Forms of soil phosphorus affected by stand development of mountain beech (Nothofagus) forests in New Zealand

Geoderma 157 (2010) 228–234

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Geoderma j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g e o d e r m a

Forms of soil phosphorus affected by stand development of mountain beech (Nothofagus) forests in New Zealand P.-O. Brandtberg a,⁎, M.R. Davis a, P.W. Clinton a, L.M., Condron b, R.B. Allen c a b c

Scion, P.O. Box 29-237, Fendalton, Christchurch, New Zealand Agriculture and Life Sciences, P.O. Box 84, Lincoln University, Lincoln 7647, New Zealand Landcare Research, P.O. Box 40, Lincoln, New Zealand

a r t i c l e

i n f o

Article history: Received 9 July 2009 Received in revised form 24 March 2010 Accepted 26 April 2010 Keywords: Catastrophic disturbance Coarse woody debris Forest floor Hedley phosphorus fractionation Stand development

a b s t r a c t The biogeochemical stability of soil P is often assumed to be related to its solubility but there are few tests of this assumption. We determined differences in forms of soil P among stages of stand development in a replicated (N = 3) age sequence of Nothofagus stands developed after catastrophic disturbance by windthrow in New Zealand. Seedling, sapling, pole, and mature stages used were approximately 10, 25, 120 and N 150 years old, respectively. We hypothesized that insoluble soil P forms would not differ among stages of stand development. Organic forms of soil P depended significantly on stage of stand development. Concentrations of labile (NaHCO3 extractable) and non-labile (NaOH extractable) organic P were significantly greater in the mature stage than in sapling and pole stages. The concentration of occluded organic P (NaOH extractable following extraction with acid) was significantly lower in the seedling and pole stages than in the other stages. The concentration of inorganic P did not depend on stage of stand development except in the case of mineral P (HCl extractable) where the seedling stands had significantly lower concentrations of mineral P than the other stages. This was probably due to different topographical conditions for the seedling stands as compared to the other stands which may have affected long term soil processes such as weathering and leaching. The return of P in litterfall was similar among stages. The storage of P in stemwood was low in the seedling and sapling stages but high in the pole and mature stages whereas the storage of P in coarse woody debris was high in the seedling and sapling stages but low in the pole and mature stages. The storage of P in the forest floor was significantly higher in the pole stage than in the other stages which all had similar amounts of P in the forest floor. The differences in soil organic P forms among stages of stand development could be explained by above ground processes such as accumulation of P in stemwood and release of P from the forest floor and decomposing CWD. Labile and non-labile pools of soil organic P were correlated with the concentration of organic C whereas occluded organic P was unrelated to organic C. Our results suggest that neither labile, non-labile nor occluded organic P is stable during stand development. © 2010 Elsevier B.V. All rights reserved.

1. Introduction The Hedley fractionation (Hedley et al., 1982) or similar fractionation schemes, for example Tiessen and Moir (1993), are often used to recognize plant-available and refractory forms of soil inorganic and organic P based on solubility in alkaline and acid extractants applied in a sequential extraction (Cross and Schlesinger, 1995). However, there are few tests of the assumption that insolubility equals biogeochemical stability. Most early studies on the effect of stand development upon soil P typically considered only soluble forms of P (NaHCO3 extractable) and neglected more insoluble forms (Polglase et al., 1992). In a recent long term study of plantation pine forest growth on an acid

⁎ Corresponding author. E-mail address: [email protected] (P.-O. Brandtberg). 0016-7061/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2010.04.022

Ultisol previously used for cotton growth, Richter et al. (2006) found that accumulation of P in the biomass and forest floor was associated with major changes in non-labile inorganic and organic P (NaOH extractable) as well as in acid extractable P. Labile P, on the other hand, was unaffected by stand development or even increased (inorganic labile P) in deeper soil layers. It is not known, however, if insoluble forms of soil P are affected by biological processes during stand development in natural forests. In contrast to tree plantations which may have received fertilizer input of P, natural forests often have low external input of P (Chadwick et al., 1999). Thus, in natural forests P is expected to be mainly redistributed between ecosystem components (stemwood, CWD, forest floor and soil) during stand development but little is known about the corresponding changes in forms of soil P. In New Zealand, mountain beech (Nothofagus solandri var. cliffortioides (Hook. F.) Poole) forms monospecific stands at high altitudes on relatively

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poor soils low in total P (Wardle, 1984). The forests are disturbed by wind, snowfall and earthquakes, although forest fires are relatively rare (Wardle, 1984; Allen et al., 1999). Large amounts of coarse woody debris (CWD) are left on the forest floor after disturbance by wind and a considerable amount of the ecosystem pool of nutrients may initially be present in CWD but are released in later stages of stand development through decomposition (Allen et al., 1997; Clinton et al., 2002). We used the mountain beech stand development stages examined by Allen et al. (1997) and Clinton et al. (2002) to determine how soil P forms depended on changes in the distribution of P in biomass, CWD and forest floor during forest development. Firstly, we tested the chronosequence assumption that soil properties in a particular stand mainly depend on stage of stand development rather than site variation. In our case, total P in the ecosystem (topsoil b2 mm, forest floor, biomass and CWD) would then be fairly constant among plots and not depend on stage of stand development assuming negligible amounts of P leached and deposited. Our central hypothesis was that insoluble forms of soil P would not be affected by stand development (Cross and Schlesinger, 1995; Johnson et al., 2003). We also examined how soil P forms were related to variations in the concentration of organic C across stages of stand development and thus whether any effect of stand development on soil P forms depended on changes in soil organic matter content. 2. Methods 2.1. Study site Monospecific stands of mountain beech were selected at varying stages of development, namely seedling (10 years old), sapling (25 years old), pole (120 years old) and mature stages (N150 years old) situated in the Craigieburn Range (43 15′S, 171 35′E), central South Island, New Zealand. The stand-initiating disturbances are approximately dated. Each stage is represented by three stands. The 12 stands are dispersed across the landscape such that the seedling and sapling stands were grouped (ca. 100 m across) within an area that contains the pole stands (ca. 300 m across), whereas the mature stands were more widely dispersed up to 3 km from the younger stages. The stands are on broad side slopes at 1064–1208 m elevation, 98–128° aspect, and 10–35° slope. At 914 m elevation mean annual temperature is 8.0 °C, mean annual precipitation is 1447 mm, and mean annual radiation is 4745 MJ/m2 (McCracken, 1980). Soils are derived from greywacke, loess and colluvium and have litter (L) and fermentation–humus (FH) layers over an A horizon of approximately 5– 20 cm of silt loam. The stony B horizon of 50–60 cm resides over a shallow C horizon (approx. 10 cm) (Clinton et al., 2002). Microtopography results from toppling of trees (Allen et al., 1997). Mineral soils (A horizon) have high concentrations of exchangeable Al and low base saturation, 278 mmolc kg−1 and 2.8%, respectively (Davis, 1990; Matzner and Davis, 1996). On these soils mountain beech often develops a shallow root distribution (Clinton et al., 2002). Mountain beech forests in Craigieburn are undisturbed by human activity. A more comprehensive description of the study site and methods is given in Allen et al. (1997) and Clinton et al. (2002). The study was initiated in 1991. One sample plot was installed in each of the 12 stands to determine standing stem wood and CWD biomass and to collect forest floor and soil samples. Plots used to sample seedling and sapling stages were 10 x 10 m, while plots of 20 × 20 m were used to sample the pole and mature stages (Clinton et al., 2002). 2.2. P in stem wood and CWD Trees were measured in 1991. On each plot, the diameter at breast height (DBH, 1.4 m height) of all stems N25 mm was measured and stemwood biomass estimated (Clinton et al., 2002). Stemwood P

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concentration was determined in April 2007 by sampling stemwood cores (pole and mature stages) or stemwood discs (sapling stage) from trees close to the plots (each stage, N = 3). The diameter of the sampled trees was close to the average diameter of the plot. Subsamples were digested in HNO3–H2O2 followed by determination of P by inductively coupled plasma atomic emission spectroscopy. The pool of stemwood P was calculated for each stand using live stem biomass and the stemwood P concentrations. For each plot, the largeand small-end diameter and the length of all pieces of CWD (largeend diameter N100 mm) were measured. Because of difficult access, small-end diameter and height were estimated for each standing dead spar. These dimensions were also measured (or estimated) for each individual dead branch. Volume was calculated using Smalian's formula (Goulding, 1986). Decaying wood was stratified into one of three decay classes: (I) wood hard but not stained, visible rings, bark intact; (II) wood hard but stained, rings indistinguishable, bark sloughed off; and (III) advanced wood decay with loss of original form, wood friable (Allen et al., 1997). On each plot, within each decay class, a wedge of CWD, including bark when present, was extracted from three pieces of debris. Wedges were cut to the centre of individual pieces of CWD using a chainsaw. Volume, by water displacement, and oven dry mass (70 °C) were used to calculate the density of each wedge sample (Allen et al., 1997). Samples for each decay class, on each plot, were finely ground and P concentration was determined colorimetrically in H2O2–H2SO4 digests using an autoanalyser. The mean P concentration obtained for each decay class and CWD mass, by decay class, were used to calculate the CWD pool of P for each plot. 2.3. P in litterfall Litterfall in each plot was collected every two months for 1 year (July 1991–June 1992) using two (1 m2) nylon nets in each plot to estimate canopy (N1.4 m height) inputs of P. Samples were separated into leaf litter and twigs which were bulked separately for each plot, and subsamples were taken for P analysis. Marked seedlings within each stand were harvested and used to estimate annual dry matter and P inputs from leaf production (equivalent to leaf litterfall) from seedlings b1.4 m height (see Allen et al., 1997). Litter samples and seedling leaf production samples were oven-dried at 70 °C and ground with a Wiley mill to pass through a 1-mm mesh. Duplicate 300-mg subsamples were digested in H2O2–H2SO4 mixture. Total P concentration was determined colorimetrically using an autoanalyser. Litterfall (twig and leaf) production for a 1-year period was calculated by combining data from litter traps (N1.4 m height) and leaf production estimates for seedlings (b1.4 m height) (Allen et al., 1997). 2.4. C and P in forest floor and soil Forest floor and soil samples were collected in March 1991 from six randomly selected points in each plot. At each point, a soil pit 300 × 300 mm was sampled in three horizons: forest floor L (including woody material less than 100 mm diameter) and FH layers (the latter included both live and dead roots) and the upper 100 mm of mineral soil. Prior to processing, samples were kept at 3 °C. The L layer samples were oven-dried at 70 °C. The FH layer and upper mineral soil samples were passed through a 6-mm sieve to remove coarse roots or large woody fragments, and then sub-sampled. The FH layer and mineral soil subsamples were then air-dried and the FH layers were later oven-dried at 70 °C and ground with a Wiley mill to pass through a 1mm mesh. Mineral soil subsamples were passed through a 2-mm sieve and finely ground (150 μm). The concentration of organic matter in mineral soil subsamples was determined by loss on ignition (Davis et al., 2003). The concentration of total P in the forest floor was determined colorimetrically using H2O2–H2SO4 digests of ground subsamples of the L and FH layers, whereas the concentration of total

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P in the mineral soil was determined colorimetrically after nitric acid/ perchloric acid (HNO3/HClO4) digestion of soil subsamples. The mass of P in the forest floor and upper 100 mm of the mineral soil was calculated using the forest floor mass or oven-dried mass of fines (b2 mm) extracted from soil pits of known volume. All data are presented on an oven dry basis. 2.5. Soil P fractions Soil P fractionation was carried out in 2004 using air-dry samples that had been stored under dry conditions since sampling in 1991. The procedure described by Condron et al. (1996) was used in this study. The first steps in this procedure distinguish ‘labile’ P (0.5 M NaHCO3 extractable), ‘non-labile’ P (0.1 M NaOH extractable) and ‘mineral bound’ P (1 M HCl extractable). Some procedures use extraction with concentrated HCl as the next step (Richter et al., 2006) which also extract an unknown amount of organic P (He et al., 2006). In order to quantify organic P that becomes soluble by extraction with 1 M HCl (which is expected to remove aluminium and iron) we used a second extraction with 0.1 M NaOH to obtain ‘occluded’ P (see for example Walker and Syers, 1976). This fraction corresponds to a part of residual P obtained in some variants of the fractionation scheme (cf. Lagerström et al., 2009). We determined total P by digestion and ‘residual’ P as a difference between total P and the sum of extracted P (labile, non-labile, mineral bound and occluded P). It should be noted that residual P obtained in this scheme may still contain organic P (Walker and Syers, 1976). Six subsamples (1.0 g) of mineral soil from each plot were extracted sequentially with 30 ml each of 1 M ammonium chloride (NH4Cl), which was discarded and not analysed since it contains only a small fraction of labile P (Chen et al., 2003), 0.5 M sodium bicarbonate (NaHCO3), 0.1 M sodium hydroxide (NaOH), 1 M hydrochloric acid (HCl) and 0.1 M sodium hydroxide (NaOH). In each extract, the concentration of inorganic P was determined in a subsample after precipitation of organic matter by addition of sulphuric acid. The concentration of total extracted P was determined in another subsample after persulfate (K2S2O8) oxidation. Organic P was determined by subtracting concentrations of inorganic P from concentrations of total extracted P. Whereas determination of total P in the forest floor and mineral soil and the mineral soil fractionation procedure were performed on each of the individual subsamples (n = 6) from each plot, averages per plot were used in the statistical calculations.

Fig. 1. Ecosystem pools of phosphorus in four stages of stand development of mountain beech at Craigieburn. Error bars show standard deviation (N = 3). Stages of stand development assigned the same letter did not differ significantly at balphaN = 0.05.

and mineral bound P (HCl extractable) were lower in the seedling stage when compared to the other stages (Table 2).

3.2. P in stemwood and CWD Stemwood P concentrations showed large variability within stages of stand development and ranged from 0.007% (pole stage) to 0.046% (mature stage) but did not differ significantly among stages. The amount of stemwood P and stemwood biomass were significantly lower in the seedling and sapling stages than in the pole and mature stages (Fig. 1, Table 3). The amount of P in CWD and mass of CWD were significantly greater in the seedling and sapling stages compared to that in the pole and mature stages (Fig. 1, Table 3). The average density of CWD decreased by decay class, whereas the concentration of P showed a minimum in decay class II (C/P ratio maximum). The N/P ratio was lowest in decay class I whereas it did not differ much between decay classes II and III (Table 4).

Table 1 Concentration of phosphorus in forest floor L and FH layer and upper soil (0–0.1 m), concentration of carbon (C) in the FH layer and soil and carbon to phosphorus (C/P) element ratio (w/w) in the FH layer and soil. Standard deviations are shown within parentheses.

2.6. Statistical analysis of data The effect of stand development on the ecosystem pools of P and total ecosystem P among the four stages of stand development (i.e. seedling, sapling, pole and mature stages) was examined using ANOVA in the general linear models procedure of the SAS statistical package (SAS Institute Inc., 1999). Duncan's multiple range test was used to examine differences between means when the effect of stand development was significant (balphaN = 0.05). A regression analysis was performed to examine how forms of soil P were related to the concentration of organic C. All data are presented on an oven dry basis. Regression analyses were performed using MINITAB (Release 13.1, www.minitab.com). 3. Results 3.1. Total ecosystem P The seedling stands had significantly (balphaN = 0.05) lower total ecosystem P than the other stages (Fig. 1) (model p = 0.042). This was mainly due to low concentration of total P in the soil (Table 1). In particular, the concentration of non-labile Pi in the first NaOH extract

P (g Mg−1)

C (%)

C/Pa

L layer Seedling Sapling Pole Mature Model:

647 (66)a 760 (22)b 738 (26)b 789 (18)b p = 0.0095

n.d. n.d. n.d. n.d.

n.d. n.d. n.d. n.d.

FH layer Seedling Sapling Pole Mature Model:

990 (102) 1218 (33) 1102 (111) 1253 (148) p = 0.059

44.0 (12.2) 37.3 (8.3) 35.9 (1.6) 34.2 (2.5) p = 0.77

441 (89)a 305 (61)b 327 (22)b 274 (16)b p = 0.029

Soil (0–10 cm) Seedling Sapling Pole Mature Model:

399 (67)a 706 (120)b 592 (171)b 671 (80)b p = 0.048

7.55 (0.23) 6.11 (0.22) 6.03 (0.80) 8.32 (1.69) p = 0.070

367 (48)a 214 (24)b 281 (32)c 207 (17)b p = 0.0010

Note: Values in a column followed by the same letter are not significantly different at balphaN = 0.05 according to Duncan's test. a Based on extractable organic P.

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Table 2 Concentrations (g Mg−1) of inorganic (Pi) and organic (Po) forms of soil P in the upper mineral soil (0–0.1 m) and coefficients of variation (%) in four stages of stand development of mountain beech at Craigieburn. Standard deviations are shown within parentheses (n = 3).

Concentrations Seedling Sapling Pole Mature Model:

Labile P

Non-labile P

Mineral P

Occluded P

NaHCO3

NaOH

HCl

NaOH

Residual

Pi

Po

Pi

Po

Pi + Po

Pi

Po

Pi + Po

9.9 (5.5) 18.0 (6.3) 22.1 (12) 13.0 (3.5) p = 0.28

45.7 (6.4)a 50.7 (9.1)a 49.2 (4.7)a 90.5 (21)b p = 0.006

93 (44) 240 (45) 216 (111) 152 (18) p = 0.084

133 (13)a 166 (15)a 137 (16)a 244 (37)b p = 0.001

6.8 (3.4)a 40.0 (3.2)b 35.7 (20)b 29.8 (5.7)b p = 0.020

23.7 (6.5) 39.9 (3.7) 47.2 (15) 30.7 (6.3) p = 0.051

29.2 (5.2)a 72.1 (19)b 28.0 (6.0)a 64.8 (2.0)b p = 0.001

57.6 (11) 78.8 (28) 55.7 (27) 45.8 (24) p = 0.44

14 18 10 24

48 19 51 12

10 9.3 12 15

50 7.9 55 19

28 9.2 31 21

18 27 21 3.2

19 36 49 53

Coefficients of variation Seedling 56 Sapling 35 Pole 55 Mature 27

Note: Values in a column followed by the same letter are not significantly different at balphaN = 0.05 according to Duncan's test.

3.3. P in litterfall The return of P via litterfall was mainly as leaf litter which comprised 65%, 80% and 79% of total litterfall in the sapling, pole and mature stages, respectively (the remainder being twigs). The total amount of P returned in litterfall on an annual basis did not differ significantly between stages of stand development and was 3.74 kg ha−1 in the seedling stage, 2.30 kg ha−1 in the sapling stage, 3.15 kg ha−1 in the pole stage and 3.07 kg ha−1 in the mature stage. On average for all stages of stand development this corresponded to one third of the amount stored in the L layer of the forest floor (data not shown). The annual flux of litterfall mass is given in Table 3.

(where P is extractable organic P) was significantly greater in the seedling stage than in the other stages whereas the pole stage had a significantly greater C/P ratio than in the sapling and mature stages (Table 1). The amount of P stored in the mineral soil to 10 cm depth comprised the greatest ecosystem pool and was significantly lower in the seedling stage than in the other stages of stand development (Fig. 1). Bulk soil (including N2 mm material) mass, which did not differ between stages of stand development, was on average 507 Mg ha−1 for the seedling, sapling, pole and mature stages. The mass of fines (b2 mm), which showed a large variability in the pole stage, averaged 333 Mg ha−1 and also did not differ significantly among stages (Table 3).

3.4. Total amount of P in the forest floor and soil 3.5. Soil P fractions The amount of P stored in the L layer of the forest floor did not differ significantly between any of the three stages of stand development whereas the amount of P stored in the FH layer was significantly greater in the pole stage than in the other stages. This was also true for the total organic layer (LFH) (Fig. 1). This was mainly due to a significantly greater mass of the FH layer in the pole stage (Table 3). Neither the concentration of P in the L layer or FH layer nor the concentration of carbon (C) nor the C/P ratio in the FH layer depended significantly on stage of stand development (Table 1). The concentration of C in the mineral soil did not depend significantly on stage of stand development whereas the C/P ratio in the mineral soil Table 3 Annual flux of litterfall and mass of ecosystem components to 0.1 m depth of the mineral soil in four stages of stand development at Craigieburn. Standard deviations are shown within parentheses (n = 3). Stand type

Litterfalla

Live stemwood

CWDb

Forest floor L layer

Forest floor FH layer

Mineral soil 0–10 cm

169 (46)a 99 (39)a 25 (17)b 24 (5.3)b p = 0.001

18 (5.6)a 10 (0.6)b 14 (2.9)ab 10 (0.74)b p = 0.043

58 (25)ab 43 (4.1)b 82 (20)a 33 (9.6)b p = 0.033

315 (21) 293 (50) 429 (159) 297 (26) p = 0.24

The concentration of labile inorganic P (0.5 M NaHCO3 extractable) did not differ between any of the four stages of stand development whereas the concentration of labile organic P was significantly greater in the mature stage as compared to the other stages of stand development. A similar result was obtained for the concentration of non-labile (0.1 M NaOH extractable) organic P (Table 2). The concentration of mineral bound P (HCl extractable) was significantly lower in the seedling stage than in the other stages of stand development. However, the concentration of occluded organic P (0.1 M NaOH extractable P following extraction with 1 M HCl) was significantly lower in the seedling and pole stages than in the sapling and mature stages (Table 2). No significant differences were found between stages of stand development in the concentration of residual P (Table 2) whereas the concentration of total P in the mineral soil was significantly lower in the seedling stage than in the other stages of stand development (Table 1). The concentrations of labile and non-labile organic P depended significantly and positively on variations in the concentration of soil organic C (p = 0.005, R2 = 56.3% and p = 0.022, R2 = 42.3%, respectively)

Mass (Mg ha−1) Seedling Sapling Pole Mature Model:

6.2 (2.1) 3.2 (0.63) 4.4 (0.22) 4.1 (0.90) p = 0.078

0.57 (1.0)a 20 (9.5)b 273 (36)c 245 (59)c p = 0.001

Table 4 Number of plots containing coarse woody debris in each stage of decay (N) and density, mean P concentration, C/P ratio and N/P ratio of coarse woody debris. Standard deviations are shown in parentheses. Decay class

n

Density (kg m−3)

P (g Mg−1)

C/P

N/P

I II III Model:

8 12 12

406 (32)a 304 (69)b 232 (59)c p = 0.001

264 (211) 139 (68) 192 (110) p = 0.19

2986 (1809) 4942 (2307) 4286 (1951) p = 0.31

7.15 (4.43)a 12.5 (4.37)b 12.8 (3.93)b p = 0.025

P (kg ha−1)c Model:

p = 0.36

p = 0.001

p = 0.003 p = 0.44

p = 0.030 p = 0.048

Note: Values in a column followed by the same letter are not significantly different at b alphaN = 0.05 according to Duncan's test. a Annual return of P in litterfall estimated from 1-year sampling. b Coarse woody debris. c Data on mass of P in Fig. 1.

Note: Values in a column followed by the same letter are not significantly different at balphaN = 0.05 according to Duncan's test.

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whereas the concentration of occluded organic P was uncorrelated to the concentration of soil organic C (p = 0.84, R2 = 0.4%) (Fig. 2). Labile and non-labile inorganic P as well as mineral bound P (1 M HCl extractable) did not depend significantly on variations in soil organic C whereas occluded inorganic P was negatively correlated to organic C (p = 0.008, R2 = 66.2%). 4. Discussion 4.1. The chronosequence assumption Firstly, our test of the chronosequence assumption revealed that the seedling stands deviated from the other stands in terms of total P (in the topsoil b2 mm, forest floor, biomass and CWD) (Fig. 1). This was mainly due to the fact that the seedling stands had lower concentrations of mineral P (HCl extractable) in the soil as compared to the other stages of stand development (Table 2). Soil mineral P is not expected to vary in a cyclic pattern during the course of stand development at the investigated sites since mineral P cannot be formed in acidic soils. In an attempt to find an explanation on why the seedling stands differed from the other stand types, we observed that average slope angles were lower for the seedling stands (13 degrees) than for the other stand types (28 degrees). It is possible that long term soil processes such as erosion, weathering and leaching differed due to topography and that soil mineral P content had been affected by this. Secondly, the pole stands showed large variability in the mass of fine soil (b2 mm) per unit area. This variability is inevitably due to site properties rather than an effect of stand development. Thus, the chronosequence assumption is not fulfilled as regards this aspect either. Thirdly, it needs to be stressed that our chronosequence is replicated but not randomized. True randomization can only be achieved in experiments and the choronosequence approach is therefore not optimal. Thus, in our case, replicate plots are strictly speaking not independent. Specifically, the seedling and sapling stands were located within a rather limited area and the risk of pseudoreplication is therefore higher for the seedling and sapling stands than for the pole and mature stands. This is due to the fact that soil chemistry naturally tends to be less variable across shorter distances. However, as regards the concentration of soil P forms the coefficient of

variation was not generally lower for the seedling and sapling stands than for the pole and mature stands. The coefficient of variation for inorganic forms of soil P was higher for the seedling and pole stages than for the sapling and mature stages (Table 2) which may be related to the specific conditions for these stand types as mentioned earlier. The coefficient of variation for organic forms of soil P did not show any clear pattern related to stage of stand development (Table 2). Finally, the chronosequence approach can be tested by re-measuring soil variables after a certain time and then comparing the direction and magnitude of change with that predicted by the chronosequence (c.f. Yanai et al., 2000). This comparison is not available for soil phosphorus, however a decrease in forest floor C content between the pole and mature stages predicted by the chronosequence was verified by a remeasurement of forest floor and soil C 10 years following the initial measurements (Davis et al., 2003). 4.2. Ecosystem processes and soil P The fact that we only examined the upper 10 cm of the mineral soil limits our ability to calculate a full P budget for each stage of stand development. Our focus will be on how the relative distribution of forms of soil phosphorus depends on stand development. Our hypothesis about the biogeochemical stability of P forms was not supported by the study. Our data suggest that labile as well as non-labile and occluded organic P forms undergo biogeochemical transformation during the course of stand development. The redistribution of P between stemwood, CWD and forest floor followed a similar pattern as has been observed for N in the investigated age sequence of mountain beech stands (Clinton et al., 2002) where relatively large amounts of N, and P in the present study, were stored in CWD in the sapling stage and in the forest floor or stemwood in the pole and mature stages. Differences among stand types in organic P forms in the soil could be interpreted as an effect of above and below ground processes such as accumulation of P in stemwood, mineralization of P from CWD, and release of organic P from the forest floor as well as mineralization of soil organic P. We did not determine the P content of branches and foliage but assume that these correlate positively to the P content of stemwood. 4.3. Transition between seedling stage and sapling stage The transition between the seedling stage and sapling stage was mainly associated with losses of P from stemwood as decomposing CWD and low levels of P uptake in stemwood of saplings (Fig. 1) whereas the concentrations of mineral P and occluded organic P in the soil increased (Table 2). The suggested increase in concentrations of occluded organic P may at least partially be due to mineralization of CWD but other processes such as root turnover could have contributed. The observed differences in mineral P is probably due to the fact that site conditions differed between the seedling stands and the other stand types as discussed earlier. It is also possible that occluded organic P could have been affected by this. 4.4. Transition between sapling and pole stages

Fig. 2. Labile (open circles), non-labile (open squares), and occluded (filled triangles) organic P as related to soil organic C for the mountain beech stands at Craigieburn (n = 12). The stage of stand development is indicated by the size of the symbol where the seedling stage is represented by the smallest symbols and the sapling, pole and mature stages by increasing symbol sizes.

The transition between the sapling and pole stages was associated with increases in P storage in stemwood and in the FH layer. On the other hand, P storage in CWD decreased between the sapling and pole stages (Fig. 1). It is likely that a considerable part of the “extra” storage of P in the forest floor in the pole stage originated from fragmented, partially decomposed CWD but possibly also from an increased production of woody litter between the sapling and pole stages when the stands tended to become denser (cf. Holdaway et al., 2008). The concentration of occluded organic P in the soil was lower in the pole stage than in the sapling stage (Table 2). This may suggest that occluded organic P was utilized by the aggrading forest when tree demand was relatively high but the exact mechanism is unknown.

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4.5. Transition between pole and mature stages The transition between the pole and mature stages was characterized by a decrease in the storage of P in the FH layer (Fig. 1) whereas in the soil, the concentrations of labile, non-labile and occluded organic P increased (Table 2). No major changes in the storage of P in stemwood or CWD were observed between these stages of stand development (Fig. 1). It is possible that P had been transferred from the FH layer to the mineral soil resulting in increased concentration of organic forms of soil P. The mechanism of transfer is unknown. However, some dissolved organic P is expected to be released from the FH layer (cf. Smith et al., 1998; Kalbitz et al., 2000). Furthermore, the mineral soils at Craigieburn contain rather high concentrations of aluminium (Davis, 1990; Matzner and Davis, 1996) which could retain dissolved organic P (cf. Qualls et al., 2002; Lilienfein et al., 2004). An alternative explanation for increases in organic forms of soil P would involve in situ transfer of inorganic forms of soil P to organic forms in the upper soil (0–10 cm) through root and mycorrhizal activity. Decreases in all forms of inorganic P between the pole and mature stages give some support to this, although changes were not statistically significant. However, root uptake of P from deeper mineral soil cannot be excluded. 4.6. Transition between mature stage and seedling stage The transition between the mature stage and seedling stage, which occurred via catastrophic disturbance, was mainly associated with losses of P from stemwood as decomposing CWD and low levels of P uptake in stemwood of seedlings (Fig. 1). The loss of P in CWD between the catastrophic disturbance (where CWD equals P in stemwood in the mature stages) and the seedling stage appeared large, i.e. more than 50% was lost during approx. 10 years (cf. Fig. 1). It should be noted that this figure is uncertain due to the fact that our estimate of stemwood P concentration was associated with large variability. Nordmeyer (unpublished) reported stemwood P concentrations between 0.027% and 0.054% in mountain beech and in comparison to these values our estimate is relatively low. It should also be noted that mature stems often are affected by heart rot (Wardle, 1984) which may have led to an overestimation of stemwood mass. Our observation of rapid losses of P from decomposing wood is in contrast to a number of studies showing that the release of P from decaying wood (CWD) may be slow or even show an accumulation at some stage during decomposition (Busse, 1994; Krankina et al., 1999; Laiho and Prescott, 1999). Our data on P concentration in CWD at different stages of decay (Table 4) suggest that considerable amounts of P were lost during early stages of decay since both P concentration and density of CWD decreased markedly between decay classes I and II. Laiho and Prescott (1999) suggested that the pattern of P release from decaying CWD may depend on whether the microbial community is P limited or limited by other nutrients (e.g. N) with a slow release, or even accumulation, of P in CWD in P limited decomposer subsystems and relatively rapid release of P in P sufficient systems. Our data on N/P ratios along CWD decay classes suggest that P was sufficient relative to N in early stages of decay as indicated by an N/P ratio below the Redfield ratio (N/P = 16) in decay class I, whereas decomposition may have been co-limited by N and P in later stages of decay (Table 4). This may explain early rapid losses of P from decomposing CWD. The concentrations of all forms of organic P in the soil were lower in the seedling stands than in the mature stands (Table 2). It is possible that canopy disturbance may have enhanced conditions for organic matter decomposition resulting in mineralization of organic P. For example, labile and non-labile organic P were associated with variations in soil organic C (Fig. 2) and the concentration of organic C decreased from the mature stage through to the pole stage. The low concentration of occluded organic P in the seedling stage as compared

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to the mature stage may, on the other hand, be related to high nutrient demand by the dense seedling stands (cf. Allen et al., 1997). However, as mentioned earlier any difference between the seedling stands and the other stand types could be influenced by pre-existing site differences between the former and the latter. 4.7. Variations in soil P forms and P availability during stand development Foliar concentrations of P did not differ significantly among stages of stand development and varied from 1.17 g kg−1 in the pole stage to 1.27 g kg−1 in the sapling stage (Clinton et al., 2002). Foliar N:P ratios were close to 10 in all stages of stand development (Clinton et al., 2002) indicating N limitation rather than P limitation (Ericsson, 1994; Güsewell, 2004). Thus, the availability of P in the soil at Craigieburn appeared to be relatively high across all stages of stand development. Our results suggest that labile, non-labile and possibly occluded organic P contribute to the long term (decades) available pool of soil P in aggrading mountain beech forests and are in accordance with those found by Richter et al. (2006) in the sense that insoluble P cannot be assumed to be of negligible ecological significance during decadal time spans. In particular, organic P is often assumed to constitute a stable pool of soil P (Walker and Syers, 1976; Cross and Schlesinger, 1995; Johnson et al., 2003). However, rapid increases in soil organic P have been observed. For example, in the Franz Josef chronosequence studied by Turner et al. (2007) organic P increased during the first 130 year from 5 g Mg−1 to 220 g Mg−1 which was close to maximum for the entire sequence. It is noteworthy that in long term soil chronosequences which have been developed in the absence of major disturbances, a maximum in organic P content (kg/ha) often coincides with relatively high productivity (Crews et al., 1995; Turner et al., 2007) when the turnover of organic P is expected to be high. Short term (years or decades) decreases in labile and non-labile organic P due to a change in land use or as an effect of plant species have also been observed (Condron et al., 1996; Chen et al., 2002). Our results are consistent with these observations indicating a rather dynamic nature of soil organic P. The availability of P in many forest ecosystems appears related to soil organic P (Harrison, 1975; Polglase et al., 1992; Parfitt et al., 2005; Watt et al., 2005; Turner et al., 2007). This could be due to the fact that many forest tree species, like mountain beech, are ectomycorrhizal which may promote recycling of organic P (Turner et al., 2007). 5. Conclusion The biogeochemical stability of soil P is often assumed to be related to its solubility. However, our results suggests that labile, non-labile as well as occluded forms of soil organic P are all affected by biological processes during stand development in natural ecosystems regenerated after windthrow. Acknowledgements We thank Larry Burrows, Dianne Carter, Kevin Platt and Graeme Rogers for assistance with the fieldwork. We also thank Murray Lang, Roger Creswell and Jason Breitmeyer for help with the phosphorus analyses and the previous reviewers for valuable comments. The project was partly funded by the Foundation for Research, Science and Technology (contract no. C09X0502) and by Carl Tryggers Stiftelse (grant no. CTS 02-38 to P.-O. Brandtberg). References Allen, R.B., Clinton, P.W., Davis, M.R., 1997. Cation storage and availability along a Nothofagus forest development sequence in New Zealand. Can. J. For. Res. 27, 323–330. Allen, R.B., Bellingham, P.J., Wiser, S.K., 1999. Immediate damage by an earthquake to a temperate montane forest. Ecology 80, 708–714.

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