Nitrogen resorption from senescing leaves in 28 plant species in a semi-arid region of northern China

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1 Journal of Arid Environments Journal of Arid Environments 63 (2005) Nitrogen resorption from senescing leaves in 28 plant species in a semi-arid region of northern China Z.-Y. Yuan a, L.-H. Li a,, X.-G. Han a,, J.-H. Huang a, G.-M. Jiang a, S.-Q. Wan b, W.-H. Zhang c, Q.-S. Chen a a Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Beijing , China b Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN , USA c School of Biological Sciences, The Flinders University of South Australia, G.P.O. Box 2100, Adelaide, SA 5001, Australia Received 19 June 2004; received in revised form 9 December 2004; accepted 27 January 2005 Available online 17 March 2005 Abstract Nitrogen resorption efficiency (NRE) and proficiency of 28plant species belonging to five different life-forms were studied in a semi-arid region of northern China. NRE in these species ranged from 29.8% to 76.1% and averaged about 48.0%, depending upon the species and the life-form. The pattern of NRE in different life-forms followed the order of herbs4shrubs4trees4graminoids4n fixers. Nitrogen resorption proficiency (NRP) ranged from 8.0 to 20.6 mg g 1, the average value of which was lowest in graminoids and highest in N fixing species. Leaf-level nitrogen use efficiency (NUE) ranged from 48.5 g g 1 to 125.8g g 1, with the average NUE being lowest in the N fixing species and highest in the graminoids. Our findings show that most of the 28species examined in this study can be categorized as low N- proficiency plants. The lower nitrogen concentration in living tissues and the greater nitrogen resorption during senescence could have contributed jointly to the leaf-level NUE of the species. It was noted that NRP was negatively correlated to NRE, while a positive correlation between the leaf-level NUE and NRE was found for all the species. We had also found a Corresponding authors. Tel.: addresses: zyyuan@ibcas.ac.cn (Z.-Y. Yuan), xghan@ibcas.ac.cn (X.-G. Han) /$ - see front matter r 2005 Published by Elsevier Ltd. doi: /j.jaridenv

2 192 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) significant positive relation between NRE and the N concentration in green leaves for all the species pulled together, suggesting that green leaf N content might have partially controlled the leaf N resorption. r 2005 Published by Elsevier Ltd. Keywords: Plant leaf nitrogen; Life-form; Nitrogen resorption efficiency and proficiency; Nitrogen use efficiency; Semi-arid ecosystems; China 1. Introduction Nitrogen (N) resorption from senescing leaves is an important mechanism of nitrogen conservation in plants (Aerts, 1996) and may be quantified by nitrogen resorption efficiency (NRE, the proportion of N resorbed from senescing leaves) or by nitrogen resorption proficiency (NRP, the nitrogen concentration in senescing leaves) (Killingbeck, 1996). It is an integral part of the highly ordered process of leaf senescence and appears to occur in most plant species (Noode n, 1988). On average, approximately 50% of the leaf N is recycled via resorption (Aerts, 1996). However, the proportion of N withdrawn from leaves during senescence varies widely among species. It has been estimated that from less than 5% to 80% of the total leaf N may be resorbed (Aerts and Chapin, 2000). Nitrogen resorption allows leaf N to be reused rather than lost with leaf fall, thus extending the mean residence time of N in plant tissues (Eckstein et al., 1999). Higher NRE and longer mean residence time are adaptation advantages for plants in infertile habitats (Eckstein et al., 1999; Aerts and Chapin, 2000). A number of studies have shown that species from N-poor habitats have higher NRE (Pensa and Sellin, 2003; Yuan et al., 2005b). However, high NRE is characteristic of nearly all perennial plants and appears not to be very responsive to changes in N supply (Aerts, 1996; Aerts and Chapin, 2000). Therefore, NRE is an important index to assess the capability for plants to conserve N, but it can not explain the distribution of life-forms over habitats differing in soil fertility. NRP can be used to describe the level to which leaf N is reduced during senescence (Killingbeck, 1996), with a higher NRP corresponding to a lower final N concentration. The inverse of the N concentration in leaf litter has been used as an index of nitrogen use efficiency (NUE) (Vitousek, 1982). There is a close relationship between N resorption proficiency and N use efficiency (Eckstein et al., 1999; Aerts and Chapin, 2000). Compared with NRE, NRP seems to be more responsive to N availability. Several studies reported that N fertilization resulted in higher N concentrations in the litter of most plant species (van Heerwaarden et al., 2003b), suggesting that N fertilization could lead to lower NRP. The relationship between NRP and N availability was also found along natural fertility gradients (Carrera et al., 2003; Distel et al., 2003; Wright and Westoby, 2003; Yuan et al., 2005a). In contrast to NRE, there are clear differences in NRP among life-forms (Aerts, 1996; Killingbeck, 1996).

3 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) So far, studies on the N resorption in plant species have been conducted mainly in USA and Europe. Most of these studies concern trees and shrubs, while studies on herbaceous species are relatively lacking (see review by Aerts, 1996). To our knowledge, the herbaceous species from semi-arid regions of northern China have drawn little attention and their N resorption characteristics have never been examined. The agro-pastoral ecotone of Duolun, which is located on the southern edge of the Inner Mongolian Autonomous Region, northern China, is characterized by a semiarid climate and poor soil nutrients. This area has been an important livestock farming base and a key water conserving zone for Beijing city. However, due to intensive human activities (e.g. cultivation and over-grazing) in recent years, desertification is becoming more and more serious, and the landscape has become scattered areas of sand-covered grasslands and eroded croplands. How effectively plants utilize N is critical for their growth, competition and survival under the harsh environment. A better understanding of the N resorption patterns in different plant species and life-forms in this area will help to understand the N use strategies and thus help to restore the ecological systems in northern China. The objectives of the study were: (1) to compare the N resorption characteristics and patterns in different plant species and life-forms native to this area; (2) to examine the relations among the nitrogen use traits (i.e. NRE, NRP and NUE); (3) to tentatively figure out the environmental and species or life-form related mechanisms in regulating the nitrogen use traits of the species. 2. Materials and methods 2.1. Study area and species The study was carried out in the north of Duolun County ( N, E, 1380 m above sea level). The climate belongs to the semi-arid monsoon climate of moderate temperature zone, with mean monthly air temperatures ranging from C in January to C in July and an annual mean temperature of 1.6 1C. Mean annual precipitation is 385 mm, with the maximum monthly value occurring in July or August. The average growing season is about 150 days. The soils in the study area are chestnut soils (Chinese classification) and Calcic-orthic Aridisol in the US soil taxonomy classification system. The major vegetation type is typical steppe, and the dominant plant species include Leymus chinensis, Stipa spp., Agropyron cristatum, Artemisia frigida, Cleistogenes squarrosa, and Chenopodium album. The field investigations were conducted in a woodland in the permanent plot of the Duolun Restoration Ecology Research Station, the Chinese Academic Sciences, which consists of scattered areas of typical steppe, mixed forest, sandland and shrubland, etc. The total area is about 1000 ha. The ground is relatively flat and well conserved, where livestock grazing had been excluded for 5 years. Plants selected for the study were the dominant species of the major stands or communities in this area. In total, 28vascular plant species belonging to 12 families and 5 life-form groups

4 194 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) (i.e. trees, shrubs, graminoids, herbs, N fixers) were examined in the study. The lifeforms were divided according to the definition by Eckstein et al. (1999) and Quested et al. (2003) Sampling and chemical analysis Green and senescing leaves were collected in the field from July to October In July, 10 g fully expanded green leaves were randomly collected from five marked individuals of each species. In autumn (late September to early October), similar collections were made for senescing leaves. For species with shedding leaves, senescing leaves were collected as dead leaves that were ready to abscise. We considered leaves ready to abscise if they were completely dry yellow without signs of deterioration (Norby et al., 2000; Wright and Westoby, 2003). These leaves were easily identified as they displayed colours (often red or yellow) different from live leaves, and can be removed by a gentle flicking of the branch or leaf. For species that retained dead leaves on the plants (all monocotyledons), leaves that were functionally disconnected from the shoot were cut off and collected. Senescing leaves were collected directly from plants rather than from leaf litter, as we were concerned that decomposition of leaf litter and leaching of leaf N would lead to underestimates of N concentration in senescing leaves. Leaves with obvious evidence of substantial mechanical damage or biotic alteration (leaves with insects, bird droppings, disease, etc.) were not sampled, and bias in terms of size, shape, or colour was minimized. Petioles and the rachides of compound leaves were generally shed as an integral component of the senescing leaves and therefore collected and processed as above. The samples were immediately taken to the laboratory, oven dried at 60 1C for at least 48h, and then finely ground in a Wiley mill to pass a 40-mesh screen for later analysis. Nitrogen concentration was analysed colorimetrically by Kjeldahl acid-digestion method with an Alpkem autoanalyzer (Kjektec System 1026 Distilling Unit, Sweden) Calculations Nitrogen concentrations in green and senescing leaves were used to calculate N resorption efficiency (NRE) on a mass basis (Killingbeck, 1996), from which N use efficiency (NUE, Vitousek, 1982) was also derived: NREð%Þ ¼ððN g N s Þ=N g Þ100%, (1) NUEðgg 1 Þ¼1=ðN g ð1 NREÞÞ, (2) where N g and N s are the N concentration in the green leaves and senescing leaves, respectively. Nitrogen concentration in senescing leaves was used directly as an indicator of the NRP (Killingbeck, 1996). NRP can be viewed as a measure of the completeness of N resorption in terms of proximity to the theoretical lower limit of the N concentration in senescing leaves.

5 2.4. Statistical analysis ARTICLE IN PRESS Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) Data were analysed using SAS 8.2 (SAS Institute, Inc., Cary, NC, USA). We employed GLM procedure to test the effects of life-form and species on N concentration, N resorption and NUE. Linear regression analysis (REG Procedure) was performed to analyse the relationships between the various parameters. 3. Results Both species and life-forms have significant effects (po0.001) on N concentration in green leaves. The lowest N concentration (15.8mg g 1 ) in green leaves was found in Calamagrostis and highest (37.9 mg g 1 )inchenopodium (Table 1). Among the five life-forms, graminoids had the lowest (18.8 mg g 1 ) N concentration in green leaves, whereas highest N concentration was found in the N-fixing species (29.2 mg g 1 ). Herbs had greater foliar N concentrations than woody and graminoid species due to the fact that several herb plants grew in N-rich habitat (Table 2). N concentration in the green leaves of different life-forms was in the order of graminoidotreeoshruboherb on fixer (Table 2). Nitrogen concentration in senescing leaves ranged from 8.0 mg g 1 in Potentilla to 20.6 mg g 1 in Melissitus (Table 1). There was a significant difference in the N concentration of senescing leaves among species and life-forms (Tables 2 and 3). Nitrogen concentration in senescing leaves was lowest in graminoids (10.8mg g 1 ) and highest in N fixing species (17.8mg g 1 ). Values of N concentration of senescing leaves indicate that NRP differed among the five life-forms. According to Killingbeck s (1996) benchmarks of complete N, all species had incomplete N resorption (Table 1). Both species and life-forms significantly affected NRE (po0.001). NRE ranged from 29.8% in Melissitus to 76.1% in Polygonum (Table 1), with an average of 48.0%. NRE was lower in the N fixers (38.9%) than in the non-n 2 -fixers (49.9%). The pattern of NRE of different life-forms followed the order of herbs4shrubs4trees4graminoids4n fixers (Table 2). There was a significant difference in NUE among the species and life-forms (Table 3). Leaf-level NUE ranged from 48.5 g g 1 in Melissitus to 125.8g g 1 in Potentilla. NUE was lowest in the N fixers (58.1 g g 1 ) and highest in the graminoids (93.2 g g 1 ). NRE, NUE, and N concentrations in green and senescing leaves were plotted against each other to examine whether there were possible relations among these parameters (Fig. 1). A significant (r ¼ 0.413, po0.05) linear correlation was found between N concentrations in senescing and in green leaves (Fig. 1a). Similarly, there was a clear positive correlation (r ¼ 0.450, po0.05) between NRE and N concentration in the green leaves (Fig. 1b). In contrast, NRE was negatively correlated to N concentration in the senescing leaves (Fig. 1c). Furthermore, we found a negative correlation between leaf-level NUE and the N concentration in

6 196 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) Table 1 Nitrogen concentrations in green leaves (N g ) and in senescing leaves (N s ), nitrogen resorption efficiency (NRE) and nitrogen use efficiency (NUE) of individual plant species in northern China Life-form Species N g (mg g 1 ) N s (mg g 1 ) NRE (%) NUE (g g 1 ) Trees Betula platyphylla 22.8(2.7) 12.1 (1.5) 46.9 (4.2) 82.4 (7.6) Ulmus macrocarpa 26.5 (1.1) 10.3 (1.4) 61.2 (7.4) 97.5 (8.4) Prunus armeniaca 22.1 (2.0) 12.6 (0.9) 42.7 (5.4) 79.2 (5.7) Prunus padus 19.5 (0.9) 10.3 (0.7) 47.1 (3.1) 97.0 (10.9) Malus baccata 20.9 (2.4) 12.3 (1.8) 40.9 (4.9) 81.0 (5.2) Shrubs Salix flavida 26.5 (2.1) 10.8(0.7) 59.4 (4.4) 92.8(6.3) Salix microstachya 27.7 (4.2) 15.3 (0.6) 44.8(4.1) 65.5 (3.6) Rosa xanthina 25.2 (3.1) 11.2 (1.6) 55.7 (5.1) 89.4 (6.2) Graminoids Leymus chinensis 21.6 (6.0) 11.5 (1.7) 45.8 (7.5) 87.2 (8.9) Stipa grandis 19.6 (2.7) 9.9 (2.7) 49.4 (5.6) (8.9) Stipa grandis 18.4 (2.7) 10.7 (3.3) 41.8 (4.7) 93.5 (8.2) Agropyron cristatum 16.8(2.6) 10.4 (3.2) 35.6 (7.2) 95.9 (7.9) Carex korshinskyi 20.8(3.5) 12.9 (3.4) 37.6 (5.1) 77.3 (5.5) Calamagrostis epigejos 15.8(1.5) 9.6 (1.3) 39.3 (4.0) (9.2) Herbs Sanguisorba officinalis 29.2 (7.0) 8.2 (1.8) 71.8 (9.7) (12.7) Sanguisorba officinalis 30.5 (2.1) 9.1 (2.8) 70.2 (8.6) (8.6) Polygonum divaricatum 34.4 (4.9) 8.2 (2.4) 76.1 (10.4) (8.8) Potentilla tanacetifolia 30.6 (4.3) 8.0 (1.5) 74.0 (8.2) (10.7) Artemisia frigida 21.1 (1.8) 11.8 (1.6) 43.9 (4.6) 85.1 (6.4) Artemisia sieversiana 30.1 (2.0) 15.0 (2.0) 50.5 (5.6) 66.7 (5.7) Artemisia scoparia 21.5 (1.6) 12.9 (2.0) 39.8(4.0) 77.3 (8.7) Chenopodium album 37.9 (2.9) 19.1 (2.0) 49.6 (6.7) 52.4 (5.4) Thalictrum squarrosum 17.7 (2.7) 9.9 (1.0) 44.1 (8.8) (9.9) Linum perenne 31.9 (2.2) 17.4 (1.9) 45.5 (5.0) 57.6 (3.2) Helianthus annuus 31.6 (2.6) 18.7 (1.8) 40.9 (6.7) 53.5 (3.6) N fixers Lespedeza bicolor 21.5 (3.1) 14.9 (2.5) 30.4 (3.1) 67.0 (8.2) Lespedeza bicolor 28.3 (4.9) 19.4 (3.2) 31.4 (4.7) 51.5 (5.0) Hedysarum laeve 26.6 (5.0) 10.2 (1.3) 61.5 (5.8) 97.7 (7.7) Vicia crocca 25.3 (1.6) 15.0 (2.8) 40.8 (5.2) 66.7 (6.8) Vicia crocca 27.6 (2.7) 18.4 (1.6) 33.5 (5.3) 54.4 (3.2) Thermopsis lanceolata 35.0 (4.0) 15.7 (1.9) 55.0 (5.2) 63.6 (6.6) Melissitus ruthenica 29.3 (3.8) 20.6 (2.9) 29.8 (3.8) 48.5 (2.7) All data 25.4 (3.7) 12.9 (2.6) 48.0 (2.2) 87.7 (8.6) Data are means with S.D. in parenthesis. green leaves (Fig. 2a) and a positive correlation between leaf-level NUE and NRE (Fig. 2b) for all the species. 4. Discussion The majority of the 28investigated species in the semi-arid region withdrew less than 50% of N from their senescing leaves (Table 1). These NRE values were

7 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) Table 2 Average values of nitrogen concentrations in green leaves (N g ) and in senescing leaves (N s ), nitrogen resorption efficiency (NRE) and nitrogen use efficiency (NUE) for different life-forms Life-form n N g (mg g 1 ) N (mg g 1 ) NRE (%) NUE (g g 1 ) Trees (2.6) 11.5 (1.2) 47.8(13.96) 87.4 (13.0) Shrubs (3.7) 12.4 (3.4) 53.3 (11.4) 82.6 (12.9) Graminoids (2.3) 10.8(1.2) 41.6 (10.2) 93.2 (18.0) Herbs (4.8) 12.6 (3.8) 55.1 (15.4) 80.5 (18.7) N fixers (3.5) 17.8 (3.3) 38.9 (8.9) 58.1 (11.2) Data are means7s.d. with the number of replication (n). Table 3 ANOVA for the effects of species and life-forms on nitrogen concentrations of green leaves (N g ) and senescing leaves (N s ), nitrogen resorption efficiency (NRE) and nitrogen use efficiency (NUE) based on the data presented in Table 1 N g (mg g 1 ) N s (mg g 1 ) NRE (%) NUE (g g 1 ) Species F p o0.001 o0.001 o0.001 o0.001 Life-form F p o0.001 o0.001 o relatively low compared with those found based on leaf mass in other studies (Carrera et al., 2003; Quested et al., 2003; van Heerwaarden et al., 2003b). However, the average NRE of 48% for all the species investigated in our study was good compared with the reported average value of NRE based on a large number of plant species worldwide (50.3%) (Aerts, 1996), and the NRE values for the five life-forms in our study were also comparable to those reported in similar studies. For example, the NRE values of 0 79% for deciduous trees (Chapin and Kedrowski, 1983) and 22 38% for deciduous shrubs in a semi-arid sandland of northern China (He and Zhang, 2003) had been reported. Our results indicated that the NRE of plant species in the semi-arid region of northern China was at the lower end of the values compiled by Aerts (1996) and Killingbeck (1996) for a wide range of ecosystems. Large differences in NRE were observed among species and life-forms in the present study. For instance, N-fixing species exhibited the lowest NRE while herbs showed the highest NRE, which was consistent with previous studies (Killingbeck and Whitford, 2001; Quested et al., 2003). Our results revealed that the average NRE values of the woody plants (49.8%) and the graminoid plants (41.6%) in this study were lower than those reported elsewhere (Killingbeck, 1996). Terrestrial plants grown in N-poor environments can adapt to N stress with different strategies at the species and the community level, including luxury consumption, reduced growth rates, increased leaf longevity, reduced leaching and N uptake by leaves (Chapin,

8 198 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) y = 0.263X r = 0.413, P< (a) N concentration in green leaves (mg g -1 ) N concentration in senescing leaves (mg g -1 ) N resorption efficiency (%) y = 1.000X r = 0.450, P< (b) N concentration in green leaves (mg g -1 ) N resorption efficiency (%) y = X r = ,P <0.01 (c) N concentration in senescing leaves (mg g -1 ) Fig. 1. (a) Relationship between N concentrations in senescing and green leaves; (b) relationship between N resorption efficiency and N concentration in green leaves; (c) relationship between N resorption efficiency and N concentration in senescing leaves. Each point represents an individual plant. Symbols: m trees; * shrubs; E graminoids; J herbs; & N fixers. 1980). Differences in the N strategy could help to explain the variations in NRE among species and life-forms observed in our study. Differences in the definition and estimates of NRE would contribute to the inconsistency among studies (van Heerwaarden et al., 2003a). NRE calculated on the basis of dry mass is influenced to a certain extent by dry-matter loss from leaves during senescence, which could change substantially with individuals, sites and years (Chapin and Kedrowski, 1983; van Heerwaarden et al., 2003a). Therefore, massbased NRE is limited in assessing N resorption. Estimates of proportional N resorption made on the basis of leaf area may be more accurate than those made on the basis of leaf mass for some species, especially broad-leaved hardwood trees and

9 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) Leaf-level NUE (g g -1 ) (a) y = X r = , P> N concentration of green leaves (mg g -1 ) leaf-level NUE (g g -1 ) (b) y = 1.217X r = 0.704, P< N resorption efficiency(%) Fig. 2. (a) Relationship between leaf-level nitrogen use efficiency (NUE) and N concentration in mature green leaves. (b) Relationship between leaf-level nitrogen use efficiency (NUE) and N resorption efficiency. Each point represents an individual plant. Symbols: m trees; shrubs; E graminoids; J herbs; & N fixers. shrubs. However, in a study on six sub-arctic bog species, van Heerwaarden et al. (2003b) reported that no different responses of NRE to N supply were found from the calculations based on both leaf area and leaf mass. Therefore, mass-based NRE data were still used in recent papers (Carrera et al., 2003; Oleksyn et al., 2003; Quested et al., 2003). N concentration in senescing leaves varied widely between 8.0 and 20.6 mg g 1 among species (Table 1). Killingbeck (1996) suggested that plants with high N concentration in senescent leaves (410 mg g 1 ) could be considered to be low N- proficient, while those with low N concentration in senescent leaves (o7mgg 1 ) might be identified to be high N-proficient. According to this criterion, most of the 28species examined in our study can be categorized as the low N-proficient plants. This result seems to be unexpected because plants growing under N limitation are more likely to reach complete resorption of this nutrient (Aerts and Chapin, 2000; van Heerwaarden et al., 2003b). These findings suggest that other environmental factors, such as drought, might have also been involved in the control of NRP. Nitrogen concentration in senescent herb foliage (12.6 mg g 1 ) was higher than that in senescent graminoid foliage (10.8mg g 1 ), suggesting that graminoids may be more proficient at resorbing N than herbs according to Killingbeck s (1996) definition of NRP. Our results are consistent with earlier reports that there are considerable differences in NRP among species and life-forms (Killingbeck, 1996; Aerts and Chapin, 2000). Mass-based NRP is directly related to the decomposition characteristics of leaves, i.e. the amount of N returned to the soil is largely determined by the leaf litter N quantity (Quested et al., 2003), with a high NRP value being associated with relatively low leaf litter decomposition and N releasing rates (Moretto and Distel, 2003). Therefore, change in the dominance of different lifeforms could influence soil N cycling at the local scale, with possibly consequent

10 200 Z.-Y. Yuan et al. / Journal of Arid Environments 63 (2005) feedbacks on the growth and competition among plant species and life-forms with different N strategies (Berendse, 1994; Aerts, 1999; Distel et al., 2003). Nitrogen resorption is critical in affecting N status of senescent leaves and litter quality among different species, life-forms, and habitats. Our results showed that N concentration in senescing leaves in 28species was generally correlated with that in the green leaves (Fig. 1a). However, NRE showed a positive linear correlation with N concentration in green leaves (Fig. 1b) but a negative correlation with N concentration in the senescing leaves (Fig. 1c). The above results suggest that plants with higher N concentration in green leaves were capable of withdrawing a higher percentage of N from leaves, resulting in a lower N content in the leaf litter. The significant positive correlation between NRE and N concentration in green leaves observed in our study (Fig. 1b) was consistent with those reported in previous studies (Chapin, 1980; Anderson and Eickmeier, 2000). However, Aerts (1996) found no relationships between NRE and plant N status, which could result from a partial control of leaf N resorption over leaf N concentration by providing a large source of osmotically active substances in the senescing leaves. Other factors such as soil N availability have also been found to affect NRE (Chapin and Kedrowski, 1983; Enoki and Kawaguchi, 1999). Resorption from senescing leaves may reduce N loss from the whole plant and increase the mean residence time of nitrogen (Eckstein et al., 1999; Yuan et al., 2005a, b). Therefore, leaf-level NUE of the plant will increase with the increased NRE (Aerts and Chapin, 2000). Higher leaf-level NUE may partly result from the lower N concentration in green leaves and higher NRE. In terrestrial plants, leaf N content accounts for a large part of the whole-plant N (Reich et al., 1992; Yasumura et al., 2002). In addition, cumulative photosynthetic NUE at the leaf level will largely determine NUE at the plant level because leaves are the only organ conducting carbon assimilation in plants (Eckstein et al., 1999; Aerts and Chapin, 2000). Therefore, leaf level NUE could be used as a proxy estimate of NUE at the wholeplant level. In this study, we had observed significant differences in N resorption and N utilization characteristics among different species and life-forms in a semi-arid region of northern China. The results suggest that there may be substantial differences in nitrogen resorption patterns and processes among plant species and life-forms, which will help to explain the strategies for plants to adapt to N-related habitats and their roles in the biotic nitrogen cycling in semi-arid ecosystems of northern China. Acknowledgements We thank the director and the staff of the Grassland Management Station of Duolun County for their help in field and laboratory work. Thanks also to insight comments from two anonymous reviewers to improve the manuscripts. This study was jointly supported by National Basic Research Program of China ( ), CAS Project of Knowledge Innovation Program (No. KZCX1-SW-01-04) and the outstanding overseas scientists team program of the Chinese Academy of Sciences.

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