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Biomass allocation and growth rates in Pinus sylvestris are interactively modified by nitrogen and phosphorus availabilities and by tree size and age Angelika Portsmuth, Ülo Niinemets, Laimi Truus, and Margus Pensa
Abstract: Biomass allocation and growth of Scots pine, Pinus sylvestris L., of various sizes (height 0.03–20 m) and ages (1–151 years) were investigated in two infertile sites (raised bog and sand dunes) to determine relative nitrogen and phosphorus limitations on productivity and their interactions and size-dependent controls. Dry mass weighted average nitrogen (NW) and phosphorus (PW) contents were higher in P. sylvestris in sand dunes than in those in the raised bog, but PW/NW ratios overlapped between the sites. Leaf dry mass ratio (FL) and leaf-area ratio (LAR) increased with NW, and FL increased with PW. The relative growth rate (RG) was more strongly associated with PW than with NW. The net assimilation rate per leaf dry mass (NARM) scaled positively with PW but not with NW, demonstrating that the stronger effect of PW on growth was due to modified biomass allocation and physiology (RG = NARM × FL), while NW affected growth via biomass allocation. Partitioning and growth characteristics were poorly related to the PW/NW ratio. The overall decrease of growth in larger trees resulted from their lower LAR and FL. Increases in size further led to a lower NW but higher PW. We conclude that optimum productivity at a given NW requires a certain minimum PW, not a specific “non-limiting” PW/NW ratio. While nutrients affect growth by changing biomass allocation and physiological activity, size primarily modifies biomass allocation. Résumé : L’allocation de la biomasse et la croissance des tiges de pin sylvestre, Pinus sylvestris (L.) de taille (0,03 à 20 m de hauteur) et d’âge (1 à 151 ans) variés ont été étudiées sur deux stations peu fertiles (tourbière et dunes de sable) de façon à déterminer les effets limitatifs de N et de P sur la productivité, leurs interactions et leurs effets conditionnés par la taille des arbres. Les contenus moyens en N (NW) et en P (PW) des arbres établis sur des dunes de sable étaient supérieurs à ceux de la tourbière, mais les valeurs du rapport PW/NW se chevauchaient entre les stations. Le rapport de masse foliaire (FL) et le rapport de surface foliaire (LAR) augmentaient avec des hausses de NW alors que seul le rapport de masse foliaire augmentait avec les hausses de PW. Le taux de croissance relatif (RG) était plus fortement associé à PW qu’à NW. Le taux net d’assimilation (NARM, sur une base de biomasse) était positivement associé à PW, mais pas à NW, ce qui démontre que l’effet plus marqué de PW sur la croissance était causé par des modifications de l’allocation de la biomasse et de la physiologie (RG = NARM × FL) alors que NW a affecté la croissance par le biais de l’allocation de la biomasse. Les caractéristiques d’allocation et de croissance étaient peu reliées au rapport PW/NW. La diminution de croissance observée chez les plus gros arbres est le résultat de leurs plus petites valeurs de LAR et de FL. Plus la taille des arbres augmentait, plus les valeurs de NW diminuaient, mais plus les valeurs de PW augmentaient. Nous concluons qu’une productivité optimale pour un NW donné requiert une certaine quantité minimale de PW, mais aucune valeur spécifique non limitative du rapport PW/NW. Alors que les nutriments affectent la croissance en modifiant l’allocation de la biomasse et l’activité physiologique, la taille des arbres modifie surtout l’allocation de la biomasse. [Traduit par la Rédaction]
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Introduction Plasticity in biomass allocation and growth rates is an important means by which plants compete along gradients of nutrient availability (Poorter and Garnier 1999; Shipley and Meziane 2002). Nitrogen is often regarded as the primary element limiting biomass production in natural ecosystems, forests, and arable fields (Aerts and Chapin 2000). However,
nitrogen limitations on productivity may frequently interact with a phosphorus shortage (DeLucia et al. 1989; Vitousek et al. 1992; DeLucia and Schlesinger 1995; Niinemets et al. 2001), but the influences of interacting nutrient limitations on plant growth have not been investigated extensively in natural environments. Experiments carried out in controlled environmental conditions have demonstrated that the effects of nitrogen and
Received 6 January 2005. Accepted 4 July 2005. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on 1 November 2005. A. Portsmuth and Ü. Niinemets.1 Department of Plant Physiology, University of Tartu, Riia 23, Tartu 51010, Estonia. L. Truus and M. Pensa. Institute of Botany and Ecology, University of Tartu, Lai 40, Tartu 51010, Estonia. 1
Corresponding author (e-mail:
[email protected]).
Can. J. For. Res. 35: 2346–2359 (2005)
doi: 10.1139/X05-155
© 2005 NRC Canada
Portsmuth et al.
2347 Table 1. Chemical characteristics of the upper soil horizon (0–15 cm) in the studied sites. Raised bog pH(H2O) pH (KCl) Soluble phosphorus (mg·g–1) Total nitrogen (%) Total carbon (%)
Sand dunes
Range
Mean ± SE
Range
Mean ± SE
3.14–3.38 2.46–3.50 0.061–0.136 0.96–1.92 45.6–49.8
3.25±0.03a 2.72±0.13a 0.094±0.10b 1.36±0.09b 47.67±0.43b
4.33–6.00 4.06–5.40 0.032–0.072 0.006–0.024 0.12–0.43
5.07±0.24b 4.64±0.19b 0.051±0.08a 0.018±0.004a 0.34±0.07a
Note: Values followed by the same letter are not significantly different (P > 0.05) according to one-way analyses of variance (ANOVA) (n = 10 for both the raised bog and the sand dunes).
phosphorus on plant growth are only partly additive, and that maximization of plant growth rates requires a balanced supply of both nitrogen and phosphorus (Ingestad 1979, 1981; Whitehead et al. 1997), because growth limitation by one of these nutrients reduces the efficiency of use of the other. The requirement for a balanced nutrient supply has led to the development of the concept of optimal nutrient proportions in plants (Ingestad 1979, 1981; Knecht and Göransson 2004). Certain predefined plant phosphorus/nitrogen ratios are often employed to determine whether nitrogen or phosphorus is the primary limiting element and to identify nitrogen and phosphorus colimitations in the field (e.g., Ingestad 1979; Wassen et al. 1995; Knecht and Göransson 2004). However, the use of any constant phosphorus/nitrogen ratio assumes that the relative minimum levels of phosphorus and nitrogen required for growth (Ågren 1988), as well as plant growth responsiveness to them, are the same for these two nutrients. This is not necessarily the case, given that a larger relative part of total foliar phosphorus than of nitrogen is in nucleic acids that are required for synthesis of proteins, which include most leaf nitrogen. Thus, the relative initial phosphorus requirement for growth may be larger than the relative nitrogen requirement, and the utility of a certain phosphorus/ nitrogen ratio in identifying limiting nutrients may strongly depend on the actual nutrient contents. In addition, “optimal” nutrient proportions determined under controlled conditions may be difficult to transfer to the field, owing to other interacting environmental constraints in natural environments (Poorter and Garnier 1999). Generalization of plant responses to nitrogen and phosphorus in the field is further complicated by large species differences in the requirement for and efficiency of use of nitrogen and phosphorus (Ingestad 1981; Cromer et al. 1993; Ryser et al. 1997). Such differences in plant demand functions and differential growth responsiveness to additions of nitrogen and phosphorus are currently only partly understood, and the overall effect of covarying and interacting nitrogen and phosphorus availabilities has been examined in only a few cases (Cromer et al. 1993; Whitehead et al. 1997). Plant growth depends on net assimilation rate (NAR) as well as biomass partitioning, both of which may be differently controlled by nitrogen and phosphorus availabilities (Cromer et al. 1993; Ryser and Lambers 1995). For instance, some studies have demonstrated that within the limiting range of both nitrogen and phosphorus, foliar-area growth is more strongly controlled by phosphorus availability than by nitrogen availability (e.g., Cromer et al. 1993), but in other studies the opposite has been observed (e.g., Ryser and Lambers 1995). This partly contradictory evidence calls for more experimental
work on natural nutrient-availability gradients to understand species’ responses to changing soil nutrient availabilities. In trees, the effects of nutrient availability on biomass allocation and growth may be further complicated by changes in tree size and age. There is conclusive evidence of a decrease of productivity in older and larger trees (Ryan et al. 1997; Bond 2000; Niinemets 2002), but most research on whole-tree responses to environmental constraints has been conducted with first-year seedlings (for a review see Walters and Reich 1999). Because plant biomass allocation strongly varies with age and size in long-lived trees (Groves et al. 1986; Walters et al. 1993; Bartelink 1998), changes in tree size may modify the responsiveness of biomass allocation and growth to nutrient availability. We investigated biomass partitioning and growth rates in Scots pine, Pinus sylvestris L., of various sizes and ages along nutrient-availability gradients in two sites of contrasting fertility. Pinus sylvestris is a shade-intolerant early-successional species that colonizes habitats that vary in nutrient availability. It may grow in soils with very low nutrient availabilities and is the dominant species in raised bogs and on shore and inland dunes. We tested the hypotheses that (i) plastic changes in whole-plant growth rates and biomass allocation vary along nutrient gradients in dependence on relative nitrogen and phosphorus availabilities, and (ii) plant nitrogen and phosphorus availabilities and requirements change during plant aging, owing to modifications in biomass allocation between tree compartments that differ in nutrient costs. We further hypothesized that the primary source of differences in plasticity in growth rates of plants between and within sites that vary in fertility and among trees of various sizes is the limited biomass allocation to leaves.
Materials and methods Study sites The study was conducted in Estonia between mid-July and early September in 2000. The first site was a raised bog at Männikjärve in Endla State Nature Reserve (58°52′N, 26°15′E). The sparse tree layer (200 trees/ha) was dominated by old (average age 30–100 years) but short (average height 1–2 m) P. sylvestris and Betula pubescens Ehrh. The roots of the woody species mostly occupied the upper peat horizons from 5 to 20 cm and did not reach the mineral soil at 8 m depth in the center of the bog and 3–4 m depth at the edges (Niinemets et al. 2002). The organic, strongly acidic soil is poorly drained and has the high total nitrogen and carbon contents and high carbon/nitrogen and carbon/phosphorus ratios characteristic of organic soils (Table 1). Leaf-level © 2005 NRC Canada
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photosynthesis measurements conducted at the site demonstrate that photosynthesis in P. sylvestris is limited by low leaf contents of both nitrogen and phosphorus (Niinemets et al. 2001), and the results of fertilization experiments further indicate that plant growth is responsive to additions of both nitrogen and phosphorus (Veber 1974; Finér 1992). A detailed description of this site is given in Niinemets et al. (2001, 2002). The second site was a sand-dune habitat in Kalevi-Liiva (59°28′N 25°1′E). The natural vegetation in this site is a sparse P. sylvestris forest. However, a central 14.8-ha area of the forest had been burned on 3 June 1992 and thereafter planted with 1-year-old P. sylvestris seedlings in the autumn of 1992. Thus, most of the trees were 8 years old by the time of the study. The soil is a deep, moderately acidic sand with excessive drainage that essentially lacks the upper humus layer (Table 1). Tree growth in sand-dune heath forests is strongly responsive to both organic and mineral nitrogen and phosphorus fertilizers (Valk and Margus 1958). In both sites, the long-term average precipitation during the growing season (May–September) is 300–350 mm and precipitation is distributed uniformly throughout the growing period (unpublished data from the Estonian Institute of Meteorology and Hydrology (http://www.emhi.ee)). Nevertheless, water may be occasionally limiting both in the sand-dune site because of good drainage and in the raised bog because of drying of the uppermost peat layers containing most of the root systems. Plant-sampling strategy In the raised bog, trees were selected from the central area to the edges. The area surrounding the bog was drained more than 40 years ago. The average height of 30- to 40year-old trees increased from 1–2 m in the center of the bog to 10 m at the drained edges, demonstrating increasing fertility of the edge areas (Niinemets et al. 2001; Niinemets and Lukjanova 2003a). According to numerous experimental studies, draining of ombrotrophic bogs improves tree growth because of the enhanced nutrient availability that results from an increase in the peat mineralization rate (e.g., Hånell 1988; Macdonald and Lieffers 1990; Regina et al. 1998), and the positive effect on growth is inversely proportional to the distance from the drainage ditches (Joamets 1953). In fact, because of low soil microbial activity, gaseous nitrogen losses from virgin bogs are often below the detection limit, while significant gaseous nitrogen losses occur after bog drainage (Regina et al. 1996, 1998). This evidence collectively demonstrates that our sampling scheme yielded a soil-fertility gradient in the bog. In the sand-dune site, the trees were sampled from the middle of the area that burned in 1992 towards the nonburned edges of the site. Again we suggest that soil fertility was greater at the nonburned edges because of thicker humus horizons, and accordingly, larger total nitrogen and phosphorus pools in the soil. Although the ash bed may initially provide somewhat greater nutrient availability in burned areas, the nutrients are quickly leached out because of the low nutrient-retention capacity of sandy soil, which has a clay fraction (diameter fine roots > coarse roots ≥ stem), except for the phosphorus contents of fine and coarse roots in the bog, which were not statistically different according to a pairedsamples t test (P > 0.07; Table 2). The nutrient contents in different plant compartments were significantly correlated (data not shown). The nutrient contents in any single plant compartment were also significantly related to the mass-weighted average contents, but the correlations were always not very strong and the data did not necessarily fit the same lines across the sites (data not shown). Thus, average nutrient contents do not just reflect the nutrient content in a specific plant compartment, but provide an integrated estimate of whole-plant nutrient status. Variation in nutrient contents with whole-plant dry mass and age Total plant dry mass of excavated plants ranged from 0.43 to 1477 g (mean ± SE = 183 ± 70 g) in the raised bog and from 0.31 to 1527 (mean ± SE = 170 ± 70 g) in the sanddune site. Plant age and total mass were strongly correlated (Fig. 1B inset), and the correlations of plant nutrient contents with age and total mass were qualitatively the same. NW was negatively related to tree age (Fig. 1A) and total mass in both sites, while PW was independent of tree age and total mass in the raised bog and scaled positively with © 2005 NRC Canada
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1.2 0.8 0.4
(A)
Leaf nitrogen content (%)
0 1.6
0.8 0.4
(C) 5
10 15 20 25 Plant age (years)
30
4
0.08
0
0.06 0.04 0.02 r 2=0.30, P0.9 r 2=0.00, P>0.7
0
0.12
Log(MT, g)
2
r =0.44, P 0.1) in the raised bog, while decreased with increasing NW (r2 = 0.24, P < 0.02) and increased with increasing PW in the sand dunes (r2 = 0.29, P < 0.02). LMA increased with increasing PW/NW ratio in both sites (r2 = 0.50, P < 0.001, and r2 = 0.19, P < 0.04, respectively). Leaf mass ratio (FL, leaf dry mass per total plant dry mass) was independent of NW in the raised bog but was positively related to NW in the sand-dune site (Fig. 2A). FL was
r 2=0.01, P>0.7
(B)
2
r =0.71, P0.2
0.10 0.08 0.06 0.04 0.02
(D)
0 0
5
10 15 20 25 Plant age (years)
30
35
independent of PW (Fig. 2B) and the PW/NW ratio (Fig. 2C) in both sites. The data from both sites were virtually part of the same general FL versus PW relationship (Fig. 2B), a suggestion that was supported by a strong positive correlation for all data pooled (Fig. 2B). A nonlinear fit to this relationship provided a larger fraction of explained variance (r2 = 0.63) than a linear fit (r2 = 0.53). Leaf allocation (γ, eq. 8), which characterizes the fraction of newly produced biomass in a specific year tended to increase with average nutrient contents within the sites, but these effects were statistically not significant (P > 0.07), partly because of a lower sample size for this variable (see Materials and methods). Nevertheless, γ was positively related to NW (r2 = 0.31, P < 0.01) and PW (r2 = 0.22, P < 0.05) when the data from the two sites were pooled. LAR, which depends on both LMA and FL (LAR = FL/LMA), was positively associated with NW (Fig. 2D) and negatively with the PW/NW ratio (Fig. 2F) only in the sanddune site, and was not associated with average nutrient contents in the other cases (Figs. 2D–2F). Dry mass averaged needle age (Λ, eq. 2) decreased with increasing NW in the sand-dune site (r2 = 0.33, P < 0.01), but within-site relationships were not significant in the other cases. Both the leaf mass ratio, FL (r2 = 0.39, P < 0.001, for the sand dunes and r2 = 0.58, P < 0.001, for all) and LAR (r2 = 0.54, P < 0.001 for all data pooled) decreased with increasing Λ, demonstrating that the increases in leaf longevity in less fertile sites could not offset the overall decrease in © 2005 NRC Canada
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Fig. 2. Leaf mass ratio (leaf to total plant dry mass) and leaf area ratio (total leaf area to total plant dry mass ratio) in relation to whole-plant average dry mass weighted nitrogen (NW; A and D) and phosphorus (PW; B and E) contents and the phosphorus to nitrogen ratio (PW/NW; C and F) in P. sylvestris in the raised bog (䊊) and sand dunes (䊉). In A–F the r2 and P values refer to site-specific linear regressions (the broken lines denote nonsignificant relationships). As the site-specific data in B were virtually part of the same relationship, they were also fitted by a common logarithmic regression (y = a Log(x) + b; r2 = 0.63, P < 0.001). For this dependence (B), the site × PW interaction was not significant (P > 0.7) but the site effect was statistically relevant (P < 0.001) according to ANCOVAs.
Leaf mass ratio (g·g–1)
0.8
0.6
2
r =0.31, P0.4
0.4 0.2
15
(B)
(A)
0
Leaf area ratio (cm2·g–1)
2
r =0.14, P>0.09 2 r =0.00, P>0.5
2
r =0.00, P>0.8 2 r =0.01, P>0.6
2
r =0.43, P0.1
(C) 2
r =0.36, P0.1
2
r =0.06, P>0.2 2 r =0.01, P>0.7
10 5 0
(E)
(D) 0.2 0.4 0.6 0.8 1.0 1.2 1.4 Nitrogen content (%)
0
(F)
0.02 0.04 0.06 0.08 0.10 0 0.02 0.04 0.06 0.08 0.10 0.12 Phosphorus content (%) Phosphorus/nitrogen ratio
annual biomass allocation to foliage with decreasing nutrient availability. Dry-mass investment in stems and roots versus internal nutrient contents Within-site analyses indicated that in the raised bog, the shoot mass ratio (FS) decreased (Fig. 3A) and the root mass ratio (FR) increased (Fig. 3D) with NW. In addition to these site-specific dependencies, the ratio of fine to coarse root mass decreased with increasing PW (Fig. 3H) and the PW/NW ratio (Fig. 3I) in the sand-dune site. Despite the weak withinsite relationships between nutrient contents and the characteristics of standing biomass allocation, FS (Fig. 3B) and FR (Fig. 3E) were strongly correlated with PW when all data were pooled, suggesting that the site-specific correlations were part of common asymptotic relationships. Site effects on leaf structure and biomass allocation According to the ANCOVAs, neither the slope (P > 0.3) nor the intercept (P > 0.07) of the LMA versus NW relationship differed between the sites, but at a common PW, the leaves in the raised bog had a higher LMA (P < 0.005). The site × NW interaction was significant for most biomassallocation characteristics (Figs. 2A, 2D, 3A, and 3D), except for the fine to coarse root mass ratio (P > 0.1; Fig. 3G). The significant interactions implied that in the raised bog, the relative biomass investment in leaf mass (FL; Fig. 2A) and leaf-area construction (LAR; Fig. 2D) responded less plastically to NW, while the standing biomass fractions (Fig. 3A, D) responded more plastically. This was possibly because of overall lower phosphorus availability in the raised bog (Figs. 1B and 1D; Table 2). For the relationships between PW and plant biomass allocation variables, none of the site × PW interactions was sig-
nificant (P > 0.3; Figs. 2B, 2E, 3B, 3E, and 3H). The site effect itself was significant in all cases (P < 0.05). However, the data were essentially non-overlapping, so the intercept differences could not be tested conclusively (Tsutakawa and Hewett 1978). In fact, the data from the two sites tended to fit common saturating relationships with PW (Figs. 2B, 3B, and 3E). The PW/NW ratios overlapped between the sites (Figs. 2C, 2F, 3C, 3F, and 3I), but there was no evidence of a uniform PW/NW ratio versus plant biomass allocation relationship in data from the two sites. Although the PW/NW ratios overlapped, the site effect was always significant for PW/NW ratio versus plant biomass allocation dependencies, indicating that tree biomass allocation was not controlled by the internal PW/NW ratio. Modification of leaf morphology and dry-matter partitioning by tree size Multiple linear regression analyses demonstrated that total plant mass (MT) significantly modified the relationships of leaf morphology and plant biomass allocation with nutrient contents (Table 3). The effects of plant size on leaf morphology and biomass allocation were qualitatively similar in the two sites, so we demonstrate the trends with all data pooled in the following. LMA increased with MT for the multiple regressions with both NW and PW (Table 3). Leaf mass ratio and LAR decreased with increasing MT for the regressions with PW, while FS increased and FR decreased with increasing MT for the regressions with NW (Table 3). However, internal nutrient contents were not wholly independent of tree size and age (Figs. 1A and 1B), possibly explaining the contrasting results of multiple regressions with either NW or PW. Although such effects complicate interpretation of the patterns, analyses of allometric relationships demonstrated that site differences in biomass allocation were maintained across © 2005 NRC Canada
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Shoot mass ratio (g·g–1)
Fig. 3. Relationships of dry mass weighted average nitrogen (NW; A, D, and G) and phosphorus (PW; B, E, and H) contents and the phosphorus to nitrogen ratio (PW/NW; C, F, and I) with shoot dry mass ratio (leaves plus stems per unit total dry mass; A, B, and C), root dry mass ratio (root mass per unit total dry mass; D, E, and F), and the ratio of fine-root mass to coarse-root mass (G, H, and I) in P. sylvestris in the raised bog (䊊) and sand dunes (䊉). The data in E were also fitted by common logarithmic regression lines to further demonstrate the relative changes in shoot and root investments at low phosphorus availability (r2 = 0.43 for B and r2 = 0.41 for E). The ANCOVAs demonstrated that the PW × site interaction was not statistically significant for any of these two correlations (P > 0.4), but the site effect was significant for both (P < 0.005).
1.0
0.8
2
r =0.00, P>0.8 2 r =0.20, P0.2 2 r =0.00, P>0.8
(C)
2 r =0.05, P>0.3 2 r =0.00, P>0.8
0.6
2 r =0.13, P>0.08 2 r =0.08, P>0.1
r 2=0.14, P>0.08 r 2=0.07, P>0.2
0.4 0.2 0
Fine root/coarse root mass ratio (g·g –1)
(B)
2.5 2.0
r 2=0.00, P>0.6 r 2=0.20, P0.08 2 r =0.02, P>0.4
(D)
(E)
(G)
(H)
(F) r 2=0.29, P0.7
2
r =0.45, P0.1
1.5 1.0 0.5
(I)
0
0.2 0.4 0.6 0.8 1.0 1.2 1.4 0 0.02 0.04 0.06 0.08 0.1 0 0.02 0.04 0.06 0.08 0.10 0.12 Phosphorus/nitrogen ratio Nitrogen content (%) Phosphorus content (%) the entire range of plant sizes (e.g., Fig. 4), indicating that site fertility and tree size both strongly affected biomass partitioning. Dependence of growth rates on plant age and nutrient contents In the sand-dune site, RG (eq. 5) was positively associated with both NW (Fig. 5A) and PW (Fig. 5B), while in the raised bog, RG tended to be positively linked only to PW (cf. Figs. 5A and 5B). For all data pooled, RG increased with both NW (r2 = 0.69, P < 0.001) and PW (Fig. 5B), but the correlation was stronger with PW. In addition, ANCOVA demonstrated that at a common NW, the trees in the sanddune site had a larger RG than the trees in the raised bog (P < 0.03), while the slopes and intercepts of the RG versus PW relationship did not differ between the sites, suggesting that these data are part of a general relationship. RG may be expressed as a product of NARA and LAR (eq. 6; Figs. 2D–2F) or as a product of NARM (eq. 7) and FL (Figs. 2A–2C). Neither NARA (Fig. 6A) nor NARM (Fig. 6D) was significantly related to NW, but there was a significant positive correlation between NARM and PW in the sand-dune site (Fig. 6E), and there were strong uniform relationships
with PW for all data pooled (Figs. 6B and 6E). As with the biomass-allocation variables, no general patterns were observed between the PW/NW ratio and RG (Fig. 5C) and net assimilation rates (Figs. 6C and 6F). Similarly to biomass allocation, tree size modified the RG versus PW relationship. Tree size also affected the NARM versus PW relationship but not the NARA versus PW relationship (Table 2), suggesting that the effects of tree size on RG were primarily mediated by size effects on FL and LAR and to a lesser degree by the changes in the dry mass based net assimilation rates (Table 3). To further generalize the patterns, growth-increment cores from 24 larger and older trees were pooled with the data from the excavated trees. For the larger trees, only leaf nitrogen and phosphorus contents, total age, and absolute basal area growth rate (GB) were available. For the extended data set, relative basal area growth rate (RB, cm2·cm–2·year–1) was positively related to both leaf nitrogen (NL, %; r2 = 0.18, P < 0.01) and phosphorus (PL, %; r2 = 0.21, P < 0.005) contents, and negatively to Log(tree age) (r2 = 0.51, P < 0.001). However, NL was not significant (P = 0.16) in the multiple regression analysis with Log(tree age) (r2 = 0.54). In contrast, both PL and Log(tree age) were highly significant determi© 2005 NRC Canada
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Table 3. Modification of biomass allocation and growth characteristics by dry mass weighted average nitrogen (NW) and phosphorus (PW) contents and whole-plant dry mass in Pinus sylvestris. (A) Average nitrogen content. Slope Dependent variable
Intercept
P
Leaf mass per area (g·m–2) Leaf area ratio (cm2·g–1) Leaf mass ratio (g·g–1) Leaf allocation (g·g–1) Root mass ratio (g·g–1) Shoot mass ratio (g·g–1) Shoot mass to root mass ratio (g·g–1) Relative growth rate (g·g–1·year–1) Net assimilation rate per unit area (g·cm–2·year–1) Net assimilation rate per unit dry mass (g·g–1·year–1)
59.5 0.23 –0.059 0.062 0.73 0.34 –0.96 –0.42 –132 –0.75
0.00 0.84 0.37 0.66 0.00 0.00 0.19 0.24 0.04 0.27
Intercept 57.9 0.20 4.11 0.32 0.56 0.47 0.63 0.28 –6.88 0.54
P
NW (%) 3.68 6.74 0.49 0.42 –0.38 0.32 3.38 1.56 271 2.96
P
Log(dry mass, g)
P
r2
0.59 0.00 0.00 0.01 0.00 0.00 0.00 0.00 0.00 0.00
3.83 –0.23 0.0050 0.019 –0.033 0.027 0.26 –0.045 10.3 –0.027
0.00 0.05 0.52 0.29 0.00 0.00 0.00 0.31 0.17 0.75
0.46 0.61 0.58 0.35 0.31 0.24 0.32 0.63 0.56 0.61
P
Log(dry mass, g)
P
r2
0.06 0.00 0.00 0.03 0.00 0.00 0.00 0.00 0.00 0.00
3.58 –0.025 –0.64 0.0020 –0.013 0.01 0.11 –0.10 0.24 –0.13
0.00 0.00 0.00 0.93 0.11 0.16 0.10 0.00 0.96 0.01
0.45 0.68 0.63 0.22 0.40 0.41 0.42 0.82 0.75 0.85
(B) Average phosphorus content. Slope Dependent variable –2
Leaf mass per area (g·m ) Leaf mass ratio (g·g–1) Leaf area ratio (cm2·g–1) Leaf allocation (g·g–1) Root mass ratio (g·g–1) Shoot mass ratio (g·g–1) Shoot mass to root mass ratio (g·g–1) Relative growth rate (g·g–1·year–1) Net assimilation rate per unit leaf area (g·cm–2·year–1) Net assimilation rate per unit dry mass (g·g–1·year–1)
0.00 0.00 0.00 0.01 0.00 0.00 0.08 0.08 0.81 0.06
PW (%) 131 5.17 61.8 2.57 –4.21 3.86 33.3 14.5 2442 27.8
Note: Leaf allocation was calculated from eq. 8, relative growth rate from eq. 4, net assimilation rate per unit leaf area from eq. 6, and net assimilation rate per unit dry mass from eq. 7. The data from the two sites were pooled. Whole-plant dry mass was log-normally distributed and therefore Log10transformed to improve normality. Values in boldface type are statistically significantly different from zero at least at P < 0.05.
Log(leaf dry mass, g)
Fig. 4. Correlation between total plant leaf and stem dry mass in P. sylvestris in the raised bog (䊊) and sand dunes (䊉). The data were fitted by linear regression.
8
2
r =0.97, P 0.6) nor the intercepts (P > 0.6) differed significantly between the sites.
2.0
r 2=0.31, P>0.06 r 2=0.27, P>0.1
r 2=0.36, P0.8
1.5
2
r =0.03, P>0.6 2 r =0.12, P>0.3
1.0 0.5 0.2 0.4 0.6 0.8 1.0 1.2 1.4 Nitrogen content (%)
(C)
(B)
(A)
0
0
0.02 0.04 0.06 0.08 0.1 Phosphorus content (%)
0 0.02 0.04 0.06 0.08 0.10 0.12 Phosphorus/nitrogen ratio
Net assimilation rate per leaf mass (g·g-1·year-1)
Net assimilation rate per foliar area (g·cm -2 ·year -1)
Fig. 6. Net assimilation rate per unit leaf area (eq. 6; A, B, and C) and dry mass (eq. 7; D, E, and F) in dependence on average nitrogen (A and D) and phosphorus (B and E) contents and the phosphorus to nitrogen ratio (PW/NW; C and F) in P. sylvestris in the raised bog (䊊) and sand dunes (䊉). The data were fitted by linear regression. Broken lines denote nonsignificant regressions. Because neither the slopes nor the intercepts differed between the sites in B and E (P > 0.1), the data were fitted by common regression lines (r2 = 0.75 for B and r2 = 0.79 for E, P < 0.001 for both).
300
2
2
r =0.28, P>0.07 2 r =0.26, P>0.1
r =0.09, P>0.3 r 2=0.01, P>0.8
2 r =0.13, P>0.2 2 r =0.23, P>0.1
200 100 0 3.5
(A) 2 r =0.24, P>0.1 2 r =0.01, P>0.8
2 r =0.41, P0.2
2.5
(C)
(B) 2
r =0.13, P>0.2 2 r =0.10, P>0.3
1.5 0.5 0
(E)
(D) 0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 0 Nitrogen content (%)
(F)
0.02 0.04 0.06 0.08 0.10 0 0.02 0.04 0.06 0.08 0.10 0.12 Phosphorus content (%) Phosphorus/nitrogen ratio
It may be disputed that apart from the nutrients, other environmental factors may explain the site differences in fertility. In nutrient-limited bogs, the survival of P. sylvestris seedlings may strongly depend on the groundwater level (Gunnarsson and Rydin 1998), while in heath forests, survival is altered by low soil water-holding capacity and plant vulnerability to biogenic stresses (Raitio 1990). Nevertheless, as fertilization experiments demonstrate, low nitrogen and phosphorus availabilities appear to control productivity to the greatest extent (Hånell 1988; Raitio 1990). Tree age and size versus internal plant nutrient contents The correlation of plant internal nitrogen and phosphorus contents with tree age and total mass (Fig. 1) demonstrates that whole-plant nutrient availability interacts with tree growth and development in a complex manner. According to previous studies, tree age itself does not necessarily affect foliar nitro-
gen content in temperate-zone conifers (Niinemets 2002), as was also observed in our study (Fig. 1C). Thus, the decrease in dry mass weighted nitrogen content with tree age and total mass (Fig. 1A) reflects accumulation of stem and coarseroot biomass, which has lower nitrogen costs than accumulation of leaf and fine-root biomass. In contrast, both average phosphorus (Fig. 1B) and leaf phosphorus (Fig. 1D) contents increased with tree age and total mass. A similar increase of leaf phosphorus status with tree size has been previously reported for a pooled sample of temperate-zone trees (Niinemets and Kull 2003), and may reflect enhanced phosphorusabsorption capacity in older and larger trees, which possess more extensive root systems than smaller and younger plants. Increasing the nutrient-absorbing surface increases the uptake of less mobile ions such as phosphate particularly strongly, but has less influence on the uptake of more mobile ions such as nitrate (Aerts and Chapin 2000). Because the nitrogen © 2005 NRC Canada
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Can. J. For. Res. Vol. 35, 2005
Fig. 7. Stem basal area growth rate in dependence on tree age and needle nitrogen content (A) and on tree age and needle phosphorus content (B) in P. sylvestris in the raised bog (䊊) and sand dunes (䊉). The data from both sites were fitted by common regression planes. The stem basal area growth rate was calculated from measurements of tree-ring widths. The highest growth rates in the raised bog correspond to edge trees growing in drained peat. The ages of sampled trees ranged from 1 to 151 years and heights from 0.03 to 20 m (n = 37 for the raised bog and n = 15 for the sand dunes).
Basal area growth rate (cm 2·year -1)
10
r 2=0.22, 8 P
