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Keywords:

  • leaching resistance;
  • nitrogen;
  • nutrient resorption;
  • organ senescence;
  • phosphorus;
  • plant economics;
  • root;
  • shoot

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • Nutrient resorption and leaching resistance, through their roles in reducing nutrient losses, are important determinants of plant nutrient economy. However, the contributions of fine-stem and fine-root resorption, as well as leaf leaching resistance, have largely been overlooked.
  • We quantified the relative contributions of these processes to nutrient depletion of these organs during their senescence using 40 subarctic vascular species from aquatic, riparian and terrestrial environments. We hypothesized that interspecific variation in organ nutrient resorption and leaf leaching would be linked to the species’ nutrient acquisitive-conservative strategies, as quantified for a set of common-organ nutrient/carbon economics traits.
  • The subarctic flora generally had both high resistance to leaching and high internal nutrient recycling. Average nutrient resorption efficiencies were substantial for leaves (nitrogen (N), 66 ± 3% SE; phosphorus (P), 63 ± 4%), fine stems (N, 48 ± 4%; P, 56 ± 4%) and fine roots (N, 27 ± 7%; P, 57 ± 6%). The link between nutrient resorption and other nutrient/carbon economics traits was very weak across species, for all three organs.
  • These results emphasize the potential importance of resorption processes for the plant nutrient budget. They also highlight the idiosyncrasies of the relationship between resorption processes and plant economics, which is potentially influenced by several plant physiological and structural adaptations to environmental factors other than nutrient stress.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

One of the overarching goals of plant ecology is to understand the mechanisms by which plants are adapted to their environment. To grow and persist under regimes of nutrient limitation, plants have developed two main strategies: optimizing nutrient acquisition and reducing nutrient losses. These adaptations are part of a well-known trade-off in and among plants between resource acquisition and conservation (Grime, 1979; Berendse & Aerts, 1987; Aerts, 1990; Reich et al., 1997; Wright et al., 2004). Adaptations that minimize nutrient loss, such as protection against leaching, effective nutrient resorption from senescing plant organs, and high nutrient use efficiency through long lifespans of leaves (Escudero et al., 1992; Reich et al., 1992) or other organs, are thus usually considered to be opposed to adaptations promoting nutrient uptake and growth (Chapin, 1980; Aerts & Chapin, 2000). These aspects of plant nutrient conservation are of predominant importance in nutrient-poor environments (Aerts, 1999).

The nutrient resorption process potentially occurs all year round, especially in evergreens, but is most pronounced during periods of organ senescence leading to plant dormancy such as winter in cold climates, and concerns all senescing plant parts (e.g. Aerts & de Caluwe, 1989; Gordon & Jackson, 2000). It is a dynamic, highly regulated process involving exchanges of nutrients and metabolites from organ to organ (Killingbeck, 1986; Aerts, 1996). The senescence and resorption processes of roots and stems are far less understood than those of leaves. The absence of abscission zones and the less pronounced seasonality of root and stem mortality imply critical differences in the mechanisms involved. Factors driving this process range from growth of new plant parts (new buds and reproductive organs; e.g. Simpson et al., 1983; Milla et al., 2005) or remobilization from underperforming organs (such as excessively shaded leaves; Saur et al., 2000) to self-induced organ senescence (such as autumn senescence of deciduous leaves). The resorption process can involve active (e.g. photosynthetic) processes and stored components, neither of which necessarily involve organ death. However, when interested in how efficiently plants reduce nutrient loss, one should focus on resorption mechanisms associated with organ senescence, for which autumn is the crucial period at higher latitudes.

Leaf nutrient resorption, from the molecular to the whole-plant level, has been remarkably well studied in the past four decades. By contrast, very few root studies and almost no stem studies have been conducted over the same period. The fate of nutrients contained in fine roots, characterized by high turnover rates and high nutrient contents (Gill & Jackson, 2000; Gordon & Jackson, 2000), and in fine stems, especially photosynthetic ones, is of great importance for the whole-plant nutrient budget. However, the question of whether and to what extent nutrients are resorbed from fine stems and fine roots has not been clearly answered. While resorption has been observed for fine roots of annuals (Simpson et al., 1983), perennial grasses (Woodmansee et al., 1981) and woody perennials (Meier et al., 1985), most studies noted no or few changes in nutrient content between live and dead roots (e.g. McClaugherty et al., 1982; Nambiar, 1987; Aerts, 1990). More recently, a meta-analysis by Gordon & Jackson (2000) suggested that roots may be not only a sink but also a source of nutrients for resorption processes. While some evidence exists for resorption of nutrients from stems of single annual species (Simpson et al., 1983; Aerts & de Caluwe, 1989), there is a clear lack of studies that might reveal patterns across multiple species with different growth forms. Renewed effort in this direction is crucial for understanding the carbon (C) and nutrient economy at the whole-plant level, for both terrestrial and aquatic species.

Leaf leaching is the passive removal of substances from leaves by the action of aqueous solutions, such as rain, dew, fog or surface water; this process occurs mostly during the latest phase of leaf maturation and during leaf senescence (Tukey, 1966, 1970; Morton, 1977). Resorption and leaching take place simultaneously during leaf senescence and concern most of the nutrients involved in plant metabolism (e.g. Tukey et al., 1958; Nambiar & Fife, 1991), although nitrogen (N) and phosphorus (P), as the main limiting nutrients to plant growth in most environments, have been the subject of most studies. Because of the generally high nutrient content of leaves as compared with other plant organs, foliar resorption efficiency and leaching resistance are of major importance in plant nutrient use strategy. On average, c. 50% of the maximum N and P content of mature leaves is retained in the plant through the resorption process (Reich et al., 1995; Aerts, 1996; Killingbeck, 1996), and this percentage is substantially increased after correction for the changing mass of senescing leaves (van Heerwaarden et al., 2003). Large amounts of organic metabolites can potentially be leached from plants (Morgan & Tukey, 1964). However, most studies have assumed that resorption is the only significant mechanism responsible for nutrient content changes between mature and senesced leaves.

Resorption and leaching resistance mechanisms, through their role in reducing nutrient losses, are potentially part of the nutrient and C acquisition–conservation trade-off among species. Some evidence exists that resorption efficiency and leaching resistance decrease with increasing leaf nutrient content (e.g. Pastor et al., 1987; Kobe et al., 2005). Nevertheless, it is still unclear whether and to what extent these mechanisms co-vary with other well-known nutrient and C economy traits such as specific leaf area or leaf dry matter content; that is, whether they fit into the ‘leaf economics spectrum’ (cf. Wright et al., 2004).

The aims of this study were: to determine the relative importance of the effects of resorption and leaching on leaf nutrient losses during leaf senescence; to compare the cross-species range of resorption efficiencies occurring in leaves, fine roots and fine stems; to test the hypothesis that resorption efficiency and leaching resistance can be predicted from a combination of other easily measurable plant traits relevant to nutrient and C acquisition-conservation. We addressed these issues in a subarctic flora representing the key species from aquatic, riparian and terrestrial environments and covering the main vascular higher taxa and growth forms in this region.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Study area and species types

The study was carried out around the Abisko Research Station, North Sweden (68°21′N, 18°49′E) at 350–400 m asl, below the treeline. The last 10 yr (1999–2008) had a mean annual rainfall of 352 mm and mean January and July temperatures of −9.7°C and 12.3°C, respectively (Abisko Research Station meteorological station, Sweden). The forested area, which covers most of the landscape below 700–800 m asl except for occasional swamps and peatlands, was the focus of this study. The three most distinct ecosystem types within the chosen forested site were dry birch (Betula pubescens) forest, riparian birch forest and forested freshwater systems (ponds and streams). The soils below birch forest are Podsols (Sjögersten & Wookey, 2002). Seven sampling sites (c. 20 m transects) each hosting all three ecosystem types were used to identify the dominant species (c. 80–90% of total vascular plant biomass) of each ecosystem (see Cornelissen et al., 2003). Sampling the most dominant species allowed us to obtain a representative estimate of the C and nutrient dynamics of the investigated ecosystems. These included 15 species from the dry forest, 18 from the riparian forest and seven from aquatic systems. When present in two or more ecosystem types, species were sampled only from the ecosystem where they occurred most abundantly. Within each ecosystem type, species were collected only from the sampling site where they were the most abundant. Species nomenclature follows Mossberg et al. (1992). The seven plant types and six clades identified were rather evenly distributed across environments (see Supporting Information Table S1 for the species list and characteristics).

Sampling

Species were sampled for mature living and recently dead leaves, fine stems (< 3 mm diameter) and fine roots (< 2 mm diameter). To ensure a fair comparison of root types, in terms of structure and function, only the finest root branch order of each species was considered and pioneer roots were avoided. In total, 40 species were sampled for leaves, 38 for stems and, because of logistical constraints, 11 for fine roots. Leaves, stems and roots were not sampled from the same individuals. A minimum of 10 different plant individuals (up to 50 for some species) were used for each species and material to ensure the representativeness of the pool collected. For each organ, part of the collected material was placed in a paper bag and air-dried for chemical analyses while the other part was immediately placed in a closed plastic bag for the purpose of dry matter content (DMC) and specific leaf area (SLA) analysis (see Cornelissen et al., 2003 for more details). For the sampling of recently dead woody stems, uncertainty regarding the time since death was minimized by selecting stems showing strictly no visual differences with living stems except for the absence of leaves or buds. For root sampling, plant individuals were excavated and brought to the laboratory with earth still attached. Soil and alien material were washed off the root system before living, undamaged roots and recently dead roots were collected. Large mycorrhizal rhizomorphs were brushed off the roots. Recently dead roots were selected according to visual and textural criteria. All selected species presented a progressive darkening and loss of turgescence of their fine-root tissues during senescence. To decrease uncertainties regarding the (complete or incomplete) death of root tissues, they were considered recently dead in the late stages of darkening and turgescence loss only; that is, before complete death. Thus, both roots in the first stages of senescence (first symptoms of browning and of turgescence loss) and completely dead roots (all-dark tissues and absence of turgescence) were avoided. For all organs, material presenting obvious symptoms of damage, infection or herbivore activity was avoided. Petioles and rachides were included as part of the leaf.

To avoid effects of seasonal variation, all living leaves were collected while fully mature and before the onset of senescence (see Quested et al., 2003), that is, between 28 July and 3 August 2008. Accordingly, mature living stems were all sampled between 4 and 10 August 2008. Senesced (mostly shed) leaves and recently dead stems were collected from mid-August to mid-October 2007, following natural senescence of each deciduous or evergreen leaf species. Perennial fine stems were collected as recently dead as possible during the same period. Mature living and recently dead roots were collected in August 2007. A subsample of dead leaves and stems was collected again from mid-August to mid-October 2008 to test for inter-annual changes in chemical composition (two-samples paired t-test). None of the traits used for resorption calculations, that is, N, P and lignin contents, showed significant differences between 2007 and 2008.

Nutrient resorption measurements

All collected materials were measured for C, N, P and lignin content, for which air-dried subsamples were ground and subsequently oven-dried for 24 h at 60°C. C and N concentrations were measured by dry combustion on an NA 1500 elemental analyser (Carlo Erba, Rodana, Italy). P was measured by acid digestion as described in Dorrepaal et al. (2005). The lignin concentration was determined by extraction of nonligneous compounds as described in Dorrepaal et al. (2005).

The resorption proficiency (RP) was defined as the extent to which the nutrient content was reduced in dead material, that is, the litter nutrient content (mg g−1), with low litter nutrient content corresponding to high proficiency and vice versa (Killingbeck, 1996). Litter nutrient content was corrected for fractional change in the measurement basis (FCMB) using lignin content as a reference value (van Heerwaarden et al., 2003), that is, it was multiplied by the ratio of litter lignin content to mature material lignin content. The substantial mass loss occurring during senescence can differ among species and lead to both underestimation of mass-based nutrient RP and unfair species comparison (van Heerwaarden, 2004). Nutrient resorption efficiency (RE (%)) was calculated as the ratio of the difference in nutrient content between mature material and litter (corrected for FCMB) to mature material nutrient content. A sensitivity analysis of the RE calculations revealed that a x% error in litter N and P measurements induced changes in organ RE of y (%) = – x(RE/100). This relationship indicates that the error in RE is always lower than the potential litter nutrient content error. Resorption efficiency measurements were therefore relatively robust to uncertainty about the stage of litter senescence/death. The negative linear relationship found between RE and the sensitivity of RE calculations also indicates that high values of RE were less sensitive to measurement errors in litter nutrient content than low RE values.

Plant trait measurements

All mature living and recently dead leaf, fine-stem and fine-root material used in the nutrient resorption experiment were measured for pH, DMC and (for leaves) SLA. For pH determination, used here as a proxy for total cation content (Cornelissen et al., 2006), 0.15 ml of each ground sample was shaken with 1.2 ml of demineralized water in an Eppendorf tube for 1 h at 250 rpm. After centrifugation at 9 000 g for 5 min, the pH of the supernatant solution was measured. Dry matter content (dry weight (mg)/water-saturated weight (g)) measurements followed Cornelissen et al. (2003), except for woody stems, which were submersed in water for 3 d in order to ensure homogeneous filling of air spaces. SLA (m2)/leaf dry mass (kg) measurements followed Cornelissen et al. (2003).

Leaf nutrient leaching

To quantify the impact of nutrient leaching processes occurring during leaf senescence, an experiment to investigate potential leaf leaching was combined with an in situ leaf leaching experiment on a representative subset of species. For our potential leaching experiment, mature living leaf material was collected between 28 July and 3 August 2008 and recently dead leaf material (both deciduous and evergreen) from mid-August to mid-October 2008, following natural leaf senescence. All leaf species were collected from a minimum of 10 different individual plants, sealed in plastic bags and processed within 3 h. Leaves were introduced gently into plastic pots, immersed in 30 ml of demineralized water and mechanically shaken at 200 rpm for 6 h. Leaves were subsequently oven-dried (60°C for 48 h) and weighed. Resulting water samples were filtered (Whatman glass microfibre filters; GFC 1822-025) to remove undissolved detached particles and dust. Concentrations of C and N in the solutions were determined using a total organic carbon analyzer (TOC-VCPN, Shimadzu, Kyoto, Japan). To determine P concentrations, 1 ml of sample was digested in 1 ml of a 1 : 4 mixture of 37% (v/v) HCl and 65% (v/v) HNO3 in a closed Teflon cylinder for 6 h at 140°C. Samples were then diluted with 3 ml of demineralized water and the total P concentration was quantified by spectrophotometry, using the ammonium molybdate method (Murphy & Riley, 1962). C, N and P losses by leaching were calculated by multiplying their concentration by the solution volume. Potential leaching (%) was calculated as the mass percentage of C, N and P leached per total C, N and P of the material considered.

In the in situ leaching experiment, 25 × 35 cm transparent plastic shelters (UV-transmitting) were used to protect leaves from rain. A subset of nine species – five woody deciduous, two forbs, one grass and one pteridophyte – were selected and four distinct individual plants were sheltered per species. Shelters were installed on 5 August 2008, when leaves were fully mature, and removed after the last species shed its leaves on 28 September. The amount of precipitation during that period was 56 mm, that is, less than the 10-yr average of 79 mm calculated over the same period. Poles were used to fix shelters above the small stature plants and to prevent tree branches from moving out of the protected area. Leaves were kept away from the shelters by loose wire cables when needed. The amount of light diverted by the shelters was assumed to be negligible. Similarly, the shelters, due to their small size and their relatively large distance from the ground, presumably did not reduce rain water supply to the plant root systems. A minimum of 20 leaves were sampled at the start of the experiment (on adjacent individual plants or branches) and at the end, when plants were ready to shed their leaves, both outside and under the protected area. All samples were air-dried for 24 h at 60°C and ground, and subsamples were analyzed for N and P content by dry combustion on an NA 1500 elemental analyser (Carlo Erba, Rodana, Italy). In situ leaching (%) was calculated from the difference between sheltered and unsheltered senesced leaf nutrient contents divided by mature leaf nutrient content.

Data analysis

Repeated measure ANOVAs were used to determine the significance of nutrient content differences among mature leaves, litter of sheltered plants and litter of unsheltered plants, across nine species with four replicates each. In order to compare nutrient resorption efficiencies and proficiencies across plant organs, paired t-tests were run between each pair of organs, after log-transforming part of the data. A Bonferroni correction was applied to the resulting P-value. Pearson’s correlations (or Spearman’s test when normality assumptions could not be met) tested for consistency of species nutrient resorption efficiencies and proficiencies across organs. The predictive values of all measured organ traits in terms of their respective organ RE and litter nutrient content (and leaf resistance to leaching for leaves) were tested using linear regressions, part of the data having been previously log-transformed.

In order to obtain a proxy for the resource economics of each plant organ, principal component analyses (PCAs) were performed on a suite of established economics traits (C, N, P and lignin contents, pH and DMC; additionally SLA for the PCA on leaf traits) for leaf, stem and root data sets, respectively. The first axis of each PCA has been shown to produce an adequate proxy for the leaf, stem and root economics, respectively (see Freschet et al., 2010 for more details). The predictive value of the different plant organ economics (as defined by their respective PCA first axis species scores), in terms of their respective organ nutrient resorption efficiencies and litter nutrient contents (and resistance to leaching for leaves only), was tested using linear regressions.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

The relative importance of leaf nutrient resorption and leaf leaching during senescence

In the in situ leaching experiment, the overall mature leaf N and P contents of the nine selected species were significantly higher than their shed leaf N and P contents, respectively, for both sheltered and unsheltered plants (< 0.001 in all cases). The average REs for these nine species were 70.3 ± 1.5% (SE) for N and 50.3 ± 2.7% (SE) for P. The overall difference in the P content of shed leaves between sheltered and unsheltered plants was not significant (= 0.35), while the difference in N content suggested a tendency towards lower N retention under shelters (= 0.09).

In the 40 species, the average nutrient loss occurring during an intensive phase of leaching (6 h at high shaking intensity) accounted for only 0.1% and 1.2% of total leaf N and < 0.001% and < 0.006% of total leaf P, for mature and shedding leaf species, respectively (Table 1). Compared with the average RE for N (REN) of 66.0 ± 3.1% (SE) and the RE for P (REP) of 63.4 ± 3.5% (SE) for the same 40 species (Table 1; Fig. 1), which are, respectively, 55-fold and > 104-fold higher than N and P potential leaching losses, nutrient leaching losses from leaves were generally negligible compared with resorption losses. The average leaf litter N and P contents of the 40 species were 6.7 and 0.7 mg g−1, respectively (Fig. 1).

Table 1.   Influence of resorption and leaching on nutrient disappearance during leaf senescence
 Resorption efficiency (%) (= 40)In situ leaf leaching (%) (= 9)Potential leaching (%)
Mature leaves (= 40)Shed leaves (= 40)
  1. Percentages are related to the initial leaf nutrient pools. n, number of species taken into account. Mean values are given ± SE. *Values for in situ leaf leaching are not significantly different from zero.

Nitrogen66.0 ± 3.1−2.4 ± 1.5*0.1 ± 0.051.2 ± 0.2
Phosphorus63.4 ± 3.5−4.7 ± 3.1*< 0.0002< 0.006
image

Figure 1.  Leaf nutrient resorption efficiency and proficiency, as compared with literature references. Grey lines, average values for the complete species set. Dotted lines represent the world-wide average resorption indices: *, average nutrient resorption efficiencies were taken from Aerts (1996) and corrected according to van Heerwaarden et al. (2003); nutrient resorption proficiency categories (†, complete; #, intermediate; ‡, incomplete) were derived from Killingbeck (1996) by applying the average correction factor (for mass loss during senescence) of our total data set to Killingbeck's thresholds.

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Resorption efficiencies and proficiencies compared across organs

Resorption efficiency and proficiency differed significantly among organs for both N and P. We found that leaf REN (66 ± 3.1% SE) was significantly higher than stem REN (< 0.001), the latter still being substantial (48 ± 3.5% SE; Fig. 2a). Stem REN in turn was higher than root REN (27 ± 6.8% SE; = 0.03). Leaf REP (63 ± 3.5% SE) was not significantly higher than stem REP (56 ± 3.6% SE; = 0.14) but was significantly higher than root REP (57 ± 5.6% SE; = 0.03), while stem and root REP were not significantly different (= 1). RP values for N were significantly higher in stems than in leaves (< 0.001) or roots (< 0.01) (Fig. 2b). Stem RP values for P (RPP) were significantly higher than leaf RPP values (< 0.001).

image

Figure 2.  Across-organ comparison of (a) nutrient resorption efficiency and (b) proficiency. Open bars, leaves; grey bars, stems; closed bars, roots. Values are means + SE. Significant differences (indicated by different letters a, b and c) for paired t-tests are shown.

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Across-organ correlations in nutrient resorption were weak or absent (Table S2). The only significant correlations were found between leaves and stems for RPN (= 0.59; < 0.001) and RPP (= 0.42; < 0.01).

Predictions of organ resorption and leaf leaching from plant functional traits

Among the suite of plant traits measured (C, N, P and lignin content, SLA, DMC and pH of both mature and senesced organs), none was significantly related to REN and REP (senesced organ N and P were excluded for reasons of autocorrelation). Mature leaf, stem and root N were the only significant (only marginally significant in the case of roots) predictors of leaf, stem and root RPN, respectively (Fig. 3). Mature leaf P was the only significant predictor of leaf RPP. No significant predictors were found for stem and root RPP.

image

Figure 3.  Predictions of litter nutrient contents from mature organ nutrient contents. Open circles, leaves; grey circles, stems; closed circles, roots. Goodness-of-fit (R2) and significance of linear regression predictions (P) are displayed to the right of each graph.

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Leaf C and N potential leaching of both mature and senesced leaves were either not significantly predicted or poorly predicted by either chemical (N and P contents, and pH) or structural (SLA, DMC, and C and lignin contents) leaf traits (Table S3).

Organ nutrient resorption, leaf leaching and plant resource economics

The link between plant organ resource economics and organ resorption was inconsistent across organs, nutrients and resorption indices (Fig. 4). Leaf and root economics were unable to predict leaf or root nutrient RE (R2≤ 0.04 for both N and P). By contrast, stem economics was closely related to stem nutrient RE (R2 = 0.37 and 0.19 for N and P, respectively; both < 0.05). Leaf, stem and root economics could not predict leaf, stem and root RP, respectively (R2≤ 0.05 for both N and P;  0.53 in all cases), except for the prediction of leaf RPN by leaf economics (R2 = 0.30; < 0.001).

image

Figure 4.  Predictions of organ nutrient resorption efficiencies and proficiencies from the respective organ nutrient and carbon (C) economics, as represented by first axis species scores of principal component analyses (PCAs) on organ nutrient and C economics traits (dry matter content (DMC), C, nitrogen (N), phosphorus (P) and lignin content, and pH for all three organs; plus specific leaf area (SLA) for leaves). The regression line, goodness-of-fit and P-value of the linear regression predictions are displayed when significant.

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Predictions of the resistance to N leaching of mature and senesced leaves by leaf resource economics were significant (< 0.05) although relatively weak (R2 = 0.10 and 0.17, respectively; Fig. S1). Senesced leaf resistance to C leaching was significantly predicted by leaf economics (R2 = 0.13; < 0.05), while mature leaf resistance to C leaching was not (R2 = 0.03; = 0.34). Given the generally negligible impact of leaching in our study, these relations are only discussed briefly in Fig. S1.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Resorption, not leaching, is the main contributor to leaf nutrient pool depletion during senescence

Both our in situ and potential leaf leaching experiments unequivocally showed a negligible influence of leaching on the nutrient status of leaves during senescence, as compared with the leaf resorption process (Table 1). The large coverage of this study in terms of plant types, clades and environments supports the representativeness of our results for infertile subarctic areas in general. The correlation between leaching resistance and the economic strategy of leaf species (Fig. S1) suggests the hypothesis that the impact of leaching is greater in more productive biomes, which are dominated by nutrient-acquisitive species. The underlying causes of this strong leaching resistance may differ according to the environment. For terrestrial environments, this resistance is likely to be a by-product of leaf traits that provide protection against herbivores, frost or desiccation or more generally an adaptation to poor soil nutrient availability. By contrast, for riparian and aquatic plants, which experience prolonged or permanent close contact with water, protection against leaching obviously has strong selective value.

Leaf nutrient resorption is particularly high in subarctic ecosystems

Killingbeck (1996) qualified resorption as complete, intermediate or incomplete based on established litter nutrient contents for woody perennial species. Here, this index was corrected to account for changes in mass loss during leaf senescence using the mature to shed leaf lignin ratio averaged over our total leaf set. According to this corrected index, N and P RP values were intermediate or complete for most of our species (Fig. 1). Most species also displayed higher N and P RE values than the average values found by Aerts (1996) and more recently by Yuan & Chen (2009), which we corrected beforehand for mass loss according to van Heerwaarden et al. (2003). In (sub)arctic environments, characterized by slow nutrient cycling and poor organic matter quality (Shaver & Chapin, 1980; Vitousek & Howarth, 1991), most species therefore seem well adapted to nutrient stress through high internal N and P recycling.

Fine-stem and fine-root nutrient resorption is substantial

In the present work, root N and P RE values were much higher than the values reported in earlier studies (e.g. Nambiar, 1987; Aerts, 1990; Nambiar & Fife, 1991; Aerts et al., 1992). This difference can be explained in part by methodological differences, as the former studies either artificially induced root death (Aerts et al., 1992) or did not correct for mass loss during root senescence. Our findings therefore support the idea that fine roots of both woody and nonwoody perennials resorb substantial proportions of nutrients (e.g. Woodmansee et al., 1981; Meier et al., 1985). Because of some uncertainties in assessing the exact stage of root senescence, early decomposition (nutrient leaching and microbial colonization) of the root material has to be considered as a potential bias in our study. These uncertainties may also partly explain the larger interspecific variability in RE found for roots than for leaves. Indeed, a sensitivity analysis conducted on RE calculations showed that the smaller the actual RE, the more sensitive the values were to litter nutrient content measurement errors. Also, considering that (arbuscular, ecto- and ericoid) mycorrhizal fungi constitute a large part of the fine-root volume of most plants – up to 40% for ectomycorrhizas and 80% for ericoid mycorrhizas according to Chapin et al. (2002)– root nutrient resorption cannot be measured confidently without a better understanding of root–fungal interactions during root senescence. To our knowledge, it is still unknown whether mycorrhizal fungi take advantage of the dying root as a source of nutrient and carbohydrates or retreat from the dying root, thus retranslocating part of their own resources from the root towards the mycelia. The substantial resorption observed from senescing roots might thus partly be attributable to the root–fungal interaction.

While living stems of perennials are considered as major sinks for nutrients resorbed from leaves (Chapin & Kedrowski, 1983; Nambiar & Fife, 1991), or nutrient sources during vegetative or reproductive growth events (Milla et al., 2005), they have been overlooked as potential sources of nutrients during their senescence, with the exception of Aerts & de Caluwe (1989), who reported N and P resorption efficiencies of 77% and 91%, respectively, for culms of the grass Molinia caerulea. We demonstrate here that both woody and nonwoody perennial stems, with either photosynthetic or essentially supportive function, display substantial RE values. Because of relatively high RE values, stems were only marginally sensitive to some uncertainty in their exact stage of senescence.

Our results show substantially higher RE in leaves than in stems and roots, while the analysis of RP indicates more complete resorption in stems than in leaves or roots. In other words, the absolute amount of nutrient resorbed is higher for leaves than for stems or roots but the extent to which the nutrient concentration is reduced in the litter is lower for stems than for leaves or roots. This is partly attributable to the higher nutrient content of live leaves and roots as compared with stems and probably to the higher fraction of hydrolysable compounds (mainly proteins) in leaves as compared with stems or roots. However, a proper understanding of the mechanisms underlying nutrient resorption from stems and roots is lacking, in contrast to the situation for leaves (Nambiar & Fife, 1991). Plant growth in the ecosystems under study is probably N-limited, as indicated by their average leaf N:P ratios of < 14 (average N:P ratios of 9, 12 and 12 for terrestric, riparian and aquatic ecosystems, respectively) (Koerselman & Meuleman, 1996). The uniformly high REP found across all organs, as compared with the more variable REN (with low resorption notably occurring in roots), therefore suggests that RE is not closely related to nutrient availability. However, it is not clear whether this trend can be generalized to other ecosystems and the underlying mechanisms involved are unknown.

What is the relative impact of stem and root nutrient resorption on the plant nutrient budget?

Assessing the consequences of these findings for the plant nutrient budget is difficult. To do so, one should take into account the relative biomass:nutrient allocation of plants to each organ as well as the specific turnover rates of these organs. This information is lacking for the species we studied. Nevertheless, we hypothesize here that the contribution of fine-stem and fine-root resorption to the recycling of plant nutrients is not as important as the leaf resorption contribution for the whole-plant budget. This is because leaves generally have higher nutrient concentrations and higher turnover rates. The generally fast turnover of first-order roots (Gill & Jackson, 2000; Guo et al., 2008), irrespective of the plant type, might be largely counterbalanced by their generally lower nutrient content than leaves, by the lower resorption rates measured in roots than in leaves, and probably by a lower biomass allocation to fine roots than to leaves. Similarly, the generally lower nutrient content of both woody and nonwoody fine stems compared with leaves, their lower RE and the slow turnover of woody stems make it unlikely that stem resorption contributes equally to the plant nutrient budget compared with leaves. Taken together, the findings suggest that the amounts of nutrients recycled from stems and roots, albeit likely to be important to the whole-plant nutrient budget, are probably lower than those from leaves.

Translocation of these nutrients within the plant is better understood. Indeed, the simultaneous nutrient resorption from leaves, fine stems and fine roots raises the question of where these nutrients are translocated to. First, high proportions of these nutrients are used to form buds and reproductive organs (Chapin & Kedrowski, 1983; Simpson et al., 1983; Chapin & Moilanen, 1991). Coarse roots and rhizomes of perennial species may also act as sinks (Lambers et al., 1998) and, in woody species, perennial stems have also been shown to store a large amount of nutrients (e.g. Chapin & Kedrowski, 1983; Aerts & de Caluwe, 1989).

Why the trade-off between the nutrient resorption process and current plant economic strategy schemes does not hold

A striking result of this study is the relative independence of resorption processes from other plant strategic adaptations – such as DMC, representative of organ lifespan and plant growth rate (Cornelissen et al., 1996; Ryser, 1996; Wright & Cannon, 2001), SLA, related to photosynthetic N use efficiency (Poorter & Evans, 1998), or pH, a proxy for cation content (Cornelissen et al., 2006; Freschet et al., 2010). Apart from the tight link between living and dead organ nutrient content (Fig. 3), no other economic traits covered in our study showed a clear relationship with resorption. Nevertheless, using a well-studied proxy for plant organ economics (e.g. Grime et al., 1997; Díaz et al., 2004; Freschet et al., 2010), we found some significant relationships between leaf economics and RPN and between stem economics and stem REN and REP (Fig. 4). In other words, the more nutrient-acquisitive the species, the less proficient the leaf resorption and the more efficient the stem resorption. This opposite trend for leaves and stems is surprising, as the resorption process is crucial in plant economy and was expected to be a consistent contributor to the nutrient acquisition–conservation trade-off. The most striking result, however, is the general weakness of the relations found between organ nutrient resorption processes and organ economics. The strong N resorption efficiencies and proficiencies found across all plant types and clades tend to indicate that most species are potentially able to resorb substantially, from the most nutrient-conservative to the most nutrient-acquisitive species. This result concurs with that of the world-wide analysis by Aerts (1996), who found no significant differences in RE between deciduous and evergreen species. Our findings also support the idea that interspecific differences in lifespan might have a stronger impact on nutrient use efficiency than differences in RE (cf. Escudero et al., 1992). However, our results do not reflect the large differences between deciduous and evergreen litter nutrient contents found by Aerts (1996), which suggested a possible link between leaf resorption and other economic strategies. We also hypothesize that the differential capacity of species to minimize environmental stresses impeding the resorption processes during senescence may be partly responsible for that trend. For instance, ‘nutrient-conservative’ species benefit from a better resistance to frost, which has been shown to inhibit the resorption process (see Norby et al., 2000). By contrast, ‘nutrient-acquisitive’ species are better able to ensure sufficient light exposure to complete the final stages of resorption (see Chapin & Moilanen, 1991; Hoch et al., 2001). Similarly, nutrient resorption of acquisitive species is facilitated by a high plant water uptake capacity (Minoletti & Boerner, 1994). Finally, resorption might be constrained by plant vascular capacity, with the more ‘acquisitive’ species having higher phloem loading or transport capacity (S. I. Lang, J. H. C. Cornelissen, R. S. P. van Logtestijn, W. Schweikert, T. Klahn, J. van Hal and R. Aerts, unpublished). Taken together, these examples stress the complexity of the interactions between the resorption process and multiple diverging plant physiological and chemical parameters. The close link between these physiological and chemical parameters and plant resource economics potentially counterbalances or camouflages any potential trend existing between organ resorption and organ economics.

Conclusion

The broad scope of this work in terms of environments, plant types and clades allows us to answer several questions concerning the nutrient resorption process with regard to the (sub)arctic flora. While nutrient leaching might be of importance in more productive biomes, it is negligible at higher latitudes. The (sub)arctic flora is well adapted to its nutrient-poor environment through efficient leaching protection and, more importantly, high internal nutrient recycling. Our results show higher nutrient resorption rates from leaves, stems and roots than previously reported in the literature. The influence of nutrient resorption on the whole-plant nutrient budget might thus be substantially greater than previously thought. Finally, we demonstrate across 40 species that a very weak connection exists between the resorption process and other important aspects of plant nutrient and C economy. Two factors may explain this very weak link. First, nutrient resorption is of tremendous importance in plant economics, irrespective of the position on the phylogenetic tree and irrespective of the environment. Second, resorption processes are influenced in many, often counteracting ways by multiple physiological factors related to organ C and nutrient economics, each with their own adaptive value in evolutionary selection.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We are grateful to the Abisko Scientific Research Station, Sweden (ANS) and its staff for their hospitality and for providing helpful meteorological data. Michael Makarov generously provided assistance with leachate analyses. Emilie Kichenin helped with the sorting of roots. Bob Douma provided help with the sensitivity analysis. We would also like to thank anonymous reviewers for their constructive comments on the manuscript. G.T.F. was supported by EU Marie Curie host fellowship grant MEST-CT-2005-MULTIARC 021143; R.A. and R.S.P.L. by EU ATANS grant Fp6 506004; and J.H.C.C. by grants 047.017.010 and 047.018.003 from the Netherlands Organisation for Scientific Research (NWO).

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  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Fig. S1 Relationships between leaf carbon (C) and nitrogen (N) potential leaching and the leaf nutrient and carbon economics.

Table S1 Species list, organ resorption efficiency and litter nutrient content

Table S2 Consistency of within-species nutrient resorption efficiency across plant parts

Table S3 Predictions of leaf carbon (C) and nitrogen (N) potential leaching from leaf structural traits

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