Plant and Soil (2005) 278:183–193 DOI 10.1007/s11104-005-8195-8
Springer 2005
Foliar nitrogen dynamics and nitrogen resorption of a sandy shrub Salix gordejevii in northern China Zhi-You Yuan1, Ling-Hao Li1,2, Xing-Guo Han1,2, Jian-Hui Huang1 & Shi-Qiang Wan1 1
Key Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, People’s Republic of China. 2Corresponding author* Received 18 January 2005. Accepted in revised form 31 May 2005
Key words: Nitrogen, resorption efficiency, resorption proficiency, Salix gordejevii, senescence, soil nitrogen
Abstract Resorption of nitrogen (N) from senescing leaves is an important conservation mechanism that allows plants to use the same N repeatedly. Seasonal variations in leaf nitrogen of mature green and senescing leaves and N resorption in Salix gordejevii Chang, a sandy shrub in northern China, were studied. Our objective was to compare N resorption of this Salix species that successfully occupy different habitats (shifting sandland, fixed sandland and lowland) with differences in soil N availability and moisture. Nitrogen concentrations in green and senescing leaves were higher in June and July. N resorption efficiency (percentage reduction of N between green and senescing leaves) was highest at shifting sandland, intermediate at fixed sandland, and lowest at lowland. There was a clear seasonal variation in N-resorption efficiency, with a lower value at the early growing season and a higher value during summer. N resorption efficiency was lower at the sites with higher soil N availability, suggesting that the efficiency of the resorption process is determined by the availability of the nutrient in the soil. Resorption from senescing leaves may play an important role in the nitrogen dynamics of sandy plants and reduce the nitrogen requirements for plant growth. We conclude that N resorption from senescing leaves in S. gordejevii was correlated to soil characteristics and higher N resorption on poor soils is a phenotypic adjustment by this species to maximize N-use at low availability.
Introduction Nitrogen (N) may be mobilized from senescing leaves and translocated to other plant tissues (N Aresorption) (Killingbeck, 1996), enabling plants to conserve and reuse this nutrient. N resorption has an important role in the plant N economy (Eckstein et al., 1999; Oleksyn et al., 2003; Richardson et al., 2005). It has been suggested that N-resorption efficiency (percentage reduction in the N concentration between green * FAX No: +86-10-6259-0833. E-mails:
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and senescing tissues) will decrease with increasing soil N availability and that plants adapted to infertile conditions will decrease N loss by higher efficiency of resorption (see review by Aerts and Chapin, 2000). However, this hypothesis remains controversial and it has been either supported (Pugnaire and Chapin, 1993; Enoki and Kawaguchi, 1999) or disputed (Chapin and Moilanen, 1991; del Arco et al., 1991). Aerts (1996) claims that there are no clear nutritional controls on nutrient-resorption efficiency. In the light of the absence of clear evidence for genotypic differences in resorption efficiency in response to N availability, Killingbeck (1996) argued that the
184 absolute level to which nitrogen is reduced in senescing tissues (resorption proficiency) appears to be a more definitive and objective measure to estimate the degree to which selection has acted to minimize N loss. N-resorption responses to soil N availability have been investigated extensively, but few studies have considered the seasonal change in resorption efficiency. It is generally assumed that N resorption takes place in autumn as the foliage senesces in response to low temperature or short daylength. Salix gordejevii Chang, a widely distributed deciduous species in northern China, continues to produce new leaves with high N content and shed old leaves with low N content during entire growing season. There might be a seasonal variation in resorption efficiency. In the Hunshandake Sandland, which is located in the northern part of China, this species appears in three types of habitats: shifting sandland, fixed sandland and lowland. It may play a potentially important role in releasing N and impacting soil N availability. But to our knowledge, the N resorption of this sandy shrub in different habitats has not been studied. Further, debate whether or not resorption efficiency increases as an adaptation to low N availability is continuing. Evidence has accumulated that there may be adaptive changes in N-resorption efficiency, but we do still not understand when and how this occurs. In the present study, the seasonal variations in leaf nitrogen of green and senescing leaves and the N-resorption efficiency of Salixgordejevii in northern China were investigated. We intended to address the question of whether this Salix species, adapted to different soil conditions, differs in its N-resorption efficiency and proficiency. The present study also addressed the intraspecific responses of N resorption in this sandy shrub to differences in N availability. The present work also addressed the role of high N-resorption efficiency as an adaptation to N-poor sites. Considering the difference in three habitats, it could be expected that there would be similar resorption efficiency in different habitats, but higher resorption proficiency in infertile habitat. Nitrogen was selected because this nutrient represents the main growth-limiting nutrient for plants in natural environments (Chapin, 1980; Vitousek and Howarth, 1991).
Material and methods Study site and species This study was carried out in Duolun (4227¢ N, 11641¢ E, 1380 m a.s.l), a semiarid area located in the central part of Inner Mongolia Autonomous Region, China. The Duolun Restoration Ecology Research Station for Agri-pastoral Ecosystems (DRERSAE), situated approximately 2.5 km northwest of the study site, recorded an average annual precipitation of 401.3 min and an average air temperature of 3.3 C between 1994 and 2003. The seasonal variations of precipitation and temperature in the study area in 2003 were given in Figure 1. In 2003, we chose three typical kinds of habitats (i.e., shifting sandland, fixed sandland and lowland) within a small range (ca. 500 m by ca. 500 m). The studied habitats are part of a nature reserve to which access is restricted. Within the three habitats, we set up the sampling plots (20 · 20 m) in shifting sandland, fixed sandland and lowland, respectively. The three sampling plots were so close to each other that they shared highly similar climate conditions (e.g., precipitation, air
Figure 1. Monthly precipitation (a) and air temperatures (b) in 2003.
185 temperature and radiation) and the same soil type (i.e., loamy sand). Salix gordejevii Chang, the selected species in our study, is the dominant plants species distributed at the three habitats. This deciduous shrub is common in the semiarid area of northern China (Liu et al., 2004). It tends to grow so densely that it can cover the sandy dunes completely. It started to expand leaves in mid-May and completed leaf abscission in Mid-November. Since this Salix species continues to produce new leaves and shed old leaves throughout the whole growing season, the youngest fully expanded leaves and senescing leaves were compared during the whole growing season. This species can cope with severe shortages of nutrients and water or with an excess of soil moisture. It survives in the shifting sand dunes as pioneer species because of its high aridity tolerance. The Salix shrubs vary in phenotype as they occupy a wide range of habitats: shrubs growing at infertile sites are rather small and exhibit low growth rates, while at fertile sites they are large and fast growing (Liang et al., 2000). Plant sampling and nitrogen analysis Plant samples were taken at nine different sampling dates during the growth period. On each sampling date, three quadrat samples (1 · 1 m) were chosen randomly from each site. We collected green leaves and senescing leaves in each quadrat. The green leaves were collected from a similar position (i.e., the youngest fully expanded leaves) because new leaves had more N than old leaves (data not shown). 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 are easily identified as they are generally a different colour from live leaves (often yellow), and can be removed by a gentle flicking of the branch or leaf, leaves without an abscission layer are not removed by this technique. Senescing leaves were collected directly from plants rather than from leaf litter, as we concerned that decomposition of leaf litter and leaching of leaf N would lead to underestimates of N concentration in senescing leaves. The leaf area of green and senescing leaves was
measured with a LI-COR portable area meter, model LI 3000. Plant samples were oven-dried at 60 C for 48 h, weighed and ground to a fine powder. The total N concentration was determined using an NC analyzer (KDY-9820, Tongrun Ltd, China) after standard Kjeldahl acid-digestion. Estimates of proportional N resorption made on a leaf area basis may be more accurate than estimates made on a leaf mass basis (van Heerwaarden et al. 2003; Vernescu et al. 2005). Accordingly, N-resorption efficiency (NRE) was calculated as nitrogen mass per unit of leaf area (grams per square meter) of green (Ng) and senescing (Ns) leaves: NRE=[(Ng)Ns)/Ng] · 100, where Ng was N concentration in the youngest fully green leaves and Ns was N concentration in the senescing leaves from the similar position on the shoot. N concentration in senescing leaves is considered a direct indicator of N-resorption proficiency, which is defined as the absolute level to which N is reduced in senescing leaves (Killingbeck, 1996). Consequently, plants with a lower N concentration in freshly fallen leaves are more proficient than plants with a higher concentration in senescing leaves. Soil sampling To estimate soil conditions, three soil samples were taken at each sampling site from a depth of 0–20 cm. Soil samples were taken on the same nine sampling dates as plant samples. One soil subsample was analyzed for gravimetric water moisture by drying at 105 C for 24 h. One soil subsample was air-dried, sieved to 0.5 mm and analyzed for total nitrogen concentration (Kjeldahl). The rest of soil was brought to the laboratory within 2 h of collection and analyzed for inorganic nitrogen (NHþ 4 –N and NO3 –N) by using the steam distillation technique in an autoanalyzer (Segmented Flow Analyzer, the Scalar SANplus, Scalar, Breda, the Netherlands) after extraction with 2 M KCl.
Statistical analyses A split-plot analysis of variance was used to analyze the data using SPSS version 11.0 (SPSS Inc.,
186 Chicago, IL, USA). Habitat was the main-plot factor with leaf status (whether green or senescing) or sampling date as the split-plot factor. Main effects and interactions were tested for significance using the appropriate error terms as determined by the expected mean square. Multiple comparisons among pairs of means were performed using the T-method (Tukey’s honestly significant difference method) when a significant ANOVA result occurred. Data were logarithmically transformed when necessary to comply with the assumptions of ANOVA.
Results The three sites had clear seasonal patterns of leaf senescence (Figure 2). Most leaves senesced during autumn (late-September–October). Some leaves began to shed prior to autumn senescence. At the shifting sandland, senescence happened much earlier than at the other sites. The sandy shrub Salix gordejevii at three habitats differed in their seasonal changes in foliar N concentration (Figure 3). At fixed sandland, N concentration in green leaves was higher in the early growing season and decreased thereafter. At shifting sandland and lowland, however, N concentration in green leaves tended to be
constant until the end of September. The patterns of seasonal variation of N concentration in senescing leaves were similar among three habitats. N concentration in senescing leaves was highest in the early growing season and decreased gradually during summer at all habitats, reaching the lowest N concentration in late-August. During autumn, N concentration in senescing leaves increased steadily. N concentrations per mass and per area differed significantly among habitats and between leaves of different status (whether green or senescing) (Table 1). The N concentration in green leaves was significantly (P
