acaciaboa forest in Hawaii. Oecologia 121: 458-466.

Gurnier, E., B. Shipley, C. Rounset, and G. Laurent. 2001. A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecol. 15: 688-695.

Hunt, R. 1978. Plant Growth Analysis. Edward Arnold, London.

Liu, J.-Q., Z.-D. Chen, and A.-M. Lu. 2002. Molecular evidence for the sister relationship of the eastern Asia-North American intercontinental species pair in the Podophyllum group (Berberidaceae). Bot. Bull. Acad. Sin. 43: 147-154.

Prado, D.E. and P.E. Gribs. 1993. Patterns of species distributions in the dry seasonal forest of South America. Ann. Missouri Bot. Gard. 80: 902-927.

Qiu, Y.-X., A.-J. Huang, and C.-X. Fu. 2000. Studies on diversity in Changium smyrnioides Wolff (Umbelliferae). Acta phytotaxon. Sin. 38: 111-120.

Rajendrudu, G., C.V. Naidu, and K. Mallikarjuna. 1997. Effect of water stress on photosynthesis and growth in two teak phenotypes. Photosynthetica 34: 45-55.

Shen, M.-L. and R.-H. Shan. 1980. Cyclorhiza and Chuanminshen-two newly proposed genera in Umbelliferae (Apiaceae). Acta phytotaxonomica Sin. 18: 45-49.

Wu, Z.-Y. (eds.). 1983. Chinese Vegetation: Science Press, Beijing, 39-40 pp.

ters and functional intensity, such as the net photosynthetic rate (P_N), transpiration (E), water use efficiency (WUE), and the fact that each is endangered. Meanwhile, these two species showed different plasticity for the main physiological process and their morphological traits respond differently to different soil water statuses. Changium smyrnioides demands medium to wet soil conditions while Chuanminshen violaceum adapts readily to droughty soil. The differences in the adaptation of physiology and morphology to the water environment cause niche partitioning, part of the reason these two species are geographical replacements in distribution. The results indicate that, at least, the mechanism and the approach of conservation for the two species should be similar.

Acknowledgements. We are grateful for the funding provided by the National State Key Basic Research and Development Plan (973) (No. G2000046805).

Literature Cited

Busso, C.A., D.D. Briske, and V. Olalde-Portugal. 2001. Root traits associated with nutrient exploitation following defoliation in three existing perennial grasses in a semi-arid savanna. Oikos 93: 332-342.