Short-term controls over inorganic phosphorus during soil and ecosystem development

Soil Biology & Biochemistry 37 (2005) 651–659 www.elsevier.com/locate/soilbio

Short-term controls over inorganic phosphorus during soil and ecosystem development L.P. Olander*, P.M. Vitousek Department of Biological Sciences, Stanford University, Stanford CA 94305-5020, USA Received 25 November 2003; received in revised form 18 June 2004; accepted 17 August 2004

Abstract Geochemical sorption and biological demand control phosphorus (P) retention and availability in soils. Sorption and the biota predominantly utilize the same inorganic form of P, from the same soil pool, on the same time scale, and thus are likely to compete for P as it flows through the available pool. In tropical soils, P availability is typically quite low and soil geochemical reactivity can be quite high. We tested whether greater P sorption strength in tropical soils resulted in lower biological uptake of available P. Since the strength of soil sorption and biological demand for P change as ecosystems develop and soils age, we used soils from the two upper horizons from three sites along a 4.1 million-year-old tropical forest chronosequence in the Hawaiian archipelago. We evaluated the strength of geochemical sorption, microbial demand, and the partitioning of added available P into biological versus geochemical soil pools over 48 h using a 32PO4 tracer. Soil sorption strength was high and correlated with soil mineral content. The amount of added phosphate geochemically sorbed versus immobilized by microbes varied more between the organic and mineral soil horizons than among soil ages. Microbial activity was a good predictor of how much available P was partitioned into biological versus geochemical pools across all soils, while sorption capacity was not. This suggests that microbial demand was the predominant control over partitioning of available P despite changes in soil sorption strength. q 2004 Elsevier Ltd. All rights reserved. Keywords: Phosphate;

32

P tracer; Sorption; Mineralogy; Hawaii

1. Introduction (POK 4 )

is the predominant form of biologically Phosphate available P in soils. In many humid tropical and volcanic soils available PO4 is rapidly and, in some cases, nearly irreversibly sorbed to iron and aluminum oxide minerals that dominate these soils (Wada, 1985; McBride, 1994). In tropical agricultural systems sorption is often cited as a reason for P limitation to plant productivity and for high P fertilizer requirements (Sanchez, 1976; Yost et al., 1979). However, mature tropical forests are generally productive without substantial P inputs, suggesting that the forest biota either have lower P demand than crops or they compete more effectively for P. Nevertheless, several studies have

* Corresponding author. Current address: Department of Global Ecology, Carnegie Institution of Washington, 260 Panama Street, Stanford, CA 94305, USA. Tel.: C1 650 462 1047x215; fax: C1 650 325 6857. E-mail address: [email protected] (L.P. Olander). 0038-0717/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2004.08.022

found that P additions can enhance tropical forest productivity, root growth, and microbial activity (Cuevas and Medina, 1988; Tanner et al., 1990; Herbert and Fownes, 1995; Ostertag, 2001; Cleveland et al., 2002). In an earlier paper, we evaluated the ability of soil microbes to compete with geochemical sorption for PO4 in a young soil with strong sorption and low P availability. In comparing horizons, microbial demand appeared to be the dominant control over partitioning of available PO4 into biological versus geochemical sinks (Olander and Vitousek, 2004). Here, we evaluate whether microbial demand maintains control over available P across a soil developmental sequence, where changes in soil mineralogy alter the strength of the geochemical sink for P (Jenny, 1941; Walker and Syers, 1976). In young systems, the soils are composed mainly of primary minerals and have relatively high pH, which normally results in a relatively weak geochemical sink. Over time the weathering of primary minerals increases soil acidity leading to the formation of secondary

L.P. Olander, P.M. Vitousek / Soil Biology & Biochemistry 37 (2005) 651–659

4.8 4.6 3.7 4.0 4.0 4.3 54.0 38.5 87.1 67.0 133.3 20.2 5.3 12.2 3.1 12.4 7.2 21.0 20.8 47.6 5.0 9.6 19.0 25.2

5.8 12.2 18.3 28.0 6.7 7.9

Al2O3a (%)

3.2 2.6 11.7 9.5 1.7 25.9 5.6 7.8 10.0 27.1 3.5 1.42

c

d

a

b

4,100,000

20,000

Data from O. Chadwick, pers comm. Some methods are described in Vitousek, 2004. Bray P1 extractable. Data from Olander and Vitousek (2000). Data from M. Torn, pers comm. and Vitousek et al. (1997).

42.3 55.2 37.0 47.9 26.8 66.2 34.3 20.7 57.52 45.8 52.9 5.3 48.3 19.9 93.5 56.3 81.6 44.0 1.15 0.60 4.32 0.27 3.22 0.47 Oa A O A Oe B Bw1 300

0.22 0.38 0.29 0.34 0.25 0.91

Soil horizon

Available Pb (mg/g)

10.30 7.86 22.71 9.86 10.31

Organic mattera H2O2 (%) Organic matter LOI (%)

2.1. Study sites

Bulk densitya (g/cm)3

Pasec (mmol/g/hr)

clay minerals that are dominated by reactive iron and aluminum oxides which sorb P more readily. Earlier research suggested that as clay mineralogy changes over time, long-term P retention shifts from biological to geochemical sinks (Crews et al., 1995; Vitousek et al., 1997). In young systems, phosphate is supplied by rock weathering and available and organic P build up in soils, but eventually rock derived P is depleted and organic P becomes the primary pool of P. Up to this time biological pools dominate, but with continued P loss and increasing occlusion, organic P also declines and the geochemical pool dominates. Does this long-term pattern of increasing geochemical sinks also drive short-term reactions, such that the control of short-term phosphate cycling shifts from biological to geochemical over time?

2. Materials and methods

Site (years)

Table 1 Soil characteristics for three sites along tropical montane forest chronosequence in Hawaii

Mineral contentd (%)

Non-crystalline minerald (%)

Sesquioxide minerald (%)

SiO2a (%)

Fe2O3a (%)

CEC PH 7.0a (%)

PH H20a (1:10)

652

We studied soils from three sites along a tropical forest chronosequence in the Hawaiian archipelago. Parent material, elevation, precipitation, slope position, disturbance history, and dominant vegetative cover are relatively consistent across this chronosequence (Crews et al., 1995). The sites range from 300 to 4.1 million years old and are found between 1100 and 1200 m above sea level, in aseasonal montane rainforest dominated by the tree Metrosideros polymorpha (Gaud.), and receive a mean annual rainfall near 2500 mm. The 300-year-old site is located near the Thurston lava tube in Volcano National Park on the island of Hawaii. The soil is classified as a Lithic Hapludand (Vitousek, 2004) dominated by feldspar, olivine and glass; it already contains significant quantities of noncrystalline minerals (Vitousek et al., 1997) (Table 1). The soil has relatively low N and P availability (Crews et al., 1995), and N limits above ground plant productivity (Vitousek et al., 1993; Vitousek and Farrington, 1997). The 20,000-year-old site is located on Mauna Kea Volcano. The soil is a Hydric Hapludand dominated by non-crystalline allophane and imogolite minerals, and is high in available N and P, and neither N nor P alone limit plant growth. The 4.1 million-year-old site is located in Kokee State Park on the island of Kauai. The soil is classified as a Plinthic Kandiudox dominated by secondary kaolin and crystalline sesquioxide minerals. It has low P and high N availability and P supply limits plant growth (Herbert and Fownes, 1995). For additional soil characteristics see Table 1. 2.2. Soil sampling At the youngest site, soils were sampled down to an ash deposit The upper organic horizon (Oa) had a dense root mat, while the lower horizon (A) had a lower root density (Ostertag, 2001), greater bulk density and higher mineral

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content (Table 1). At the intermediate aged site, the organic horizon (OeCOa) and the underlying mineral (A) horizon were sampled. At the oldest site, the organic horizon sits above a plinthite layer of rocky concretions with little or no A horizon in between with a mineral clay horizon directly below the plinthite. The plinthite is very low in microbial activity (Lohse, 2002); we sampled the clay (Bw1) horizon instead. Soils were sampled from three random locations in each of three replicate areas separated by at least 15 m at each site. Soil samples were composited by horizon and site to provide homogenized samples representative of field soils with two horizons from three sites for our comparative laboratory manipulations. Samples were stored at 4 8C and analyses were conducted within 3 weeks of sampling (for details see Olander and Vitousek, 2004). 2.3. Soil characterization Soil organic matter content and Bray P1 extractable P were measured on all soils. An index of microbial biomass was determined using chloroform fumigation direct extraction (CFDE) (Vance et al., 1987; Beck et al., 1997) with a 24 h fumigation period, followed by extraction with 0.5 M K2SO4 for 1 h. As an index of potential microbial activity, cumulative CO2-C flux was measured from soil suspensions of 1 g soil to 10 ml 0.01 M KCl over 24 h after a 3 mg acetate C addition (for details see Olander and Vitousek, 2004). Modified sorption isotherms for the six homogenized soil samples were developed by adding eight concentrations of phosphate-P to suspensions of 1 g soil to 10 ml solution for final concentrations ranging from 0 to 300 mgP/g soil. We used six replicate subsamples from each soil sample for each concentration. Soil suspensions were shaken for 24 h at 4 8C. The low temperature eliminates microbial activity and immobilization of P. After the incubation, Bray Pi was measured in the soil suspensions. We defined sorbed P as added P not extractable with Bray P1; thus sorbed P here includes only the more recalcitrant (specifically) sorbed P. The added P extractable by Bray P1 includes the soil solution and loosely (non-specifically) sorbed P. Bray P1 was used; (1) so that the isotherms measured specific sorption, which may be more directly related to P availability (2) to measure the same P pools that are used in the tracer experiments; and (3) to determine a sorption correction for our measurement of microbial biomass P, which was also measured using Bray P1. 2.4. Tracer study We added a radioactive 32P-labeled phosphate tracer (1.38!103 Bq/ml) to a 10 mg/ml phosphate-P solution (in 0.01 M KCl) made from a 1000 ppm P-phosphate standard (KH2PO4 in water, Fisher LC18590-1). 10 ml of labeled phosphate solution was added to 1-quart mason jars for every 1 g dry weight of soil, with a total of 12–26 g of soil in

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each jar. We used three sets of samples for three different manipulations: (1) phosphate added with no C added, sampled at 30 min, 24, and 48 h; (2) C added 1 h before phosphate added, sampled at 30 min and 24 h; and (3) C added 24 h after phosphate added, sampled at 24 h, immediately before C was added, and again at 48 h. Labile C was added as 3 mg acetate/g soil (0.8784 mg C) to stimulate microbial activity and demand for P. Carbon added 1 h before the phosphate addition was used to assess the effect of C supply on microbial competition for P. Carbon added 24 h after the phosphate addition was used to evaluate microbial acquisition of already-sorbed tracer P. There were three replicates jars for each combination of soil, P concentration, and C addition. At each sampling, 80 ml of soil suspension were removed from the jars; 20 ml for soil solution Pi, 20 ml for determination of Bray Pi and 40 ml for microbial P. We define the non-specifically sorbed P as Bray Pi minus soil solution Pi. Microbial biomass P was determined using a modified CFDE method (Brookes et al., 1982, 1984; Morel et al., 1996; Oberson et al., 1997). We measured 32P and total 31PO4 in each of these pools. 32P concentrations were measured by Cherenkov scintillation counting. 3–5 ml of sample was diluted to 20 ml with deionized water before counting. The ratio of 32P to 31P in the added phosphate solutions was used to transform the measured activity of 32P in each of the pools into the amount of added 31P found in each pool. pH was measured in all solution P samples. For details on the methods and modifications see Olander and Vitousek (2004). 2.5. Calculations and corrections CFDE P is an underestimate of the total microbial P pool, thus our data for microbial biomass P and microbial immobilization of P are underestimates. Ideally corrections would be determined for each soil under study, but the methods are difficult and uncertainty persists. As a result, many researchers compromise using an average correction factor based on other studies (Brookes et al., 1982; Hedley and Stewart, 1982; McLaughlin et al., 1986). Due to the uncertainty in the corrections we generally present uncorrected CFDE P numbers. However, we did determine a correction to provide another, perhaps upper, constraint on microbial P and P immobilization. Because our soils vary significantly in sorption strength, we experimentally determined a correction for the sorption of microbial P released during fumigation for each soil (Barrow and Shaw, 1975; Morel et al., 1996; Oberson et al., 1997). We combined this with a literature-based estimate for the average amount of P released from bacterial and fungal cells in culture. We used a microbial release factor of 0.80 (Hedley and Stewart, 1982; McLaughlin et al., 1986; Eberhardt et al., 1996). The amount of added tracer P specifically sorbed was calculated as the total P added minus the amount of added

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P found in the other measured pools (solution P C nonspecifically sorbed P C microbial CFDE P), which is in practice the fumigated Bray-Pi. Where measurements yielded a negative microbial P pool, we assumed it was zero for calculation of sorbed P. These cases are noted in the tables. We ran the tracer study for a maximum of 48 h to minimize the transfer of labeled phosphate into the organic pool, where it would be measured as part of the sorbed pool (Oehl et al., 2001; Buehler et al., 2002). 2.6. Data and statistical analysis An index of sorption capacity for each soil horizon was determined by fitting the modified sorption isotherm data to the Langmuir model (Sigmaplot Co. 2000). The a-value from the regression is an estimate of soil P sorption capacity (Langmuir, 1918). We assessed whether potential microbial activity (cumulative CO2-C flux) corresponded well with other indices of microbial activity and P demand using a Pearson’s correlation index with P availability (Bray Pi), microbial biomass C and P (CFDE), and potential phosphatase activity (JMPIN, 1995). For analyses of the tracer data, the Bray Pi, CFDE P, and uncorrected sorbed P data were log10 transformed to obtain normal distributions. Two-way analysis of variances were used to determine the significance of differences among sites and between horizons in potential microbial activity and the amount of tracer P in each of the soil pools (JMPIN, 1995). The relationship between sorption capacity and soil mineral content, and trends in the partitioning of tracer phosphate with soil age were assessed using linear regression analysis. The effect of C on the partitioning of phosphate was assessed separately for the initial C addition and the 24 h C addition using one-way analysis of variance for each (JMPIN, 1995). To evaluate the relative importance of microbial demand and sorption strength in controlling phosphate partitioning in the tracer experiment, we conducted multiple analyses of variance. We tested the importance of the two independent soil characteristics that quantify the strength of microbes and sorption: sorption capacity using the Langmuir a-value index, and microbial demand using the potential microbial activity index. We evaluated how well these indices predicted the amount of added P found in Bray extractable, microbial, and sorbed pools—the dependent variables— over time and with different C additions (JMPIN, 1995). The analysis was done with both uncorrected and corrected data for microbial and sorbed P. In those cases where measurement of the uncorrected microbial P was zero or negative it was not possible to calculate an estimate of corrected microbial and sorbed P; these cases were left as missing values in statistical analyses. Since the uncorrected and corrected data for microbial and sorbed P contain uncertainty we conducted an analysis to determine how sensitive the ANOVA results were to biased error in these data. By biased error, we mean error in the methods or

corrections that are caused by difference between soils or treatments (for details see Olander, 2002).

3. Results P sorption was strong across the chronosequence. With microbial uptake suppressed, all soils sorbed 100% of additions up to 50 mgP/g soil and from 30 to over 90% of 300 mg phosphate-P additions (Fig. 1). The Langmuir model fit the soil isotherm data well (adj R2Z0.70–0.98; NZ6), providing an index of sorption capacity on a soil weight basis that followed the order: 20,000 year AO300 year AZ 300 year OaO4.1 m. yr BO20,000 year OO4.1m year O (Table 2). In the upper organic horizons, sorption capacity decreased with soil age as total mineral content decreased. In the lower mineral horizons, sorption followed noncrystalline mineral content; greatest at the 20,000 year old site where non-crystalline minerals dominate, a bit lower in the 300-year-old site where non-crystalline minerals are present, and lowest in the clay dominated (B) horizon of the 4.1 million-year-old soil with its sesquioxide crystalline minerals (Table 1). Cumulative C flux, a measure of potential microbial activity, was positively correlated (p!0.01) with indices of P availability and potential P demand including: Bray extractable Pi (adj R2Z0.73), potential acid phosphatase activity (0.94), and microbial CFDE P (0.82) and CFDE C

Fig. 1. Sorption of added PO4-P where; P sorbedZ (P addedCP extractable with no P added)Kextractable P. Bray P1 was used for the extractions, and with no P added, extractable P was less than 0.4 mgP/g in all soils. Incubations were conducted over 24 h at low temperatures to eliminate microbial activity. Soils are upper horizons from three sites along a Hawaiian montane forest chronosequence.

L.P. Olander, P.M. Vitousek / Soil Biology & Biochemistry 37 (2005) 651–659 Table 2 Sorption capacity for soils from the long soil age chronosequence in Hawaii based on P sorption isotherm data on a per gram soil basis fit to the Langmuir model (NZ6). The Langmuir is yZabx/(1Cbx), where yZ sorbed P, xZP remaining extractable, and a and b are fitting parameters. The a-value provides an estimate of sorption capacity Site (years)

Soil horizon

Langmuir model a-value (mg P)

SE

Adj. R2 (model fit)

300

Oe Oa O A Oe B

0.397 0.383 0.255 0.485 0.085 0.385

0.044 0.027 0.026 0.034 0.007 0.022

0.87 0.96 0.77 0.97 0.70 0.98

20,000 4.1 m

(0.74). Potential microbial activity was at least two times greater in the nutrient rich intermediate aged site for both organic and mineral horizons than in the young and old sites (Fig. 2a). For all sites, microbial activity in the upper organic horizon soils was at least two times higher than in

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the lower. Microbial activity in the B horizon of the oldest site was notably low, probably due to its location below the plinthite layer where root density, organic C, and microbial biomass were low. Uptake of tracer P into microbial and geochemical pools was extremely rapid. For all soils, over 70% of tracer P was sorbed or immobilized only 30 min after phosphate addition, and by 48 h over 95% was consumed leaving less than 5% in the extractable pool (Table 3). The uncorrected data for microbial P suggest that most added phosphate was sorbed, from 60 to over 90% sorbed with only 5–35% immobilized, but the corrected data suggest most added phosphate was immobilized in the upper organic horizons, with sorption and immobilization comparable in the lower mineral horizon. We observed significant differences in the amount of tracer P found in the extractable, microbial and sorbed pools with soil age and with horizon, and for all but the sorbed pool with soil age by horizon (uncorrected data, p!0.01, Table 3).

Fig. 2. Indices of microbial activity and P sorption capacity across the soil chronosequence, and the uncorrected data showing partitioning of tracer phosphate 24 h after P addition with no C additions: (a) potential microbial activity measured as CO2-C flux from soil suspensions over 24 h; (b) sorption capacity based on the Langmuir a-value; (c) phosphate tracer immobilized, and (d) phosphate tracer sorbed.

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Table 3 Partitioning of 10 mg of added P per g soil into Bray extractable, microbial immobilized and sorbed pools based on 32P tracer recovery in soils of the long age gradient in Hawaii Site (years)

Time (h)

300

Oa

A

20,000

O

A

4,100,000

Oe

B

0.5 24 48 0.5 24 48 0.5 24 48 0.5 24 48 0.5 24 48 0.5 24 48

Bray extractable P

Microbial immobilized P

Sorbed P

Mean

SE

Mean

SE

Mean

SE

0.53 0.44 0.46 2.79 0.46 0.41 0.96 0.22 0.12 1.67 0.30 0.11 1.33 0.19 0.12 2.49 0.90 0.49

0.13 0.01 0.09 0.20 0.01 0.01 0.10 0.02 0.01 0.30 0.04 0.02 0.01 0.02 0.02 0.16 0.04 0.07

3.53 3.34 1.54 K0.57 1.64 1.62 2.30 2.40 2.16 K0.02 0.32 0.54 1.86 1.90 1.32 K0.71 0.48 K0.47

0.71 0.73 0.31 0.50 0.22 0.08 0.22 0.41 0.18 0.49 0.08 0.04 0.51 0.45 0.10 0.20 0.19 0.14

5.93 6.22 8.01 7.77a 7.90 7.97 6.74 7.37 7.73 8.35a 9.38 9.35 6.81 7.91 8.56 8.22a 8.61 9.97a

0.37 0.42 0.13 0.19 0.13 0.05 0.12 0.23 0.10 0.04 0.02 0.01 0.25 0.25 0.04 0.07 0.08 0.01

Corrected immobilized P mean

Corrected Sorbed P mean

8.08 9.17 7.45

1.38 0.39 2.10

4.89 4.59 6.67 10.77 10.60 3.58 3.70 6.10 5.61 6.40 4.86

4.65 5.00 2.37 K1.00 K0.72 5.35 6.00 3.79 3.06 3.40 5.02

3.08

5.94

The amount of added P found in each pool is an average of three replicates in mgP/gsoil. a Since CFDE P data were negative, they were assumed to be zero in calculation of sorbed P.

As typically observed in soils, sorption strength and biological demand co-vary. P sorption increased as microbial immobilization decreased with depth (Fig. 2a and b). Also, sorption increased with age while microbial immobilization decreased (Fig. 2c and d). In both horizons sorption was negatively correlated with immobilization across the sites (organic, adj R2Z0.95, p!0.01; mineral, adj R2Z0.55, p!0.05). The changes in microbial immobilization with soil age were relatively small, compared to differences between horizons, with immobilization at least two times greater in the upper horizons at all sites. Because the factors driving P partitioning—microbial demand and sorption strength—and the partitioning itself co-vary it is

difficult to distinguish the relative importance of microbial demand and sorption strength in controlling partitioning into microbial and sorbed pools. Thus, we assumed that if sorption strength or our index of microbial activity was better able to predict P partitioning across the soil horizons, ages, and C additions, this would tell us whether sorption strength or microbial demand was the primary determinant of P partitioning. Based on multiple analyses of variance, the respiration based index of potential microbial activity was consistently the only significant predictor for the partitioning of tracer phosphate into microbial, sorbed and extractable pools, regardless of whether the uncorrected or corrected data for tracer P were used (Table 4). The results

Table 4 Multiple ANOVA describing the relative influence of potential microbial activity versus soil sorption capacity on the partitioning of added inorganic P into available, microbial and sorbed P pools Df

Potential microbial activity Sorption capacity

Bray extractable available P (ObsZ126)

Uncorrected immobilized P (CFDE P) (ObsZ126)

Uncorrected sorbed P (ObsZ126)

Estimated corrected immobilized P (ObsZ100)

Estimated corrected sorbed P (ObsZ100)

p-value

F-ratio

p-value

F-ratio

p-value

F-ratio

p-value

F-ratio

p-value

F-ratio

1

!0.0001

16.7

!0.0001

36.1

0.0536

3.80

!0.0001

68.4

!0.0001

62.6

1

0.6077

0.1720

1.89

0.0109

0.26

0.0431

4.17

6.75

0.0132

6.38

Bray extractable, uncorrected CFDE P and sorbed P data were all log10 transformed for analyses. Corrected data were not transformed; Sorption capacity based on isotherm data fitted to Langmuir model. The a parameter value is the model estimated sorption capacity; Potential microbial activity is based on cumulative CO2-C flux from soils with C added over 24 h; Multiple tests drops level of significance by the number of tests. We have three pools (two different calculations)!2 factorsZ6 tests; Therefore to be significant at a level equivalent to: 0.05 the p-value needs to be equal or less than 0.0084; 0.01 the p-value needs to be equal or less than 0.0016.

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of these ANOVAs were insensitive to changes in the corrections for microbial P (Olander, 2002). Also, C additions provided a direct test of whether microbial demand could drive phosphate partitioning. If adding C enhanced P demand, resulting in increased P immobilization and decreased sorption, we would have strong evidence for direct microbial control over phosphate partitioning. We did observe a significant increase in P immobilization and reduced P sorption in the mineral horizon when C was added 24 h after P (Fig. 3).

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4. Discussion Theory suggests that soil sorption strength should increase as soils age (Jenny, 1941). We did not see this pattern. Soils derived from volcanic substrates, like those in our sites, pass through a stage dominated by amorphous non-crystalline minerals, which have an enormous surface area (Fox and Searle, 1978). The reactive surface area of minerals is a primary determinant of the size and strength of the geochemical sink for P (Parfitt, 1978; McBride, 1994).

Fig. 3. The effects of the 24 h C addition on P partitioning into (a) microbial and (b) sorbed pools measured 48 h after P addition in the lower horizon soils. Uncorrected data are shown.

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Thus these amorphous minerals have a greater capacity to sorb phosphate than the secondary crystalline clays, and consequently the greatest P sorption is observed before the secondary clays form in volcanically derived soils. Soils at the young and intermediate aged sites both contain significant amounts of these reactive amorphous minerals, while the oldest site is dominated by less reactive secondary clays. As a result, in the mineral horizon, we saw greatest sorption in the intermediate aged site, a bit less in the young site, and even less in the oldest. Differences between horizons in both sorption and microbial activity are greater than among sites. Since most available P tends to cycle through the organic horizon, the characteristics of this horizon may be important in controlling short-term P availability, while the lower horizons may be more important in longer-term retention and cycling (Wood et al., 1984). In the organic horizons, sorption remains fairly weak, and decreases with soil age as mineral content decreases, suggesting that the role of sorption in short-term cycling of available P may actually decrease as soils age and biological P demand increases. Since volcanic soils have unique mineralogical characteristics as they age, it would be interesting to see if this is a general pattern for other soils. Although placing soils into suspension could potentially be a shock to the microbes, it did not seem to have an adverse affect on P immobilization; we saw very rapid immobilization within the first 30 min after the soils were suspended. We also observed no lag in soil respiration (CO2-C flux) in hourly measurements taken after the soils were suspended (data not shown). These soils experience high rainfall, often in torrential downpours, and often retain high moisture between events—making it likely that the microbial community is accustomed to watery conditions. Both biological uptake and sorption of P are rapid processes that consume phosphate from the available soil solution pool. Sorption interferes with biological uptake of P by slowing the diffusion rate of P to areas of low concentration (Bowen and Rovira, 1966; Lewis and Quirk, 1967; Farr and Vaidyanathan, 1972; Bhat and Nye, 1973), and by directly competing with biota for available phosphate ions. In the well-mixed soil suspensions used in our study we eliminated limitation by diffusion and assessed the direct competition between sorption and microbial immobilization. The strength of these processes varied inversely here as elsewhere (Wood et al., 1984; Walbridge et al., 1991), complicating the determination of whether sorption or microbial uptake is controlling partitioning of available P. However, the combined results from all the sites suggest that microbial demand was the better competitor for available P, controlling how much P was immobilized and thus how much remained to sorb (Table 4). We found that tracer P was immobilized in all soils irrespective of P status or productivity, even though P has been found to limit primary productivity in only one of

these sites (Vitousek and Farrington, 1997). Since P supply is tightly regulated by biological and geochemical processes that keep P availability low and excess available P does not build up in soils under natural conditions, perhaps biological demand remains high. Biological release of available P is controlled by negative feedback to enzyme production, which reduces mineralization when P supply is sufficient (Speir and McGill, 1979; McGill and Cole, 1981; Olander and Vitousek, 2000). Geochemical retention also reduces P availability. When a pulse of available P that exceeds immediate biological demand enters the soil solution, what is not consumed by the biota is quickly sorbed by soil minerals. In our soils, with microbial activity suppressed, sorption consumed from 65 to 98% of a large, 100 mg P/g soil, pulse addition within 24 h (Fig. 1). Through these mechanisms P availability remains low. In addition, the covariance of P availability and primary productivity across the sites may augment the consistent biological demand and control of phosphate partitioning observed across the chronosequence. Tight regulation of available soil solution P across the chronosequence may also help explain the strong effects of long-term fertilization (Vitousek et al., 1993; Herbert and Fownes, 1995; Vitousek and Farrington, 1997). Across the sites long-term P fertilization altered leaf and leaf litter P concentrations, litter decomposition rates, and soil phosphatase activity, while N fertilization usually had a much smaller or less consistent effect (Vitousek, 1998; Olander and Vitousek, 2000). Since P tends to have a closed cycle with P availability consistently low for all chronosequence soils and P always in demand by the microbes, P fertilization affects biological processes at all sites. In contrast, N can have a relatively open cycle because sorption of N is weak and N supply may exceed demand in the older soils. As a result, N fertilization in the older sites often has little effect on biological processes (Olander and Vitousek, 2000; Vitousek et al., 1997).

Acknowledgements We thank D. Turner, C.A. Smith, and S. Allison for laboratory assistance, H. Farrington, D. Penn, Hawaii Volcanoes National Park, the Division of Forestry and Wildlife of the State of Hawaii, and the Joseph Souza Center for logistical support and/or access to field sites; P. Hanawalt and G. Spivak for laboratory access and support; O.Chadwick and M. Torn for providing data on soils; and S. Fendorf, C. Field, P. Matson, J. Verville, K. Treseder, S. Allison, B. Cade-Menun and two anonymous reviewers for discussion and helpful comments on the research and manuscript. A NSF Dissertation Improvement Grant, a NASA Earth System Fellowship, and a grant from The Andrew W. Mellon Foundation supported this research.

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