Effect of Stem Density on Leaf Nutrient Dynamics and ... - CiteSeerX

Pedosphere 19(4): 496–504, 2009 ISSN 1002-0160/CN 32-1315/P c 2009 Soil Science Society of China Published by Elsevier Limited and Science Press

Effect of Stem Density on Leaf Nutrient Dynamics and Nutrient Use Efficiency of Dwarf Bamboo∗1 WU Fu-Zhong1,2,3 , YANG Wan-Qin1,2 , WANG Kai-Yun1,4 , WU Ning1,∗2 and LU Ye-Jiang1 1 Chengdu

Institute of Biology, Chinese Academy of Sciences, Chengdu 610041 (China) of Forestry, Sichuan Agricultural University, Ya’an 625014 (China) 3 Graduate University of the Chinese Academy of Sciences, Beijing 100049 (China) 4 Shanghai Key Laboratory of Urbanization Processes and Ecological Restoration, East China Normal University, Shanghai 200062 (China) 2 Faculty

(Received January 26, 2009; revised May 30, 2009)

ABSTRACT The monthly dynamics of nitrogen (N) and phosphorus (P) concentrations and stocks in leaves, resorption efficiency, and resorption proficiency as well as leaf-level use efficiency, nutrient productivity, and mean residence time were studied to understand the effect of stem density of dwarf bamboo (Fargesia denudata Yi) on leaf-level N and P use efficiency in three dwarf bamboo stands with different stem densities under bamboo-fir (Picea purpurea Mast.) forest over one growing period in the Wanglang National Nature Reserve, Sichuan, China. Dwarf bamboo density had little effect on the dynamics pattern of both N and P concentrations, stocks, resorption efficiency, and resorption proficiency, but strongly affected their absolute values and leaf-level use efficiency. Higher density stands stored more nutrients but had lower concentrations. There was a clear difference in the resorption of limiting nutrient (N) and non-limiting nutrient (P) among the stands. Phosphorus resorption efficiency, N resorption proficiency, and P resorption proficiency increased with increase of stem density, but no significant variation of N resorption efficiency was found among the stands. Moreover, the higher density stands used both N and P more efficiently with higher N productivity and higher P mean residence time, respectively. Higher P productivity was found in the lower density stands, but there was no clear variation in the N mean residence time among stands. These suggested that the higher density stands may have more efficient strategies for utilizing nutrients, especially those which are limiting. Key Words:

mean residence time, nutrient productivity, nutrient resorption

Citation: Wu, F. Z., Yang, W. Q., Wang, K. Y., Wu, N. and Lu, Y. J. 2009. Effect of stem density on leaf nutrient dynamics and nutrient use efficiency of dwarf bamboo. Pedosphere. 19(4): 496–504.

The ecology of resource use by plants is one of the main topics in plant nutrition and ecology. A common approach to the study of the adaptive significance of resource use by plants is to determine their resource use efficiency (Aerts and Caluwe, 1994). Owing to the large discrepancy between demand and supply and their important roles in plant carbon assimilation (Yuan et al., 2005), nitrogen (N) and phosphorus (P) are two of the primary growth-limiting factors in several terrestrial ecosystems (Chapin, 1980; Vitousek and Howarth, 1991), and have been the subject of various studies (Vitousek, 1982; Berendse and Aerts, 1987; Aerts and Caluwe, 1994; Aerts and Chapin, 2000). Generally, nutrient use efficiency has been defined as dry mass productivity per unit resource that is taken up or lost (Hirose, 1971; Vitousek, 1982). Berendse and Aerts (1987) further divided it into the product of nutrient productivity and the mean residence time of nutrient in the plant (MRT). In this context, nutrient use efficiency equals total productivity divided by the total nutrient loss through litter production. The MRT measures how long a unit of nutrient is present and measures the rate of dry matter production per unit of nutrient in the plant. An important assumption is that the plants are in a steady state with ∗1 Project

supported by the National Basic Research Program of China (No. 2005CB422006), the National Natural Science Foundation of China (No. 30771702), and the Sino-Finland International Cooperative Program (No. 30211130504). ∗2 Corresponding author. E-mail: [email protected].

STEM DENSITY EFFECT ON LEAF NUTRIENTS

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respect to their nutrient content, so that their annual nutrient uptake equals nutrient loss. Additionally, Eckstein et al. (1999) demonstrated that adult plants under in-situ conditions satisfied this steady-state assumption in experiment practice. Most of the previous studies have focused on overstorey trees in forest systems, and have shown that several biotic and abiotic factors influencing nutrient productivity or MRT can subsequently contribute to nutrient use efficiency (Del Arco et al., 1991; Knops et al., 2002). However, little attention has been paid to understorey shrub populations, another vital component. There may be very large differences in resource use between overstorey and understorey plants (Tateno and Kawaguchi, 2002). In addition, plant density may be more important in competition for understorey resources with density itself correlated to several factors such as light, water, and nutrient availability (Sprugel, 1984; Meekins and McCarthy, 2000; Wu et al., 2005a, c; Lu et al., 2005b) in natural ecosystems. Few studies have been aimed at identifying the mechanisms underlying nutrient use by understorey populations, and even fewer have focused on the relationship between plant density and nutrient use efficiency (Shujauddin and Kumar, 2003). Dwarf bamboo, a staple food of the giant panda (Schaller et al., 1985; Reid et al., 1991), is the dominant plant in several subalpine and montane forests (Taylor and Qin, 1987; Tomoyuki et al., 2002). Bamboo plays an important role for the giant panda itself and its habitat protection (Taylor and Qin, 1987, 1993; Taylor et al., 1995; Wu et al., 2005b), forest regeneration, and forest structure and function maintenance (Franklin et al., 1979; Narukawa and Yamamoto, 2002). However, cold temperature often limits plant growth in most of the dwarf bamboo habitats, leading to poor soil nutrient availability in spring (Lu et al., 2005a). Thus, plant performance may be dependent on the considerably efficient mechanism for nutrient use (Lu et al., 2005b). As yet, little information has been published on nutrient use efficiency in these bamboo dominant forests, which limits our ability to understand the mechanisms underlying plant adaptation to their environment. This study focused on the effect of an understorey plant dwarf bamboo (Fargesia denudata Yi) density on leaf-level N and P use efficiency. Leaf-level N and P use efficiency was investigated because leaf nutrient concentrations and nutrient use efficiency may be sensitive indices of limiting nutrient use by plants, being strongly related to plant growth and health. Thus, this approach can provide effective tools for indicating whole plant nutrient use efficiency (Tessier and Raynal, 2003; Yuan et al., 2005), therefore increasing our understanding of plant nutrient use and the related underlying mechanisms in forests. The objectives of this study were to determine the effect of dwarf bamboo density on N and P concentrations, stocks, resorption efficiency, and resorption proficiency, and leaf-level use efficiency, and their monthly dynamics over one growing period and to explore the likely nutrient use strategy of dwarf bamboo in different stands with different stem densities. MATERIALS AND METHODS The study was conducted in the Wanglang National Nature Reserve (103◦ 55 –104◦ 10 E, 32◦ 49 –33◦ 02 N; altitude 2 300–4 980 m above sea level), which is located in Pingwu County, western Sichuan, China. The climatic and vegetational features have been described by Wu et al. (2005a, c). The mean annual temperature is 2.9 ◦ C, the annual cumulative temperature (≥ 10 ◦ C) is 1 056.5 ◦ C, and the absolute maximum and minimum temperatures are 26.2 and −17.8 ◦ C, respectively. The annual precipitation ranges from 801 to 825 mm depending on the elevation, most of which falls from May to August. The precipitation and temperature are shown in Fig. 1. Heavy snow covers the site from November to the following April. The soil is classified as a dark brown soil. The forest studied was dominated by Picea purpurea Mast. and Sabina saltuaria (Rehd. et Wils.) Cheng et W. T. Wang in the canopy, while dwarf bamboos covered over 95% of the understorey. Only a few shrubs occurred together with bamboo, such as Euonymus hamiltonianus Wall., Lonicera webbiana Wall. ex DC., Ribes glaciale Wall., Rubus amabilis Focke and some young firs, with their total coverage and biomass less than 5% of the total (Wang et al., 2004).

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Fig. 1

Average precipitation and temperature at the study site from May to October, 2003.

To understand the distribution and growth status of dwarf bamboo at the study site, a preliminary investigation was performed in the winter of 2002. The bamboo stands naturally regenerated from seed in 1978 after synchronous flowering in the area (Taylor and Qin, 1987; Taylor et al., 1995) had culms 100–250 cm in height, 4.00–9.50 mm in basal diameter, and 10–27 nodes depending on the culm age. Three representative 10 m × 10 m stands of similar environments (soil texture, slope, aspect, plant community, etc.) but different dwarf bamboo densities, low-density (80 ± 4 stems m−2 ) stand (Dl), medium-density (140 ± 7 stems m−2 ) stand (Dm), and high-density (220 ± 11 stems m−2 ) stand (Dh) at aspect 26◦ , 28◦ , and 31◦ , respectively, of a 30◦ north-east slope (32.91◦ N, 104.05◦ E, 2 920 m above sea level) were selected in May 2003. Some chemical and physical properties of the soils under each stand are given in Table I. There was a distance of 10 m between the two higher density stands (Dm and Dh), 15 m between the lower (Dl and Dm), and 25 m between Dl and Dh. Thirty-seven 1 m × 1 m sampling plots were established with similar growth status at each stand (30 for leaf harvest sampling and 7 for senesced leaf collecting), with at least 2–3 m between plots to avoid disturbance. Seven 30 cm × 30 cm plastic senesced leaf collecting traps with 1-mm mesh screen were randomly set in the seven plots in each dwarf bamboo stand for collection of senesced leaves. TABLE I Soil properties of the stands sampled Standa)

pH

Dl Dm Dh

6.45 6.34 6.51

a) Dl

Bulk density

Gravel content

Water content

Organic carbon

g cm−3 0.66 0.67 0.66

52 47 45

486.3 493.9 496.6

89.35 85.56 84.27

Kjeldahl nitrogen g kg−1 4.33 4.51 4.57

Total phosphorus

Total potassium

1.27 1.25 1.24

19.71 18.97 19.11

= low-density stand, Dm = medium-density stand, Dh = high-density stand.

At the end of every month from May to October 2003 (dwarf bamboo growing period), the dwarf bamboo leaves were harvested in five 1 m × 1 m sampling plots in each stand, and at the same time, the senesced leaves were collected in the plastic traps. All the leaves were immediately brought to the laboratory, oven-dried at 70 ◦ C for at least 48 h to a constant weight, and weighed to the nearest 0.01 g. The oven-dried samples were ground finely to pass through the 1-mm stainless steel sieve. Total N and P in the samples were determined as described by Lu (1999). 0.2500 g sub-samples were digested with 8 mL 1.84 g cm−3 H2 SO4 and 3 mL H2 O2 solutions at 190 ◦ C for 10 min in a microwave laboratory system (Milestone, Italy). The digested solution was then transferred to a 100-mL volumetric flask, rationed, and stored for measurements of total N and P concentrations. Nitrogen and P were analyzed by indophenol-blue colorimetry and phosphomolybdenum-yellow colorimetry, respectively. All analyses were carried out in triplicates.


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Although several studies have reported that estimates of proportional nutrient resorption on a leaf area basis may be more accurate than on a leaf mass basis (Van Heerwaarden et al., 2003; Vernescu et al., 2005), the specific mature leaf area and specific senesced leaf area do not differ statistically (Wang et al., 2004) in this study, as reported by Helmisaari (1992). Accordingly, resorption efficiency (RE) was calculated as nutrient mass per unit of leaf mass of fresh (MLf ) and senesced leaves (MLs ): RE = [(MLf − MLs )/MLf ] × 100 (Finzi et al., 2001). The nutrient concentration in senesced leaves was considered as a direct indicator of resorption proficiency, which is defined as the absolute level to which the nutrient is reduced in senescing leaves (Killingbeck, 1996). According to Eckstein and Karlsson (2001), nutrient productivity = (LMMax − LMMin )/(LSMax − LSMin ), where LMMax , LMMin , LSMax , and LSMin are the maximum leaf mass, minimum leaf mass, maximum leaf nutrient stock, and minimum leaf nutrient stock during the dwarf bamboo growing period, respectively. To calculate the MRT in the leaf, the following equation adopted from Eckstein et al. (1999) was used: MRT = 1/[LR × (1 − RE)], where LR is the leaf biomass loss rate, calculated as annual biomass loss/annual biomass. Therefore, we obtained the nutrient use efficiency defined by Berendse and Aerts (1987), that is, the product of nutrient productivity and MRT. There would be an underestimate in calculating nutrient productivity and MRT, because we used growing period biomass instead of annual biomass. Samples were not obtained in the experimental site from November to April owing to heavy snow. Statistical analyses were performed with SPSS 11.5 for Windows. Multiple comparisons among pairs of means were done using the Student-Newman-Keuls test. Differences were considered significant at P < 0.05 level. The density and month effects were tested by analysis of variance (ANOVA). RESULTS Dynamics of N and P concentrations and stocks As seen in Fig. 2, there was little effect of the stem density on the dynamics of the N and P concentrations and stocks. All three bamboo stands had the highest nutrient concentrations and stocks in July and the lowest in June, with an obvious increase in October during the dwarf bamboo growing period in 2003.

Fig. 2 Monthly dynamics of N concentration (a), N stock (b), P concentration (c), and P stock (d) in leaves of three bamboo stands with different stem densities from May to October, 2003. Dl = low-density stand, Dm = medium-density stand, Dh = high-density stand. Bars indicate standard deviation (n = 5).

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However, the three stands differed significantly in nutrient concentrations and stocks. The concentration decreased with increase of stem density, but did not differ statistically between Dl and Dm or between Dm and Dh overall; however, Dl significantly differed from Dm (P < 0.05) in several months (May, June, July, August, and October for N; May, June, and July for P) (Fig. 2a, c). In contrast, the stock increased with increase of stem density (Fig. 2b, d). Significant differences (P < 0.05) were found among the stands in most months during the dwarf bamboo growing period, 2003. In addition, the N:P ratios did not differ significantly among the three stands with values approximating 10 (Table II). TABLE II Dynamics of N to P ratios in leaves of different bamboo stands with different stem densities during one growing period, 2003 Standa)

N to P ratio in leaves May

Dl Dm Dh

1.35b)

10.57 ± 10.71 ± 2.03 a 10.17 ± 0.98 a

ac)

Jun.

Jul.

Aug.

Sep.

Oct.

9.55 ± 1.12 a 9.16 ± 1.73 a 9.34 ± 1.24 a

10.81 ± 2.33 a 10.82 ± 2.15 a 10.38 ± 3.02 a

11.37 ± 1.47 a 11.20 ± 1.67 a 10.76 ± 2.17 a

11.48 ± 2.06 a 9.10 ± 1.85 b 10.10 ± 1.36 a

9.06 ± 0.87 a 9.34 ± 1.02 a 9.49 ± 0.65 a

a) Dl

= low-density stand, Dm = medium-density stand, Dh = high-density stand. ± standard deviation (n = 5). c) Means within a column followed by the same letter are not significantly different (P > 0.05). b) Mean

Dynamics of N and P resorption efficiency and proficiency There was no significant effect of stem density on the dynamics of both N and P resorption efficiency and proficiency (Fig. 3). For nitrogen resorption efficiency, the three stands shared the same highest value (77%) in July and lowest value (63%) in June and there was no significant difference (P > 0.05) among May, July, and October. The same trend was exhibited between June and September.

Fig. 3 Monthly dynamics of leaf N resorption efficiency (REN ) (a), N concentration in senesced leaves (b), leaf P resorption efficiency (REP ) (c), and P concentration in senesced leaves (d) of the three bamboo stands with different stem densities from May to October, 2003. Dl = low-density stand, Dm = medium-density stand, Dh = high-density stand. Bars indicate standard deviation (n = 7).

However, P resorption efficiency was significantly higher (P < 0.05) in Dh than in the other stands; no significant differences (P > 0.05) were observed between Dl and Dm. In the three stands (Dl, Dm, and Dh), the highest P resorption efficiency, 62%, 63%, and 75%, respectively, were observed in October, and the lowest, 28%, 30%, and 53%, respectively, in August. No significant (P > 0.05) differences were observed between May and October. The N and P concentrations in senesced leaves decreased with increase of stem density (Fig. 3b, d). According to Killingbeck (1996), therefore, the N resorption proficiency and the P resorption proficiency increased with increase of stem density. Significant differences (P < 0.05) were observed between Dl and Dh. All the three stands had lowest N and P resorption proficiency in July.


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N and P use efficiency There was significant effect of stem density on leaf-level N and P use efficiency (Table III). The N use efficiency increased significantly (P < 0.05) with increase of stem density. Similar results were also observed in one of its components, nitrogen productivity. However, no significant (P > 0.05) differences were observed in N mean residence time among the three stands. In contrast, P use efficiency also increased with increase of stem density, but its two components exhibited an inverse tendency. Phosphorus productivity significantly (P < 0.05) decreased with increase of stem density, while the P mean residence time increased significantly (P < 0.05). TABLE III N and P use efficiency (NUE and PUE) and their two components, productivity and mean residence time (MRT) in leaves of different bamboo stands with different stem densities Standa)

N productivity g−1

year−1

g 60.89 ± 4.57b) ac) 86.88 ± 10.25 b 126.56 ± 8.26 c

Dl Dm Dh

N MRT year 4.34 ± 0.51 a 4.26 ± 0.67 a 4.11 ± 1.01 a

NUE g−1

g 264.52 ± 41.25 a 370.12 ± 28.37 b 520.16 ± 39.75 c

P productivity g−1

year−1

g 515.71 ± 63.24 a 428.51 ± 45.71 b 382.70 ± 29.85 c

P MRT

PUE

year 2.08 ± 0.13 a 2.65 ± 0.34 b 3.50 ± 0.28 c

g g−1 1 072.27 ± 94.58 a 1 135.58 ± 87.50 b 1 339.45 ± 96.67 c

a) Dl

= low-density stand, Dm = medium-density stand, Dh = high-density stand. ± standard deviation (n = 5). c) Means within a column followed by the same letter are not significantly different (P > 0.05). b) Mean

DISCUSSION Nutrient concentrations and stocks The higher-density stands had higher nutrient stocks, but lower concentrations. Since nutrient stocks are often determined by biomass, and denser stands have higher leaf biomass (Wu et al., 2005a), the higher-density stands therefore exhibited higher stocks. Dilution effects, where accumulated dry mass may dilute nutrients (Chapin, 1980), may be the other possible reason for the higher productivity in higher-density stands (Wang et al., 2004). The dynamics of leaf nutrient concentrations and stocks was almost independent of stem density during the dwarf bamboo growing period, being likely attributed to climate (temperature and precipitation) as described in Fig. 1. Clonal plants, like dwarf bamboo, can be united together with a strong underground (rhizome) system and can share the same resources in the entire stand (Hutchings, 1999). Provided that the favorable climatic conditions occurred, all the resources would be transformed to carbon-fixing organs, but the resources in leaves would be rapidly transformed to perennial tissues when the climatic conditions became unfavorable (Cooke and Weih, 2005). Although stem density had no significant effect on leaf nutrient dynamics, the pattern may be more sensitive to climatic changes in lower-density stands owing to less regulative ability (Wu et al., 2005c). Nevertheless, the results did not indicate such an effect, and this needs further study. According to Koerselman and Meuleman (1996), biomass production is N-limited when the N:P ratio is < 14 in plant tissues, which is confirmed by several other studies (G¨ usewell, 2004). In the present study, the N:P ratios in leaves approximated 10, and there were no significant monthly differences among stands (Table II), suggesting that N may be the limiting nutrient in the study area. This finding is in agreement with that of Li (1997). It will therefore be of interest to compare the difference in using limiting and non-limiting nutrients. Nutrient use efficiency The dwarf bamboo density played different roles in resorbing limiting (N) and non-limiting (P) nu-

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trients in this study. It had considerably strong effect on P resorption efficiency, but little effect on N resorption efficiency. Faced with much stronger internal competition, dwarf bamboo stands of higher density often show higher nutrient resorption efficiency, presumably to alleviate the pressure of internal competition (Sprugel, 1984). With respect to limiting nutrients, plants can not resorb more in the higher density stand owing to the resource limitation. The results may, therefore, reveal an efficient mechanism where plants conserve and re-use limiting nutrients in natural systems, and more efficient re-use of the non-limiting nutrients by higher density stands. The same conclusion can also be drawn from the nutrient resorption proficiency (Killingbeck, 1996) in this study, that is, both N and P resorption proficiency increased with increase of stem density as both N and P concentrations in senesced leaves decreased. The dwarf bamboo density did not influence the dynamics pattern of nutrient resorption efficiency and proficiency significantly. Several authors have reported considerable nutrient resorption from senesced leaves at the end of a plant growing period (Aerts, 1996; Renteria et al., 2005), while only a few have paid attention to the dynamics of nutrient resorption efficiency (Wang et al., 2003). Our nutrient resorption efficiency results also showed a pattern similar to the study of Wang et al. (2003). At the beginning and end of the growing period, several nutrients were resorbed from senesced leaves. For limiting nutrients such as nitrogen in this study, the plants did not absorb enough from the soil for rapid growth in July; the plants used them more efficiently partly through high resorption efficiency (Lim and Cousens, 1986). This mechanism may be an efficient strategy of plants as an adaptation to low-nutrient habitats. Furthermore, the values of nutrient resorption efficiency were higher in this study than reported for trees (Finzi et al., 2001; Renteria et al., 2005) and herbs (Niva et al., 2003). The results suggested that shrubs played an important role in forest ecological processes, especially in nutrient cycling (Yarie, 1980). However, there were no reports of overstorey tree nutrient use mechanisms in such sites. By analyzing the productivity and MRT of N and P, it was found that the dwarf bamboo stands of higher density used both nutrients more efficiently, but they developed different strategies in using limiting and non-limiting nutrients among the three stands. With respect to the limiting nutrients such as N, owing to the stronger internal competition in the higher density stands, their transformation to biomass was more efficient (Sprugel, 1984), showing higher productivity (Hirose, 1971), thus suggesting that plants of higher density had more efficient nutrient utilization strategies. Therefore, the higher density stands should also have higher P productivity; however, in fact, our study showed the opposite. This can be explained by luxury consumption of phosphorus in the leaves (Chapin, 1980); the leaves absorbed more nutrients for further growth but did not increase productivity simultaneously. As a result, the higher density stands conserved P more efficiently and employed higher P MRT, compensating for lower P productivity (Eckstein and Karlsson, 1997). Generally, there are two main ways to increase nutrient MRT: 1) having leaves with a long life span; and 2) resorbing N from senescing leaves with high efficiency (Eckstein et al., 1999). Although the life span of dwarf bamboo leaves decreased with increase of stem density because of shading (Li, 1997), nutrient MRT was positively related to nutrient resorption efficiency (Fig. 3, Table IV) in this study. We did not observe significant differences of N MRT among the three stands as N resorption efficiency and P MRT increased with increase of stem density, and so did P resorption efficiency. Therefore, nutrient resorption efficiency determined the nutrient MRT in the dwarf bamboo stands rather than the leaf life span (Tateno and Kawaguchi, 2002). Results of N and P use efficiency implied that the dwarf bamboo stands had efficient strategies for conserving limiting nutrients regardless of the stem density. Further, the higher density stands developed higher productivity of limiting nutrients, and conserved non-limiting nutrients more efficiently, thus showing greater efficiency in the use of both nutrients. In contrast, owing to rapid turnover rate of non-limiting nutrients and lower productivity of limiting nutrients, the lower density stands were less efficient in using nutrients. In conclusion, dwarf bamboo density had little effect on the dynamics of leaf nutrient characteristics; however, higher density stands stored more nutrients but had lower nutrient concentrations in


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leaves. Using and resorbing limiting or non-limiting nutrients, dwarf bamboo stands with different stem densities developed different utilization and conservation strategies although the higher density stands used both N and P more efficiently by virtue of higher N productivity and P MRT. As a whole, the results revealed that dwarf bamboo stands with different stem densities had different strategies for using limiting and non-limiting nutrients and that the higher density stands could have more efficient nutrient utilization strategies, especially when a nutrient is limiting. ACKNOWLEDGMENTS Many thanks are due to Prof. Katharine Dickinson, Department of Botany, Otago University, New Zealand and Dr. Yin Chunying, Chengdu Institute of Biology, Chinese Academy of Sciences, who have patiently read the manuscript and made valuable suggestions. The authors also would like to thank Dr. Qi Zemin of the Wanglang National Nature Reserve, Sichuan, China, for his help in the field work, and Qiao Yunzhou of the Wanglang National Nature Reserve, Sichuan, China, for his help during laboratory experiments. REFERENCES Aerts, R. 1996. Nutrient resorption from senescing leaves of perennials: are there general pattern? J. Ecol. 84: 597–608. Aerts, R. and Caluwe, H. 1994. Nitrogen use efficiency of Carex species in relation to nitrogen supply. Ecology. 75: 2 362–2 372. Aerts, R. and Chapin III, F. S. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv. Ecol. Res. 30: 1–67. Berendse, F. and Aerts, R. 1987. Nitrogen-use-efficiency: a biological meaningful definition? Funct. Ecol. 1: 293–296. Chapin III, F. S. 1980. The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11: 233–260. Cooke, J. E. K. and Weih, M. 2005. Nitrogen storage and seasonal nitrogen cycling in Populus: bridging molecular physiology and ecophysiology. New Phytol. 167: 19–30. Del Arco, J. M., Escudero, A. and Garrido, M. V. 1991. Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology. 72: 701–708. Eckstein, R. L. and Karlsson, P. S. 1997. Above-ground growth and nutrient use by plants in a subarctic environment: effects of habitat, life-form and species. Oikos. 79: 311–324. Eckstein, R. L. and Karlsson, P. S. 2001. Variation in nitrogen-use efficiency among and within subarctic graminoids and herbs. New Phytol. 150: 641–651. Eckstein, R. L., Karlsson, P. S. and Weih, M. 1999. Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol. 143: 177–189. Franklin, J. F., Maeda, T., Ohsumi, Y., Matsui, M., Yagi, H. and Hawk, G. M. 1979. Subalpine coniferous forests of central Honshu, Japan. Ecol. Monogr. 49: 311–334. Finzi, A. C., Allen, A. S., Delucia, E. H., Ellsworth, D. S. and Schlesinger, W. H. 2001. Forest litter production, chemistry, and decomposition following two years of free-air CO2 enrichment. Ecology. 82: 470–484. G¨ usewell, S. 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytol. 164: 243–266. Helmisaari, H. S. 1992. Nutrient retranslocation within the foliage of Pinus sylvetris. Tree Physiol. 10: 45–48. Hutchings, M. J. 1999. Clonal plants as cooperative system: benefits in heterogeneous environments. Plant Species Biol. 14: 1–10. Hirose, T. 1971. Nitrogen turnover and dry matter production of a Solidago altissima population. Jpn. J. Ecol. 21: 18–32. Killingbeck, K. T. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology. 77: 1 716–1 727. Knops, J. M., Bradley, H. K. L. and Wedin, D. A. 2002. Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol. Lett. 5: 454–466. Koerselman, W. and Meuleman, A. F. M. 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33: 1 441–1 450. Li, C. B. 1997. A Study of Staple Food Bamboo for the Giant Panda (in Chinese). Guizhou Science and Technology Press, Guiyang. Lim, M. T. and Cousens, J. E. 1986. The internal transfer of nutrients in a Scots pine stand 2: the pattern of transfer and the effects of nitrogen availability. Forestry. 59: 17–27. Lu, R. K. 1999. Soil and Agro-chemical Analytical Methods (in Chinese). China Agricultural Science and Technology Press, Beijing. Lu, Y. J., Wang, K. Y., Yang, W. Q. and Wu, F. Z. 2005a. Review on interactions between soil and arrow bamboo community. World Sci-Tech R&D (in Chinese). 27(2): 58–62.

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