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Aluminum Control of Phosphorus Sorption by Lake Sediments

Release of reactive (phosphate-like) phosphorus (P) from freshwater sediments represents a significant internal P source for many lakes. Hypolimnetic P release occurs under reducing conditions that cause reductive dissolution of ferric hydroxide [Fe(OH)3]. This hypolimnetic P release may be naturally low or artificially reduced by sediment with naturally high or artificially elevated concentrations of aluminum hydroxide [Al(OH)3]. We present field and laboratory data for a common extraction analysis of sediments from 43 lakes differing in trophic status, pH regime, climate, and P loading. The results indicate that a simple sequential extraction of sediment may be a useful predictor of sediment’s ability to release P. Sequential extractions of sediment P, Al, and Fe by water (H2O), bicarbonate-dithionite (BD), and NaOH (at 25 °C) showed that negligible amounts of P would be released from lake sediments during hypolimnetic anoxia if either (1) the molar AlNaOH∼25:FeBD ratio is >3 or (2) the molar AlNaOH∼25:P(H2O+BD) ratio is >25. These ratios can be used as operational targets for estimation of sediment P release potential and Al dosing of P-rich sediment to prevent hypolimnetic P release under anoxic conditions.


Introduction
Phosphorus sorption capacity of freshwater sediments has been related to concentrations of ferric oxyhydroxides or hydroxide [Fe(OH)3] and calcium carbonate (CaCO3) in high-pH lakes (1,2), and aluminum hydroxide [Al(OH)3] in noncalcareous sediments of lower pH lakes (3). Release of reactive phosphorus (P) from the sediments into the water column is of great concern because it can contribute significantly to the total in-lake pool of bioavailable P (4). Lake and coastal marine sediments, whose sorption capacities are dominated by Fe(OH)3, release P during the development of hypolimnetic anoxia that results in the reductive dissolution of Fe III solid phases and release of Fe 2+ into solution or reprecipitation as Fe II sulfide (1,5). Elevated concentrations of Al(OH)3 in the sediment can prevent P release during anoxia by adsorbing the P liberated from Fe(OH)3 (6,7). The Al(OH)3 has a high sorption capacity (8) and is stable under both oxic and anoxic conditions, provided that the sediment pH is circumneutral. Such pH conditions are produced by microbial reduction that generates alkalinity by the carbonate and sulfide buffering systems. The ability of Al(OH)3 to prevent P release from sediments during anoxia suggests the following question: What are the characteristics of sediment (e.g., concentrations of P, Fe, and Al, or ratios among them) that permit or inhibit P release?
Despite numerous shortcomings of sequential P extraction schemes (e.g., their low selectivity, readsorption of liberated P, or changes of solid phases during extraction) (2,9) they provide a rapid and inexpensive answer to the question. In this study, we use field and experimental data to show that the ratio between sediment Al and Fe hydroxide concentrations determines P release from noncalcareous sediments during reducing (low Eh) conditions.

Materials and Methods
Site Description. Data from 52 sediment samples form the basis of our hypothesis. Samples are from 43 European and North American lakes (13 alpine lakes, 8 mountain forest lakes, 6 lowland lakes, 8 mountain reservoirs, and 8 lowland reservoirs). Eighteen lakes have been acidified by atmospheric deposition and have experienced (at least episodically) elevated fluxes of Al from their watersheds (10)(11)(12). The lakes were generally studied from spring to fall turnover. The trophic status of the water bodies ranged from oligotrophic to hypereutrophic. The epilimnetic concentrations of total P ranged from 0.04 to 10 µmol L -1 and water pH from 4.5 to 8.5. The lakes covered a wide range in elevation (60-2145 m), surface area (0.2-31 500 ha), and maximum depth (1-75 m). For more detailed characteristics of the lakes, see the Supporting Information.
Sediment Sampling and Analyses. The sampling and analyses are from four studies in the 1994-2004 period. Methods and analyses varied only slightly (see Supporting Information), allowing us to reasonably compare data. The uppermost layers of 0-1 to 0-5 cm of the fresh wet sediment were used for P fractionation analyses according to Psenner and Pucsko (13). Sediment was sequentially extracted by five processes: (1) Distilled water (H2O fraction) was used to obtain loosely bound and pore-water soluble reactive P (PH2O).
(2) NaHCO3 (0.1 M) buffered 0.1 M sodium dithionite (Na2S2O4) at 40°C (BD fraction) was used to release soluble reactive PBD from Fe III oxyhydroxides under low redox conditions. (3) NaOH (1 M) at 25°C (NaOH∼25 fraction) extracted soluble reactive PNaOH∼25 from the amorphous Al(OH)3 (which dissolves due to high pH) and some Fe III oxyhydroxide that was not extracted in the BD step. This step also results in the extraction of some of the sediment organic P. (4) HCl (0.5 M) (HCl fraction) was used to release soluble reactive P associated with any calcite and apatite (PHCl). (5) NaOH (1 M) at 85°C (NaOH∼85 fraction) was used to remove refractory and other organically bound soluble reactive P (PNaOH∼85). All fractions were centrifuged at ∼1000 g for 15 min and filtered (glass-fiber filters, pore size 0.4 µm).
In the filtrate, P concentrations were determined by the molybdate method (14) or by inductively coupled plasma atomic emission spectrometry (ICP), and Al and Fe concentrations, by ICP or colorimetrically (15). Total extractable P (PTE) is the sum of the P released in all extraction steps.
Organic carbon (OC) in the sequential extracts was determined with a TOC 5000A analyzer (Shimadzu).
Sediment pH was measured directly in the wet sample. Concentrations of total phosphorus in the sediment were determined from freeze-dried subsamples after their acid digestion, either by ICP or colorimetrically (15). All chemical results reported in this paper were calculated on a dry weight sediment basis.
Laboratory Experiments. Samples of surface sediments (0-15 cm layer) were taken from the inlet and the deepest (pool) part of Jordán Reservoir (Czech Republic) in August 2001. Suspended sediment (10 g L -1 ) was mixed with a suspension of poly-aluminum chloride (10 g of Al L -1 ), with the pH adjusted to 6 with NaOH. The poly-aluminum chloride concentration was calculated so that the original concentration of total extractable Al in sediment (1.5 and 1.8 mol kg -1 in the inlet and the deepest area, respectively) was increased incrementally by addition of 0, 0.5, 0.9, 1.9, and 3.7 mol of Al kg -1 of dry sediment. After the Al addition, the suspension pH was adjusted to the original pH of 7.1. The samples were kept in the dark at 15°C, under oxic conditions (stirred in the open bottles), and at constant pH (adjusted as necessary each month) for 18 months. Finally, sequential extraction (13) was performed on wet samples, and P, Al, and Fe concentrations were determined in the five fractions described above.
A second experiment was done with surface sediments (differing in Al concentration) from two mountain forest reservoirs (Saidenbach and Neunzehnhain, Germany, April 1996). Na2HPO4 was added at final concentrations of 46 and 38 mmol kg -1 of dry sediment to the fresh sediments from Saidenbach and Neunzehnhain reservoirs, respectively, and shaken for 1 h at constant pH in the dark at 8°C. Sequential extraction (13) was then performed on both the original and spiked samples, and P, Al, and Fe concentrations were determined as described above.
Phosphorus Sorption Capacity of Sediments. Sorption capacity of sediments was measured for samples taken from all lowland reservoirs, mountain forest lakes, and three alpine lakes. Methodological details are in ref 6. In short: eight subsamples of wet sediment (containing ∼15 mg of dry matter) were shaken for 24 h at ∼25°C with 25 mL of artificial lake water containing 0-1.3 mmol of KH2PO4 L -1 at the original pH values. The equilibrium P concentrations in the water were determined as reactive P (14). The difference between P concentrations before and after the procedure was assumed to have been sorbed by the sediments. The sorption data were fitted to the linear form of the Langmuir isotherm (correlation coefficients were >0.98) and the sorption capacity (Xm) was calculated for each sample.

Results and Discussion
Fractionation Results. Total P concentrations in sediments ranged from 11 to 141 mmol kg -1 , with small differences among lake categories. The PTE concentrations (sum of soluble reactive P extracted by all steps) were 20-104% of total P. The average PTE concentrations were lowest in sediments of oligotrophic alpine and mountain forest lakes ( Figure 1).
The PH2O contributed <3% to the PTE for all sediments, regardless of lake category ( Figure 1). The PBD was 1-45% of PTE. The relative importance of the BD step increased generally with the trophic status of lakes, with PBD being highest (on average 32% of PTE) in lowland reservoirs and lowest (on average 7% of PTE) in alpine lakes. The NaOH∼25 extraction liberated 3-92% of PTE, with the lowest and highest average yields of PNaOH∼25 in sediments of lowland reservoirs (39%) and mountain forest lakes (80%), respectively. The mountain forest lakes received high terrestrial Al export from naturally and atmospherically acidified soils (12), and the PNaOH∼25 was accompanied by high Al concentrations ( Figure   1 and Figure S1 in Supporting Information). In general, high PNaOH∼25:PTE ratios (60-92%) were typical for all lakes with the epilimnetic pH < 6 and decreased linearly with pH increase between 6 and 8.5 (see Figure S2 in Supporting Information).
PHCl represented a significant fraction of PTE pool only in lowland lakes (average of 32%) and lowland reservoirs (21%) with water pH > 7. The PHCl may have been associated with CaCO3-bearing particles but was not analyzed in more detail. The NaOH∼85 extraction yielded an average of 8% of the PTE. Consequently, P extracted in the first three steps (P(H2O+BD+NaOH∼25)) included the majority (79% on average) of PTE in the sediments (Figure 1), despite the importance of the HCl and NaOH∼85 steps for Fe and Al extractions in lowland lakes and reservoirs (see Figure S1 in Supporting Information). This indicates that the P adsorption capacity of the sediments studied was predominantly associated with Fe(OH) 3 and Al(OH)3, which are mostly dissolved in the BD and NaOH∼25 steps, respectively (13).
The P(H2O+BD) fraction (sum of P extracted by the H2O and BD steps) indicates a P pool that may be potentially released from sediments under natural conditions in water bodies, as discussed below. The BD extraction simulates low Eh conditions (i.e., hypolimnetic anoxia) and leads to the reductive dissolution of Fe(OH)3 and liberation of P adsorbed to Fe(OH)3. Due to lower Eh, the BD extraction mobilizes P more efficiently than the natural processes, a fact supported by the presence of the BD-extractable P in deep anaerobic sediment of many lakes (16,17). Therefore, the P(H2O+BD) fraction represents the upper estimate of P that can be released from sediments into the water column under anoxic conditions in the hypolimnion. In contrast, the low PBD concentrations in some sediments did not necessarily mean that there was no P originally bound to Fe(OH)3. More likely, some of the P liberated in the BD extraction step may have been readsorbed by Al(OH)3. The pH ranged between 5.0 and 7.5 in the sediments, and the pH at the beginning of the BD extraction was ∼7. Changes in the solubility of Al(OH)3 are small in this pH range (18). Consequently, most of the newly and originally Al-bound P remained in the sediment during the BD extraction. This P was finally released during the NaOH∼25 extraction, which dissolved most of the amorphous Al(OH)3. Therefore, PBD and FeBD concentrations were uncorrelated (p >0.05) for the sediments studied.
Aluminum Impact on P Release from Sediments. The sediments from alpine lakes, mountain forest lakes, and mountain reservoirs had higher AlNaOH∼25 concentrations than the lowland lakes and reservoirs (see Figure S1 in Supporting Information), which caused differences in their sediment  Figure 2A). In contrast, most of the PTE was liberated in the NaOH∼25 fraction together with AlNaOH∼25 from the acidified mountain forest Plešné Lake sediment ( Figure 2B). This lake has received elevated Al inputs from the strongly acidified soils (6).
The importance of naturally high Al concentrations in the sediments on their sorption properties was also demonstrated by the experiment with sediments from mountain forest reservoirs (Table 1). Sediment from Neunzehnhain Reservoir had 5-6 times higher AlNaOH∼25 concentrations than from Saidenbach Reservoir, whereas FeBD concentrations were comparable in both reservoirs. Of the P added to the sediments, 94-96% was adsorbed, as calculated by difference. Of the adsorbed P, 96-103% was recovered as PTE. The PBD fractionation step liberated most (49-57%) of the PTE in both the original and P-spiked sediment from Saidenbach Res-ervoir. In contrast, the PNaOH∼25 fraction was the dominant form of PTE (82% and 73% in the original and P-spiked sediments, respectively) in Al-rich sediment from Neunzehnhain Reservoir.
The importance of artificially elevated Al input to the sediments on their sorption properties was demonstrated by the experiment with sediments from inlet and deepest parts of Jordán Reservoir (Figure 3). The sediment from the inlet part had most of its P extracted by the HCl step, possibly due to the presence of CaCO3. PBD was the second most important P fraction in the sediments near the inlet. The PBD fraction, however, dominated the deep water sediments in the reservoir. Concentrations of PNaOH∼25 were quantitatively insignificant in the sediments prior to the Al treatment. The Al treatment significantly affected the P sorption characteristics of both sediments. Small changes occurred in concentrations of the quantitatively insignificant PH2O and PNaOH∼85 fractions. Of the Al added, 87% (on average) was found in the NaOH∼25 fraction (data not shown here). Even the smallest Al dose (0.46 mmol kg -1 ) reduced the PBD concentrations by up to 80% and increased the PNaOH∼25 concentrations by 300-500%. A new equilibrium between PBD and PNaOH∼25 was reached at the Al dose of 0.9 mmol kg -1 ; higher Al input had no impact on the P extraction results (Figure 3).
The sediment from Jordán Reservoir is an important source of P for the water column during periods of hypolimnetic anoxia. The Al treatment increased the AlNaOH∼25 pool, and consequently, changed the sorption characteristics of Jordán sediments from those of a nonacidified lake such as Ř ímov Reservoir (Figure 2A) to those typical of an acidified lake such as Plešné Lake ( Figure 2B) and significantly reduced the amount of P extractable under anoxic conditions. Similar results were obtained in other laboratory experiments (19,20) and during lake restoration treatments with Al (21,22).
The fractionation data, as well as the experience with the Al-treated lakes (7,22), show that sediments with naturally high or elevated AlNaOH∼25 concentrations do not release P into the water column during hypolimnetic anoxia. This is the case for Plešné Lake sediment, which releases negligible

FIGURE 3. Results of P extraction analyses (13) of Al-treated sediments from near the inlet (upper panel) and deepest part (lower panel) of Jordán Reservoir (Czech Republic). Symbols are abbreviations for the individual extractions. P, reactive P; BD, bicarbonate-dithionite.
P either through BD extraction ( Figure 2B) or into the anoxic hypolimnion (6). Similarly, Amirbahman et al. (23) found, in a set of 11 oligo/mesotrophic to eutrophic lakes in Maine, that two lakes did not release P during the development of hypolimnetic anoxia, even as dissolved Fe increased substantially. The sediment of these two lakes (both oligotrophic) had relatively high proportions of AlNaOH∼25 compared to FeBD (24). Minimal release of P in the BD extraction and low release of P from anoxic sediments (despite elevated Fe 2+ concentrations above them) occurred also in AlNaOH∼25-rich sediments from mountain reservoirs (10,12). These data suggest that if AlNaOH∼25 concentrations are high, the P [liberated either from Fe(OH)3 or by microbial processes (25)] becomes bound to Al(OH)3, buried in the sediment, and withdrawn from inlake cycling. In contrast, the sediment of Ř ímov Reservoir has low AlNaOH∼25 concentrations and releases considerable P both during the BD extraction ( Figure 2A) and into the water column during hypolimnetic anoxia (26). The parallels between our fractionation and field studies [as well as recent research (27)] suggest that sediments with low P(H2O+BD) concentrations have low ability to release P into anoxic hypolimnia, and vice versa.
Even though the AlNaOH∼25 concentration affects P adsorption in noncalcareous sediments, it cannot, by itself, be used as a measure of sediment ability to release P during anoxia (see Figure 1 and Figure S1 in Supporting Information). So, at what threshold in sediment composition is the P release inhibited and what should be the target for Al dose to lakes to prevent P release?
Thresholds. Figure 4 suggests that the major threshold for the P(H2O+BD) release is the ratio between Al and Fe concentrations extracted in the first three steps of the sequential extractions. Concentrations of P(H2O+BD) extracted from sediments with (Al:Fe)(H2O+BD+NaOH∼25) molar ratios >3 were low. In contrast, many sediments with (Al: Fe)(H2O+BD+NaOH∼25) ratios <3 yielded high P(H2O+BD) concentrations. The batch experiments with sediment from Jordán Reservoir also showed that at a (Al:Fe)(H2O+BD+NaOH∼25) ratio exceeding 2-3, P release under reducing conditions ceases (Figure 4). A similar threshold as for P(H2O+BD) was observed also for total P extracted by the H2O and BD steps (TP(H2O+BD)), because P(H2O+BD) represented the dominant (75% on average) fraction of TP(H2O+BD) (data not shown).
Surprisingly, no correlation (p > 0.05) occurred between P(H2O+BD) and FeBD even for the sediments with (Al: Fe)(H2O+BD+NaOH∼25) ratios <3. Only 25% of the variability in P(H2O+BD) concentrations was explained by the (Al: Fe)(H2O+BD+NaOH∼25) ratio. For most sediments in this group, most of this variability was closely associated (p < 0.001) with concentrations of OC extracted by the H2O and BD steps (OC(H2O+BD)) ( Figure 5). Such a relationship is in concordance with models of phosphate adsorption on metal oxyhydoxides in sediments and soils (28,29). These models assume competition between OC and phosphate for available adsorption sites on Al hydroxide. The high sediment OC(H2O+BD) concentrations probably decrease P readsorption on Al(OH)3 during BD extraction. Concentrations of OC(H2O+BD) were related to concentration of total organic C (or loss on ignition) in sediments (p < 0.001), suggesting that a potential risk of P release from sediments with (Al:Fe)(H2O+BD+NaOH∼25) ratios <3 increases with the organic content of sediments. However, if AlNaOH∼25:P(H2O+BD) ratios exceeded 25 (b in Figure  5), only low P(H2O+BD) concentrations were extracted, even at high OC(H2O+BD) concentrations. Similarly, the experimental results showed that low PBD concentrations were extracted at high AlNaOH∼25:P(H2O+BD) ratios, while PBD dominated the PTE pool at the lower ratios (Table 1). We hypothesize that for AlNaOH∼25:P(H2O+BD) ratio >25, the Al(OH)3 adsorption capacity was high enough to prevent P release from anoxic sediments.
The (Al:Fe)(H2O+BD+NaOH∼25) ratio and concentrations of OC(H2O+BD) and AlNaOH∼25 together explain 64% of the variability in the observed P(H2O+BD) concentrations at (Al: Fe)(H2O+BD+NaOH∼25) ratios <3. The remaining variability may be associated with other sediment characteristics such as particle size, degree of saturation of sorption sites, or degree of crystallinity of Fe and Al hydroxides.
Aluminum Impact on Sediment Sorption Capacity. The presence of AlNaOH∼25 in the sediments affected not only their ability to release or bind P during anoxia but also their total sorption capacity. The sediment sorption capacities (Xm) averaged ((1 standard deviation) 171 ( 69, 74 ( 19, and 50 ( 40 mmol of P kg -1 for forest mountain lakes, alpine lakes, and lowland reservoirs, respectively. Concentrations of FeBD and AlNaOH∼25 explained together 79% of variability in the Xm values (see Figure S3 in Supporting Information). The FeBD  concentrations were comparable in all lake categories (with averages between 95 and 127 mmol kg -1 ). The difference in Xm was mainly associated with higher AlNaOH∼25 concentrations in mountain lakes (912 and 355 mmol kg -1 in forest and alpine lakes, respectively) and lower values in lowland reservoirs (108 mmol kg -1 ). The AlNaOH∼25 concentrations alone explained 75% of the Xm variability.
The total capacity of the sediment to bind P by both sorption and chemical bonds can be estimated as the sum of Xm and PTE, and the original percent saturation of this total binding capacity with P can be estimated as the P(TE):(Xm + PTE) ratio (30). The PTE:(Xm + PTE) ratio was 15% ( 7% for mountain forest lakes and 55% ( 25% for lowland reservoirs. This difference shows that sediment saturation with respect to P was lower in mountain lakes and their capacity to bind more P was substantially higher than that of lowland reservoirs, with low AlNaOH∼25 concentrations. McLaughlin et al. (31) showed that freshly prepared Al colloids sorb 1-2 orders of magnitude more P than crystalline gibbsite. This implies that the ability of Al-rich sediments to retain P decreases with time due to Al(OH)3 aging. Studies involving Al-treated lakes (7,22,27), however, suggest that the increased AlNaOH∼25 concentrations can elevate P sorption in sediments and prevent its repartitioning into the BD fraction for at least several decades. Implication for Lakes. The P release from Fe(OH)3 is commonly considered as a mechanism occurring in eutrophic lakes with anoxic hypolimnia (1,4), even though P release may occur even during oxic conditions (32). Some studies (2,33), however, show that even P-rich sediments may not release P during anoxia. Such results may be interpreted as arguments against Mortimer's generalization of P liberation from the reduced Fe(OH)3. Our results suggest an alternative explanation for "exceptions" from Mortimer's schemasediments that do not release P have sufficient Al(OH)3 to provide additional sorption capacity and bind P liberated from Fe(OH)3 at low Eh conditions. Association of P with Al(OH)3 in sediments is especially important in lakes with the following characteristics: (1) Alpine lakes with noncalcareous bedrock and high erosion rates in their watersheds. These lakes receive soil particles with Al oxyhydroxides, which have high P sorption capacity (30). (2) Lakes in atmospherically or naturally acidified watersheds that receive elevated terrestrial export of dissolved and particulate Al (10,12,34). If the terrestrial flux of Al is increasing as a consequence of soil acidification but that of P does not intensify, recycling of P from sediments may be reduced. The net result is oligotrophication. (3) Lakes that have undergone chemical remediation for high P concentrations by Al treatment (19,21). The efficiency of P inactivation by addition of Al, however, depends on the extent of external P load and the resulting P sedimentation (22).
Our results suggest that under anoxic conditions small P concentrations are released from sediments with Al(OH)3: Fe(OH)3 molar ratios >3. The Al(OH)3:Fe(OH)3 ratio can be simply estimated as the ratio between Al and Fe extracted by the first three steps of the extraction method of Psenner and Pucsko (13). Alternatively, the AlNaOH∼25:FeBD ratio can be used, because the NaOH∼25-extractable Al and BDextractable Fe represent the dominant forms among the first three extractions (see Figure S1 in Supporting Information). At Al(OH)3:Fe(OH)3 molar ratios <3, P release from anoxic sediments is low provided the AlNaOH∼25:P(H2O+BD) ratio is >25. These ratios may be used as simple operational predictors of sediment's ability to release P under reducing conditions and an appropriate in-lake measure for estimation of the sediment P release potential (35). The fractionation experiments were, however, performed with 0-1 to 0-5 cm sediment layers and 1 M NaOH. The use of 0.1 M NaOH (common in other extraction schemes) may provide lower AlNaOH∼25 concentrations, which would likely increase the necessary threshold ratios somewhat. Moreover, the direct implication for natural conditions should be better based on extraction of surface sediment to better describe chemical conditions at the sediment-water interface. Surface sediments may yield slightly different results than the 0-5 cm layer, due to diagenesis and steep chemical gradients in the upper layers (10,17,36). An unanswered question is the effectiveness of Al(OH)3 in limiting diffusion and release of organic P compounds, concentrations of which are quantitatively important during early diagenesis (37)(38)(39).