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Plant Soil (2008) 306:149–158 DOI 10.1007/s11104-008-9565-9 REGULAR ARTICLE Changes in nitrogen resorption traits of six temperate grassland species along a multi-level N addition gradient Ju-Ying Huang & Xiao-Guang Zhu & Zhi-You Yuan & Shi-Huan Song & Xin Li & Ling-Hao Li Received: 25 April 2007 / Accepted: 28 January 2008 / Published online: 22 February 2008 # Springer Science + Business Media B.V. 2008 Abstract Nitrogen (N) resorption from senescing leaves is an important mechanism of N conservation for terrestrial plant species, but changes in Nresorption traits over wide-range and multi-level N addition gradients have not been well characterized. Here, a 3-year N addition experiment was conducted to determine the effects of N addition on N resorption of six temperate grassland species belonging to three different life-forms: Stipa krylovii Roshev. (grass), Cleistogenes squarrosa (T.) Keng (grass), Artemisia frigida Willd. (semishrub), Melissitus ruthenica C.W. Wang (semishrub and N-fixer), Potentilla acaulis L. (forb) and Allium bidentatum Fisch.ex Prokh. (forb). Generally, N concentrations in green leaves increased asymptotically for all species. N concentrations in senescent leaves for most species (5/6) also increased asymptotically, except that the N concentration in Responsible Editor: Alfonso Escudero. J.-Y. Huang : X.-G. Zhu : Z.-Y. Yuan : S.-H. Song : X. Li : L.-H. Li (*) Key Laboratory of Vegetation and Climate Change, Institute of Botany, the Chinese Academy of Sciences, Xiangshan, Beijing 100093, People’s Republic of China e-mail: [email protected] J.-Y. Huang : X.-G. Zhu Graduate University of the Chinese Academy of Sciences, Yuquanlu, Beijing 100049, People’s Republic of China senescent leaves of A. bidentatum was independent of N addition. N-resorption efficiency decreased with increasing N addition level only for S. krylovii and A. frigida, while no clear responses were found for other species. These results suggest that long-term N fertilization increased N uptake and decreased Nresorption proficiency, but the effects on N-resorption efficiency were species-specific for different temperate grassland species in northern China. These interspecific differences in N resorption may influence the positive feedback between species dominance and N availability and thus soil N cycling in the grassland ecosystem in this region. Keywords Leaf N concentration . N cycling . N fertilization . N-resorption efficiency and proficiency . Semi-arid grassland ecosystem . Species composition Introduction Nitrogen (N) resorption from senescing leaves is an important mechanism of N conservation, which minimizes the dependence of terrestrial plants on N uptake from soils and increases N-use efficiency (Aerts 1996; Killingbeck 1996). Previous studies on N resorption focused mainly on whether species from N-poor habitats have higher N-resorption efficiency (the proportional N withdrawn from senescent leaves prior to abscission, NRE) or N-resorption proficiency 150 (the terminal N concentration in senescent leaves, NRP) (Cote et al. 2002; Oleksyn et al. 2003; Richardson et al. 2005). It has been shown that there is no clear nutritional control on NRE, and NRE does not explain the distribution of growth-forms over habitats differing in soil N availability (Aerts 1996; Aerts and Chapin 2000). Killingbeck (1996) alleged that NRP is more responsive to changes in N availability. This allegation is supported by a number of recent studies (e.g., Cordell et al. 2001; Kobe et al. 2005; van Heerwaarden et al. 2003a; Wright and Westoby 2003). In contrast to NRE, there are significant differences in NRP between growth-forms (Aerts 1996). In temperate grasslands, Yuan et al. (2005a) found that the herbs and shrubs were more proficient at N resorbing than the N-fixing species, but less proficient than graminoids. N-resorption responses to changes in soil N availability have been found in previous studies. However, most of these studies were conducted along natural nutrient gradients or within a narrow range of N fertilization. Studies on the changes in N resorption of plants along wide-range and multi-level N availability gradients are almost completely lacking, and it is not clear whether or not these changes are life-form-specific. The temperate grasslands of Inner Mongolia cover a total area of about 0.6 million km2 and constitute a major part of the Eurasian grasslands (Li et al. 1998). It has been noted that some grass species in this region are highly dependent on internal N cycling (Yuan et al. 2004, 2006). However, for plant species of other life-forms, it is not clear whether this mechanism still holds true. If the responses of different species to changing soil N supply are species- or life-form-specific, there will be significant changes in dominant species composition of grasslands where N supply has been increasingly altered by human activities in the region. In this study, we conducted a 3-year experiment of N fertilization in a temperate grassland community to address the following questions: (1) how do N-resorption traits in plant species with different life-forms respond to a wide range of N addition levels? (2) What are the major N-conserving mechanisms for species of different life-forms in terms of N-resorption traits? (3) What are the differential effects of N addition on the dominance of these species in the community and the N-resorption-related mechanisms? Plant Soil (2008) 306:149–158 Materials and methods Study site and experiment design The study was conducted in a long-term N fertilization experiment started in 2002 in a grassland at Duolun County (42°02′N, 116°41′E, 1,380 m a.s.l), Inner Mongolian Autonomous Region, China. The climate is temperate and semiarid with a dry spring and wet summer. Mean annual precipitation is about 385 mm. Mean annual temperature amounts to 1.6°C, ranging from −18.3°C in January to 18.5°C in July. The major soil type of the study site is chestnut soil (Chinese classification), which is equivalent to Calcisorthic Aridisol in United States Soil Taxonomy classification (Yuan et al. 2005b). The vegetation was a degraded typical steppe dominated by Artemisia frigida Willd., Stipa krylovii Roshev. and Allium bidentatum Fisch.ex Prokh. In July 2002, 40 sub-plots measuring 15×10 m were selected on a well-conserved (fenced and free from animal disturbance) and very flat ground in a S. krylovii community. These plots were separated by buffer zones of about 4 m in width. Since 2002, five replication plots have been N fertilized at one of 8 N levels (N levels were 0, 1, 2, 4, 8, 16, 32 and 64 g N m−2 year−1). N fertilizer (NH4NO3) was added in mid-July annually. The sub-plots were aligned randomly in the total plot (150×70 m). In early August 2005, soil properties were investigated (X.L. Zhang et al. unpublished data, Table 1). Field sampling Six perennial plant species in the community belonging to three different life-forms were selected: two grasses (S. krylovii and Cleistogenes squarrosa (T.) Keng); two forbs (Potentilla acaulis L. and A. bidentatum), and two semi-shrubs [A. frigida and Melissitus ruthenica C.W.Wang (also N-fixer)]. From early May to mid-June in 2005, six typical individuals (three for measuring N concentration in green leaves and three for senescent leaves) of each species with similar morphology were selected and tagged in each sub-plot. In early August (peak growth period), fully expanded mature leaves (free from disease and insect damage) were collected from the tagged species, and attached senescent leaves (yellow and ready to drop) Plant Soil (2008) 306:149–158 Table 1 Changes in soil chemical properties for each N addition treatment after 3-year N fertilization 151 N fertilization gradient (g N m−2 year−1) Soil properties Organic C (g kg−1) pH Total N (g kg−1) AmmoniaN (mg kg−1) Nitrate-N (mg kg−1) 0 1 2 4 8 16 32 64 22.42±1.72 22.37±1.77 22.88±1.53 22.89±1.27 24.50±0.66 24.35±1.01 25.57±1.01 24.57±2.43 7.30±0.05 7.31±0.06 7.25±0.04 6.97±0.06 7.03±0.22 6.38±0.19 5.85±0.15 5.79±0.16 2.14±0.15 2.32±0.19 2.30±0.13 2.17±0.16 2.25±0.09 2.46±0.12 2.58±0.11 2.65±0.20 2.60±0.24 2.39±0.23 2.42±0.11 3.23±0.55 2.67±0.35 2.92±0.89 9.60±0.39 15.72±5.26 2.08±0.47 1.48±0.21 1.21±0.30 1.48±0.24 1.71±0.46 2.69±1.54 15.15±2.88 25.46±3.56 were collected by gently clipping in mid-October (Aerts et al. 2007; Güsewell 2005). In early August, live aboveground biomass was sampled by harvesting the standing biomass within 1×1 m2 quadrats and separated according to species. All plant samples were oven-dried at 65°C and weighed. N concentrations in leaves were analyzed colorimetrically by the Kjeldahl acid-digestion method with an Alpkem auto-analyzer (Kjektec System 1026 Distilling Unit, Sweden). NRE was estimated as the percentage of N withdrawn from green leaves before leaf abscission. The formula is: NRE ¼ 100%½ðNgr NsenÞ=Ngr; where Ngr and Nsen are the N concentrations in green and senescent leaves, respectively. NRE is expressed on the basis of leaf mass rather than leaf area or leaf cohorts because the leaves of grass species are relatively small and needle-shaped, making it difficult to determine changes in leaf area or to collect leaf cohorts. Dominance value was calculated as the proportion of canopy biomass of a certain species in the total canopy biomass in the community. Data were analyzed by SPSS version13.0 (SPSS, Chicago, IL). Regression analysis was used to describe the relationships between the variables (Ngr, Nsen, NRE, and Dominance value) and N levels, and two-way ANOVA was used to test for the effects of N levels and species on the variables. Data used in the regression analyses were the means of the variables for each treatment. Results Effects of N addition on N concentration in green leaves As shown in Table 2, both N addition and species had significant effects on the N concentrations in green leaves of the six species (P<0.0001) whereas the effects of their interaction were minor (P=0.4800). Among the three life-forms, semi-shrubs had the highest green leaf N concentrations, and grasses had the lowest, while forbs displayed intermediate N concentrations. Among all the species, M. ruthenica (a N-fixer) had the highest N concentration, while the lowest N concentration occurred in S. krylovii. The values follow the order M. ruthenica > A. frigida > P. acaulis > A. bidentatum > C. squarrosa > S. krylovii. Table 2 Effects of species and N addition and their interaction on N concentrations in green (Ngr) and senescent leaves (Nsen) and on N-resorption efficiency (NRE) of six temperate grassland species Ngr Nsen NRE Source d.f. F P N addition Species N addition× species N addition Species N addition× species N addition Species N addition×species 7 5 35 7 5 35 7 5 35 37.200 51.799 0.998 21.849 90.569 1.967 3.335 41.604 4.012 <0.0001 <0.0001 0.4800 <0.0001 <0.0001 0.0040 0.0020 <0.0001 <0.0001 152 N concentration in green leaves increased asymptotically and significantly with N addition for all species (Fig. 1). The N concentrations in leaves reached a maximum at N levels ranging from 8 to 32 g m−2 year−1 of N application for the different species examined (Fig. 1). Effects of N addition on N concentration in senescent leaves N addition, species and their interaction had significant effects on the N concentration in senescent leaves of the six species (P<0.01, Table 2). In cantrast to the situation in green leaves, concentrations in senescent leaves differed more among species but less among life-forms (Fig. 2). However, semishrubs still held the highest values. Among species, N concentration in senescent leaves in M. ruthenica was highest, while that in S. krylovii leaves was lowest. Altogether, N concentrations in senescent leaves follow the sequence M. ruthenica > A. frigida > P. acaulis > C. squarrosa > A. bidentatum > S. krylovii, generally similar to that for green leaves. The same asymptotic patterns between N concentrations in senescent leaves and N addition were found for the two grasses, the two semi-shrubs and one of the forbs (P. acaulis), with breakpoints appearing at a range between 8 and 32 g m−2 year−1 of N application, while no clear pattern was found in A. bidentatum (Fig. 2). Effects of N addition on N-resorption efficiency N addition species and their interaction had significant effects on the NRE of the six species (P<0.01, Table 2). Among the six species, the two semi-shrubs showed the lowest NRE while the remaining species displayed comparable efficiency. Regression analysis revealed that NRE decreased linearly and significantly with increasing N addition in A. frigida and S. krylovii, whereas no significant changes in the rest four species were detected (Fig. 3). Effects of N addition on species dominance Dominance values of the six species had changed substantially after 3 years of N fertilization (Fig. 4). The response patterns were less species-specific but were more life-form dependent. Two changing pat- Plant Soil (2008) 306:149–158 terns in dominance values of the six species were detected with increasing N addition, namely, (1) values decreased linearly and sharply at lower N addition (between N8 and N32), and changed slightly at higher N addition in the two forbs and the two semi-shrubs; (2) bell-shaped patterns in the two grasses, with an initial increase at lower N addition, followed by a slight decline after the peak value at intermediate N addition levels (between N16 and N32). Discussion Relationships between N availability and N-resorption traits It has been suggested that NRE is similar among habitats but that NRP is higher in N-limited habitats. In the present study, N concentrations, both in green leaves and in senescent leaves, increased with increasing N availability whereas NRE showed a decreasing trend in two species (A. frigida and S. krylovii) and no responses in the remaining species. Our results show that NRP was more sensitive to N addition than NRE, consistent with previous results based on fertilization experiments (Feller et al. 2003; van Heerwaarden et al. 2003a; Vitousek 1998) and natural communities (Rejmankova 2005; Wright and Westoby 2003; Yuan et al. 2005b). These increased N concentrations indicate that N fertilization increased the dependence of N acquirement on soil N pool rather than on leaf N resorption. Increased green leaves N and unchanged or reduced NRE may lead to a decrease in NRP, as reported by Soudzilovskaia et al. (2007). It is worth noting that, to obtain more accurate relations between N-resorption traits and N fertilization experimentally, a multi-level and wide-range N addition gradient is extremely important. For example, in the present study, NRE and NRP values were rather variable and irregular at lower N addition rates (Figs. 2 and 3), but our broad range of N fertilization rates ensured a full view of changes in N-resorption traits. The highest N addition rates in most other studies have been about 10 g N m−2 year−1, thus we speculate that one reason for the varying responses of nutrient resorption to nutrient addition in different experiments could be differences in N addition amounts and ranges. Plant Soil (2008) 306:149–158 153 Fig. 1 Relationships between N concentrations in green leaves of six species and N addition. Data were fitted with piecewise regression (mean ± SE, n=5) A. frigida r 2=0.962, P=0.003 M. ruthenica 2 40 r =0.916, P=0.013 30 20 10 0 S. krylovii 2 40 r =0.942, P=0.006 C. squarrosa r 2=0.959, P=0.003 -1 [Ngr] (mg g ) 30 20 10 0 A. bidentatum r 2=0.960, P=0.011 P. acaulis 2 40 r =0.955, P=0.014 30 20 10 0 0 10 20 30 40 50 60 0 10 -2 20 30 40 50 60 -1 N addition gradients (g m yr ) In the present study, NRE was expressed on the basis of leaf mass, which might bias the estimation of NRE to a certain extent if considerable leaf mass loss occurred due to mass resorption (van Heerwaarden et al. 2003b; Vernescu et al. 2005). As a major mass resorption pathway, reallocation of carbohydrates from canopy to basal tillers and root crowns in grassland species has been well documented (Xu et al. 1995). Substantial increases in the total carbohy- drate content of root crowns and basal tillers from the leaf-mature stage to leaf-senescent period were reported in the two forbs (about 10%) (Xu et al. 1995), and minor increases (below 5%) were observed in the two semi-shrubs and in C. squarrosa (about 2%), whereas a decrease was observed in A. frigida (about 4%) in the same area (Xu and Bai 1994), suggesting that leaf losses due to mass resorption may be relatively large only in the two 154 Plant Soil (2008) 306:149–158 Fig. 2 Relationships between N concentrations in senescent leaves of six species and N addition. Data were fitted by piecewise regression (mean ± SE, n=5) M. ruthenica r 2=0.974, P=0.001 A. frigida r 2=0.981, P=0.001 S. krylovii r 2=0.989, P<0.001 C. squarrosa r 2=0.986, P<0.001 P. acaulis r 2=0.955, P=0.004 A. bidentatum 20 10 0 -1 [Nsen] (mg g ) 20 10 0 20 10 0 0 10 20 30 40 50 60 0 10 -2 20 30 40 50 60 -1 N addition gradients (g m yr ) forbs, which possibly led to an underestimation of their NRE in the study. Soil characteristics changed greatly with the increase in N supply. For example, soil pH decreased from 7.3 in the control plot to 5.8 in the high N addition plot (Table 1), which might also affect NRP. It has been proposed that, in natural habitats, NRP of grasses was negatively correlated to soil pH whereas NRE was independent of soil pH (Yuan et al. 2005b). Life form-specific mechanisms in N resorption N concentrations in senescent leaves were considerably lower than those in green leaves for all species (cf. Figs. 1 and 2), indicating the widespread existence of N resorption as an N-conserving mechanism in the temperate ecosystem of the study area. Our findings show that N concentrations in green leaves were highly dependent on life-form but less species-specific within life-form. Aerts (1996) also Plant Soil (2008) 306:149–158 155 Fig. 3 Relationships between N-resorption efficiency in six species and N addition. Data were fitted by linear regression (mean ± SE, n=5) A. frigida r 2=0.785, P=0.004 M. ruthenica 100 80 60 40 20 0 S. krylovii 100 r 2=0.770, P=0.004 C. squarrosa NRE (%) 80 60 40 20 0 P. acaulis A. bidentatum 100 80 60 40 20 0 0 10 20 30 40 50 60 0 10 -2 20 30 40 50 60 -1 N addition gradients (g m yr ) found that N concentrations in mature leaves of shrubs and forbs were consistently higher than in grasses. However, in his analysis, N concentrations in green leaves within growth-forms were quite speciesspecific. Yuan et al. (2005a) reported similar results. The six plant species in our study displayed high NRE. NRE values for the two forbs were much higher than the average NRE value (about 41.4%), while those for the two grasses were comparable to those reported worldwide (Aerts 1996). N concentration in green leaves reflects the ability of plant species to acquire N. On the other hand, low N concentration in green leaves is considered an efficient mechanism to conserve and utilize N (Carrera et al. 2000). In light of these arguments, it can be concluded that the semishrubs were most capable of acquiring N, and the grasses conserved more N by absorbing less N in leaves, while the forbs adopted both methods in their 156 Plant Soil (2008) 306:149–158 A. frigida M. ruthenica 10 r 2=0.803, P=0.068 r 2=0.937, P=0.007 8 40 6 30 4 20 2 10 0 S. krylovii 100 r 2=0.974, P=0.001 Dominance value (%) 50 0 C. squarrosa r 2=0.670, P=0.180 10 80 8 60 6 40 4 20 2 0 P. acaulis 50 r 2=0.890, P=0.022 Dominance value (%) Fig. 4 Changes in species dominance along the N addition gradient. Data were fitted by piecewise regression (mean ± SE, n=5) 0 A. bidentatum r 2=0.896, P=0.019 50 40 40 30 30 20 20 10 10 0 0 0 10 20 30 40 50 60 0 10 20 30 40 50 60 N addition gradients (g m-2 yr-1) competition for limited N supply from the habitat. There were only small differences in NRE values among life-forms, implying that the grasses contributed more to N conservation via their low N concentrations in green leaves than via N resorption. Effects of N-resorption changes on species composition After 3 years of N fertilization, species composition in the community changed from multi-species-dominant to S. krylovii-dominant. In the control plots, A. frigida, S. krylovii and A. bidentatum co-dominated the community, accounting for 26.6%, 25.8% and 22.6% of the total canopy biomass, respectively. The situation did not change significantly at the lower N addition rates until N4, which is understandable because soil N regimes did not change either (Table 1). Species dominance in the community changed substantially at the higher N addition rates, with grasses (specifically S. krylovii) increasing significantly while other life-forms decreased greatly (Fig. 4). N concen- Plant Soil (2008) 306:149–158 tration in senescent leaves was lowest and NRE was highest for S. krylovii in the control sub-plots, suggesting that S. krylovii is better adapted to the relatively N-poor habitat than the other species. On the other hand, NRE in S. krylovii was most sensitive to changes in soil N regime, which explains its success over other species at a wide range of soil N availability. Our results show that, with increases in soil N availability, plant growth became less dependent on N resorption for the dominant species (i.e., S. krylovii and A. frigida, see Fig. 3), while other nutrients (e.g., P) or resources (e.g., water and light) could become limiting factors for plant growth. Life-forms might have played a very important role in determining the species dominance in the community. Grasses are more favored by their clonal growth-form and high competitiveness for light over forbs and semi-shrubs, which is especially true for S. krylovii over A. frigida in this study. Increased dominance in grass species resulting from long-term fertilization has also been reported in other studies (Press et al. 1998; van Heerwaarden et al. 2003a). Güsewell (2005) explained that this could be attributed to their high resorption proficiency. Additionally, P became limiting due to 3-year N fertilization. Rejmankova (2005) noted that grasses may be more dominant in P-poor habitats. Implications for N cycling in the ecosystem N concentrations in green leaves increased for all species, while NRE decreased for the two mostdominant species (S. krylovii and A. frigida) with increased N fertilization, implying that the community as a whole will absorb more N from the soil and become less N-resorption dependent in the N economy in regions where N supply has increased greatly via N atmospheric deposition due to rapid industrialization and urbanization. N concentrations in senescent leaves increased for most species with increased N fertilization, indicating that litter N content in the community as a whole became higher. Thus, the amount of N returned to the soil via leaf litter production would also increase. The decomposition rate of plant litter is controlled largely by litter quality (N concentration) (Knorr et al. 2005), with N-high litter being more easily decomposed (Quested et al. 2003). It has been reported that increased N availability can exert indirect 157 effects on N cycling via shifts in species composition of vegetation (Cornelissen and Thompson 1997; Shaver and Chapin 1991). Our findings suggest that shifts in species composition will change the N cycling rate to a certain extent in the studied community. As S. krylovii becomes the most dominant species with increased N fertilization, the community will absorb more N from soils. On the other hand, the higher N in canopy litter would speed up decomposition, thus leading to more rapid N returns to soils. All these mechanisms will eventually facilitate N cycling in the plant–soil system. Acknowledgments We thank the staff of Duolun Restoration Ecology Research Station, the Chinese Academy of Sciences (CAS) for providing meteorological data, Mr. G.J. Wang for the maintenance of the field experimental plot. We also thank Stephen Hart for kindly correcting the English language of the manuscript. 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