Chemical estimation of phosphorus released from hypersaline pond sediments used for brine shrimp Artemia franciscana production in the Mekong Delta

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Aquaculture 274 (2008) 275 – 280 www.elsevier.com/locate/aqua-online

Chemical estimation of phosphorus released from hypersaline pond sediments used for brine shrimp Artemia franciscana production in the Mekong Delta Chau Minh Khoi a,⁎, Vo Thi Guong a , Margriet Drouillon b , Pieter Pypers b , Roel Merckx b a

Department of Soil Science and Land Management, College of Agriculture and Applied Biological Sciences, Cantho University, 3/2 Street, Cantho City, Vietnam Division of Soil and Water Management, Department of Land Management and Economics, K.U. Leuven, Kasteelpark Arenberg 20, 3001 Heverlee, Belgium

b

Received 13 August 2007; received in revised form 26 November 2007; accepted 27 November 2007

Abstract Artemia production in the Mekong Delta of Vietnam occurs in hypersaline conditions and depends on adequate algal growth. In turn, algal proliferation mostly depends on mineral nutrients derived from pond bottom sediment. This study was carried out to evaluate chemically rapid procedures reliable to estimate the capacity of the sediment in supplying available phosphorous (P) in hypersaline Artemia ponds. To this end, sediments were sampled from Artemia ponds and artificially submerged by Instant Ocean at 70 g L− 1 salinity. The amounts of dissolved reactive P (DRP) and unreactive P (DUP) released from the sediments were analyzed during 4-day submergence. Linear and exponential regression analyses were employed to determine the correlation between the amounts of DRP released over submergence and the concentrations of P extracted by Olsen method and by shaking the soil slurry for 24 h. The results showed that the concentrations of DRP and DUP in hypersaline conditions (EC≈ 97 dS m− 1) were on average 1.5 to 3 fold higher than those in less saline conditions (EC≈ 11–23 dS m− 1) (Pb 0.001). During the early stage of submergence, the amount of DRP released from sediment after 4 days was linearly correlated with Olsen-P content in the sediment (R2 =0.64, Pb 0.001), while its relationship with DRP present in the saline extracts after a 24-h equilibration followed a logarithmic pattern (R2 =0.84, Pb 0.001). The results from this study revealed that Olsen-P and/or DRP measurements after a 24-h equilibration allow predicting the availability of P in the conditions prevailing in Artemia cultivation. © 2007 Elsevier B.V. All rights reserved. Keywords: Artemia; Algal growth; Hypersaline condition; Dissolved reactive P; Dissolved unreactive P

1. Introduction Phosphorus is frequently the most limiting nutrient for algal growth both in fresh water (Reddy et al., 1993; Huang and Hong, 1999; Kuang et al., 2004) and marine environments (Hu et al., 1989; Barak et al., 2003; Neill, 2005). The role of phosphorus in the physiology of algae is well-known (reviewed by Hooper, 1973; Agren, 2004). However, only a vague understanding of the fate of phosphorus in different aquatic environments and under variable edaphic conditions seems to exist. Rational recommendations on phosphorus management in aquatic production systems therefore remain scarce. In an aquatic system, the dissolved fractions of P consist mainly of ⁎ Corresponding author. Tel.: +84 71 835062; fax: +84 71 830814. E-mail address: [email protected] (C.M. Khoi). 0044-8486/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2007.11.039

orthophosphate (predominantly H2PO4− and HPO42− at pH of natural waters, and a small part as phosphate esters), condensed phosphates, and dissolved particulate inorganic and organic P (Van Wazer, 1973; Hens, 1999). In chemical terms, P in the water column is often defined as dissolved reactive P (DRP, biologically the most available fractions of P in the water column, including orthophosphate and some organic compounds that can pass through a specified filter pore size and reacts with an acidic molybdate solution) and total dissolved P (TDP, including DRP and the fractions of P which can be hydrolyzed by either acid or alkaline persulfate digestion to convert to DRP) (Hens, 1999; Baldwin et al., 2003). It is commonly accepted that algae and other aquatic organisms assimilate P mainly in the form of orthophosphate (Huang and Hong, 1999; Gardolinski et al., 2004). However, this information is often based on ill-understood methodology and kinetics

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of exchange between orthophosphate and other P-pools is largely unknown. Another form prevailing in aquatic systems is organic P, contributing up to 50–58% of TDP. In aquatic systems low in orthophosphate, this form of P may be released from suspended particulates (Froelich, 1988; Bjorkman and Karl, 1994; Chapman and Kimstach, 1996). In aquatic ecosystems, P is highly active both chemically and biologically, undergoing numerous transformations and continuously exchanging between the particulate and dissolved phases, between the sediment and water column, and between the biota and the abiotic environment (Mainstone and Parr, 2002). In hypersaline ponds used for Artemia cultivation, which can be considered as a closed aquatic ecosystem, the availability of P is mainly dependent on the release or regeneration of these elements from the pond bottom soil or sediment. Extremely high salinity, often exceeding 70 g L− 1, may an additional factor determining the mobility and availability of P in these systems. Our previous study showed that P is a limiting nutrient for algal growth in most of Artemia ponds in the studied region (Khoi et al., 2006). Understanding the dynamics of P and predicting its availability in the hypersaline ponds used for production of Artemia in the Mekong Delta of Vietnam is necessary since the population and density of algae is one of the key factors determining the success or failure of Artemia cyst production. The objectives of this study were therefore to: i) investigate the availability of P in hypersaline conditions similar to those prevailing in Artemia ponds. ii) determine whether some easily measurable soil properties may be used to predict the availability of P for hypersaline brine shrimp Artemia. 2. Materials and methods 2.1. Sediments Sediment samples used for this study were obtained from Artemia ponds at both the experimental station of Cantho University and the surrounding area located in Vinh Chau district, Soc Trang province, Vietnam. In general, the ponds

are used for culture of Artemia during the dry season, from February to early May, whereas in the rainy season they are used to raise other aquatic organisms or left fallow. Samples were taken before starting an Artemia cycle at a depth between 0 and 5 cm below the pond bottom surface, where an intense interaction between soil and overlying water can be assumed. Pond bottom soils are classified as Salic Fluvisols (Driessen et al., 2001). Sediment samples were air-dried at room temperature (28–30 °C). Visible organic residues and gravel were removed by handpicking. The air-dried soils were ground by a mortar to pass a 1-mm mesh for chemical analyses and to pass a 2-mm mesh for use in the P dynamics studies. Chemical properties of the selected sediments are presented in Table 1.

2.2. Sediment capacity in supplying P under hypersaline conditions In field conditions, it is difficult to determine the capacity of sediments in supplying P because the concentrations of P present at sampling time are controlled by the density of algae and aquatic plants or the duration of algal bloom. To overcome this problem, the capacity of the sediment to supply P under hypersaline conditions was determined in a separate study in which sediment samples were artificially submerged and the amounts of P released over time were measured. Phosphorus-free Instant Ocean (Synthetic Sea Salt manufactured by Aquarium System Inc., USA) was used to submerge sediments instead of the hypersaline water from Artemia ponds in order to avoid contaminating algae and phosphorus. Sediments were submerged at a ratio of 100 g sediment:1000 mL Instant Ocean and at a saline concentration of 70 g L− 1. Sediments were run in triplicates. In order to simulate to the practice of Artemia culture where the pond bottoms are daily raked/disturbed to feed Artemia and the above water column is continuously stirred by wind, the water column in this experiment was disturbed via a plastic tube connecting to an aeration pump. Since algal bloom corresponding to an excess of P availability often occurs at the early stage of Artemia cultivation, the amounts of DRP and TDP released from the sediments was measured at day 4 after submergence.

2.3. Effect of hypersaline conditions on P availability The effects of high salinity on P mobility and availability were investigated by submerging sediments with phosphorus-free Instant Ocean in 50-mL centrifuge bottles. Sediments were submerged at a ratio of 3:30 (w:v) and at a concentration of 70 g L− 1 salinity. In the control, sediments were submerged with deionized water at the same ratio (w:v). Determination of the equilibrium concentration of P between sediment and aqueous phases was done by end-overend shaking for 24 h at 20 °C. The suspensions were then centrifuged at 4000 rpm for 5 min, and approximately 10 mL supernatant was withdrawn for analyses of DRP and TDP. Since salinity of the water column and salt accumulation in pond bottom sediments may be different amongst Artemia ponds, the EC values of different supernatants after extraction were measured. All treatments were run in triplicate.

Table 1 Selected chemical properties of 13 sediments sampled from Artemia pond bottoms in Vinh Chau — Vietnam a Sediment codes

pHH20 (1:2.5)

EC (1:2.5) (dS m− 1)

Total N (%)

b Mineral N (mg NH4–N kg−1)

Organic C (%)

C:N

Olsen-P (mg 100 g− 1)

Total P (%P2O5)

VC-T1 VC-T2 VC-T3 VC-T4 VC-T7 VC-T9 VC-T12 VC-K VC-F0 VC-F1 VC-TK4 VC-UH2 VC-UH4

6.87 6.93 6.60 6.57 6.42 6.54 6.35 7.18 6.95 6.93 6.89 7.52 7.54

22.1 22.3 22.5 22.9 23.2 23.1 23.0 23.0 23.2 23.3 55.5 67.9 68.0

0.178 0.186 0.141 0.134 0.153 0.181 0.160 0.119 0.167 0.204 0.144 0.200 0.207

15.20 13.36 17.54 13.21 17.27 23.08 15.81 15.54 14.51 23.24 17.02 19.99 24.25

3.04 3.54 1.87 1.55 2.35 3.03 2.11 1.35 2.53 3.15 1.92 4.12 3.73

17 19 13 12 15 17 13 11 15 15 13 21 18

1.65 1.87 1.44 1.85 1.21 0.92 0.78 1.94 1.41 1.54 1.09 1.63 1.77

0.125 0.123 0.135 0.141 0.124 0.118 0.121 0.133 0.111 0.119 0.110 0.116 0.130

a The first ten sediment samples abbreviated as VC-T1…T12, K, F0, F1 were sampled at the experimental station in Vinh Chau of Cantho University. The remaining three samples VC-TK4, UH2 and UH4 were sampled from the farmer's ponds. b Mineral N includes only NH4–N because NO3–N was not detected in the pond sediments.

C.M. Khoi et al. / Aquaculture 274 (2008) 275–280 Table 2 The accumulated concentrations of DRP, DUP and TDP in the water column during 4-day submergence under continuously air supplied conditions (n = 3) Sediments

DRP (mg P L− 1)

TDP (mg P L− 1)

a

DUP (mg P L− 1)

DRP/TDP (%)

VC-T1 VC-T2 VC-T3 VC-T4 VC-T7 VC-T9 VC-T12 VC-K VC-F0 VC-F1 VC-TK4 VC-UH2 VC-UH4 b SED

0.0685 0.0616 0.0723 0.0771 0.0522 0.0156 0.0151 0.1287 0.0646 0.0836 0.0379 0.1113 0.1383 0.0073⁎⁎⁎

0.2214 0.1783 0.1445 0.2134 0.1621 0.1208 0.1378 0.2431 0.1575 0.2363 0.1929 0.2552 0.3231 0.0273⁎⁎⁎

0.1529 0.1167 0.0722 0.1363 0.1099 0.1052 0.1227 0.1144 0.0929 0.1527 0.1550 0.1439 0.1848

31 35 50 36 32 13 11 53 41 35 20 44 43

a

DUP concentrations were calculated by the differences between TDP and DRP. SED — Standard error of differences of least squares means; ⁎⁎⁎ — significant at 0.1%.

b

2.4. Prediction of P availability Throughout this study, we assume that DRP is biologically the most available fraction of P in aquatic ecosystem as suggested in previous studies (Twist et al., 1998; Baldwin et al., 2003; Yin et al., 2004). This corresponds with many observations in natural ponds where the occurrence of algal blooms was observed together with high concentrations of DRP in the water column. In this study, we determined whether sediment Olsen-P can be a useful tool to predict P availability in hypersaline conditions since Olsen-P has been widely used as an index of soil P availability to plant (Olsen and Sommers, 1982; Mainstone and Parr, 2002). Besides, we analyzed the relationship between the amounts of DRP released from sediments during 4-day submergence and 24-h P equilibrium concentrations to evaluate whether these P forms may be an additional indicator of P availability in our aquatic system.

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2.5. P analytical methods At sampling, about 10 mL supernatant was withdrawn by a syringe fitted with a membrane filter of 0.45 μm pore size. Filtration through 0.45 μm pore size membranes is used to separate suspended particles from water samples, thereby separating between a “dissolved” or “soluble” fraction and a “particulate” fraction (Hens, 1999). The malachite green method (Hens, 1999) was used for analysis of dissolved P species in this study. The dissolved fractions of P measured by this method are in terms of DRP and are assumed to include orthophosphate and some organic compounds that are hydrolyzed in the acidic molybdate solution during color development (Hooper, 1973; Hens, 1999). The TDP concentration was measured as DRP after digesting the filtered supernatant with a mixture of H2SO4 and K2S2O8 for 30 min at 110 °C in an autoclave (Rowland and Haygarth, 1997; Hens, 1999). A further subsequent ‘cool’ digestion was carried out for samples with an appearance of brown precipitates after digestion, by adding a small amount of diluted hydrogen peroxide (≈ 10 mM). Dissolved P fractions that did not react with molybdate at low pH, but required such an additional digestion are termed dissolved unreactive P (DUP). Throughout this study, this DUP fraction is calculated as the difference in concentrations between TDP and DRP and accounts for organic and/or colloidal P species that passed the 0.45 μm sieve. In order to avoid analytical errors from interference caused by high salinity in spectro-photometric absorbance, the standard series were prepared with phosphorus-free Instant Ocean (70 g L− 1). Before being used, Instant Ocean had been filtered through Whatman no. 42 filter paper to remove all calcium carbonate formed at high pH. Similarly, the standard series used to measure DRP and TDP in the deionized water extracts were also prepared with Instant Ocean diluted at 9 g L− 1 having an EC value of 14 dS m− 1. This EC value was in the range of the EC values of the sediment water extracts. Throughout analyses, all equipments were acid washed followed with twice deionized water washes and rinsed once with deionized water prior to use.

2.6. Statistical analyses All statistical analyses were performed by SAS (SAS, Enterprise Guide 2.1, 2002). The mixed model in ANOVA analysis was used to test the significance of differences in DRP and DUP released from sediments during submergence. This model was also applied to test the effects of high salinity on DRP and DUP availability. Linear and exponential regression analyses were employed to determine the relationship between sediment Olsen-P or 24-h equilibrium

Table 3 Mean values of pH, EC, and concentrations of DRP, DUP, TDP (n = 3) in saline or water extracts from 13 Artemia pond sediments, equilibrated during 24-h shaking Sediments

VC-T1 VC-T2 VC-T3 VC-T4 VC-T7 VC-T9 VC-T12 VC-K VC-F0 VC-F1 VC-TK4 VC-UH2 VC-UH4 b SED a

Saline extracts

Deionized water extracts

a

EC (dS m− 1)

DRP (mg L− 1)

DUP (mg L− 1)

TDP (mg L− 1)

DRP/TDP (%)

EC (dS m− 1)

DRP (mg L− 1)

DUP (mg L− 1)

TDP (mg L− 1)

DRP/TDP (%)

88 90 89 90 90 88 87 88 90 88 91 84 94

0.0170 0.0168 0.0345 0.0530 0.0165 0.0072 0.0055 0.1090 0.0129 0.0487 0.0137 0.0537 0.2820 0.0019⁎⁎⁎

0.0725 0.0478 0.0486 0.0502 0.0457 0.0370 0.0413 0.0352 0.0672 0.0459 0.0649 0.0375 0.0727 0.0078⁎⁎⁎

0.0895 0.0646 0.0831 0.1032 0.0623 0.0443 0.0468 0.1442 0.0801 0.0946 0.0786 0.0912 0.3547 0.0074⁎⁎⁎

19 26 42 51 27 16 12 76 16 51 17 59 80

14.1 15.0 14.2 14.5 15.7 11.2 11.2 11.0 15.1 13.0 18.6 18.1 22.6

0.0111 0.0070 0.0127 0.0182 0.0058 nd nd 0.0422 0.0070 0.0196 0.0060 0.0329 0.1138 0.0008⁎⁎⁎

0.0113 0.0005 0.0000 0.0014 0.0017 nd nd 0.0000 0.0120 0.0057 0.0001 0.0052 0.0057 0.0046⁎⁎

0.0225 0.0075 0.0122 0.0196 0.0075 0.0117 0.0012 0.0442 0.0191 0.0253 0.0062 0.0381 0.1195 0.0047⁎⁎⁎

50 93 – 93 77 – – 95 37 78 98 86 95

EC was measured in a composite sample of three replicates and could not be statistically analyzed. SED — Standard error of differences of least squares means; ⁎⁎ — significant at 1%; ⁎⁎⁎ — significant at 0.1%. nd — not determined (DRP concentrations were below detection limit).

b

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P measurements and the amounts of DRP and TDP released from sediments over 4-day submergence under hypersaline conditions.

3. Results 3.1. Sediment characteristics The pond sediments used in this study varied widely in their composition, as indicated by total organic C concentrations ranging from 1.35 to 4.12%, total N contents varying from 0.119 to 0.207% and inorganic N concentrations ranging from 13.2 to 24.3 mg N kg− 1. The concentrations of total P in these sediments ranged from 0.111 to 0.141% P2O5 and are low in general. Olsen-P varied from 0.78 to 1.94 mg P 100 g− 1. Sediments VC-T2, VC-F1, VC-UH2 and VC-UH4 with high organic C contents are also rich in total N and inorganic N concentrations. In contrast, sediment VC-K was poor in organic C and total N but relatively rich in Olsen-P. Different concentrations in sediment organic C, total N, mineral N and Olsen-P reflect differences in topography, level of sea sediment build-up or management history of the ponds. Most sediment samples were nearly neutral, with pH values between 6.35 and 6.95. Exceptionally, sediments VC-K, VC-UH2 and VC-UH4 are slightly alkaline. EC values of these sediments were high, ranging from 22 to 68 dS m− 1. Both the high values of pH and EC reflect extremely high salt accumulation in these studied sediments (Table 1). 3.2. P-supply from sediments and P availability under hypersaline condition After four days of submergence under continuous air-supply, the concentrations of TDP varied from 0.138 to 0.323 mg P L− 1. The concentrations of DRP ranged from 0.015 to 0.138 mg P L− 1, accounting from 11 to 53% of TDP (Table 2). The deionized water and the Instant Ocean solution used to extract P had pH 6.2, EC 1.9 × 10− 3 dS m− 1 and pH 7.9, EC 97 dS m− 1, respectively. Shaking sediments with highly saline water for 24 h resulted in a significantly higher release of DRP as compared to those in deionized water extracts. The concentrations of DRP under high salinity widely varied, ranging from 0.0055 to 0.28 mg L− 1 and were 1.5 to 2 fold above the concentrations of DRP in the extracts performed with deionized water (P b 0.001). Also, DUP fractions were substantially smaller when soils were extracted by water compared to those extracted by saline solution (Table 3). Apparently, salinity had a more dramatic effect on the extractability of DUP than of DRP. Saline on average extracted 1.5 to 2

times more DRP than deionized water, while for DUP, at least 5 times more was extracted with saline than with deionized water. After 24-h shaking, there was a slight increase in EC of sediment: water extracts, ranging from 11 to 23 dS m− 1. The increase in EC in sediment:water extracts reflected the large accumulation of salts in these sediments at sampling. In sediment:saline extracts, EC values decreased only slightly after extraction, ranging from 84 to 94 dS m− 1 (Table 3). 3.3. Relationships between DRP and Olsen-P or 24-h equilibrium P In this study, we found that the amounts of DRP released from sediments in hypersaline and disturbed aquatic ecosystems significantly correlated with sediment Olsen-P and the DRP after 24-h shaking, with R2 = 0.64 (P b 0.001) and R2 = 0.84 (P b 0.001), respectively. While the relationship between the amounts of diffused DRP and Olsen-P can be described by a linear regression [DRP = (0.084 × Olsen-P) − 0.052], their relationship with the 24-h equilibrium DRP followed a logarithmic pattern [DRP = 0.032 × Ln(DRP released after 24-h shaking) + 0.187) (Fig. 1).

4. Discussion The availability of P in aquatic systems is controlled by a multitude of simultaneous processes such as precipitation/dissolution, adsorption/desorption and immobilization/mineralization. In recent years, many studies have established a quantitative comparison of P dynamics in fresh water versus marine ecosystems. However, the conclusions on how salinity affects P dynamics are contradictory. In marine ecosystems, the limited availability of P has repeatedly been mentioned. Salinity along with high pH in seawater stimulates the oxidation and hydrolysis of iron and aluminum and results in an occlusion of P in Fe/Al precipitates. Paludan and Morris (1999) and Gunnars et al. (2002) observed that the precipitation processes involving dissolved P complexes and Fe/Al oxides occur when salt water is mixed with nutrient rich freshwater. Similarly, precipitation of P together with calcium carbonate is well-known to occur at high pH in seawater (Bostan et al., 2000; Mainstone and Parr, 2002; Coelho et al., 2004). On the other hand, increasing salinity is also reported to entail an increase in P availability. Lau and Chu (1999) found that an increase in salinity from 5 to 15 g L− 1 resulted in an increase in

Fig. 1. The relationship between DRP diffused during 4 days under conditions of continuous air-supply and the mean concentrations of Olsen-P (n = 2) and DRP equilibrated during 24-h shaking (n = 3).

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orthophosphate released from the sediment, under warm conditions (28 °C). Similarly, Gardolinski et al. (2004) found that rapid releases of filterable P occurred at salinities of ≥10 g L− 1, and of this, nearly half was present as filterable organic P, which subsequently underwent rapid mineralization to filterable reactive P. In our experiment, extremely high salinity has a positive effect on both DRP and DUP concentrations in which DUP was more strongly affected than DRP. Higher P mobility and availability resulted from high salinity in this study can be explained by a convergence of both high ionic strength and high pH value of the extractant. High ionic strength resulted in phenomena as i) ligand exchange of SO42− and Cl− and/or OH− for HPO42− on the ironoxyhydroxides surfaces (Gardolinski et al., 2004; Suzumura et al., 2004; Karthikeyan et al., 2004) and ii) the release of dissolved organic P through the lysis of sediment bacteria (Fox, 1983; Gardolinski et al., 2004). On the other hand, high pH may prevent phosphate sorption on iron-oxyhydroxides by changing the surface charge on the iron-oxyhydroxides (Lebo, 1991; Zwolsman, 1994), meanwhile shifting the speciation of phosphate from H2PO4− to HPO42− (Coelho et al., 2004; Karthikeyan et al., 2004). This study indicated that the capacity of sediments to supply P in hypersaline Artemia ponds can be reasonably estimated by the concentrations of sediment Olsen-P or the amounts of equilibrated DRP after 24-h shaking. Although there was higher correlation between the released DRP and the 24-h equilibrium P, analyzing sediment Olsen-P to predict DRP in the water column is preferably recommended because this procedure takes less turnaround time. 5. Conclusion Although the mobility and availability of P in the water column are controlled by a myriad of physical–chemical reactions and biological processes, there were more DRP and DUP released from the pond sediments submerged under extremely high salinity compared to those in less saline conditions. In practice of Artemia culture, the accumulation of dissolved P in the water column during the early stage of submergence can be reliably predicted by simple analyses of sediment Olsen-P or DRP concentrations during 24-h equilibration. Acknowledgement This study was supported by the Institutional University Collaboration programme of the Flemish Interuniversity Council (VLIR). We specially thank Prof. Patrick Sorgeloos from Gent University for his never-ending support and valuable advices during the entire period of the project. We are grateful to Dr. N.V. Hoa and N.T.H. Van from the College of Aquaculture and Fisheries — Cantho University for their professional advices. We also thank the staffs and farmers at the experimental station in Vinh Chau for their technical assistance. References Agren, G.I., 2004. The C:N:P stoichiometry of autotrophs — theory and observations. Ecology Letters 7, 185–191.

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Baldwin, D.S., Whittington, J., Oliver, R., 2003. Temporal variability of dissolved P speciation in a eutrophic reservoir — implications for predicating algal growth. Water Research 37, 4595–4598. Barak, Y., Cytryn, E., Gelfand, I., Krom, M., van Rijn, J., 2003. Phosphorus removal in a marine prototype, recirculating aquaculture system. Aquaculture 220, 313–326. Bjorkman, K., Karl, D.M., 1994. Bioavailability of inorganic and organic phosphorus compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Marine Ecology. Progress Series 111, 265–273. Bostan, V., Dominik, J., Bostina, M., Pardos, M., 2000. Forms of particulate phosphorus in suspension and in bottom sediment in the Danube Delta. Lakes and Reservoirs: Research and Management 5, 105–110. Chapman, D., Kimstach, V., 1996. Selection of water quality variables. In: Chapman, D. (Ed.), Water quality assessments, pp. 51–119. Coelho, J.P., Flindt, M.R., Jensen, H.S., Lillebo, A.I., Pardal, M.A., 2004. Phosphorus speciation and availability in intertidal sediments of a temperate estuary: relation to eutrophication and annual P-fluxes. Estuarine, Coastal and Shelf Science 61, 583–590. Driessen, P., Deckers, J., Spaargaren, O., Machtergacle, F., 2001. Lecture notes on the major soils of the world. World Soil Resources Reports, vol. 94. FAO, Rome. 334 pp. Fox, L.E., 1983. The removal of dissolved humic acid during estuarine mixing. Estuarine, Coastal and Shelf Science 16, 431–440. Froelich, P.N., 1988. Kinetic control of dissolved phosphate in natural rivers and estuaries: a primer on the phosphate buffer mechanism. Limnology and Oceanography 33, 649–668. Gardolinski, P.C.F.C., Worsfold, P.J., McKelvie, I.D., 2004. Seawater induced release and transformation of organic and inorganic phosphorus from river sediments. Water Research 38, 688–692. Gunnars, A., Blomqvist, S., Johansson, P., Andersson, C., 2002. Formation of Fe(III) oxyhydroxide colloids in freshwater and brackish seawater, with incorporation of phosphate and calcium. Geochimica et Cosmochimica Acta 66 (5), 745–758. Hens, M., 1999. Aqueous phase speciation of phosphorus in sandy soils. PhD. Thesis. Katholieke Universiteit Leuven, Leuven, Belgium. Hooper, F.F., 1973. Origin and fate of organic phosphorus compounds in aquatic systems. In: Griffith, E.J., Beeton, A., Spencer, J.M., Mitchell, D.T. (Eds.), Environmental Phosphorus Handbook. John Wiley & Sons, Inc., pp. 179–201. Hu, M.H., Yang, Y.P., Harrision, P.J., 1989. Limitation of phosphate on phytoplankton growth in Yangtze River estuary. Acta Oceanologia Sinica 11, 439–443. Huang, B., Hong, H., 1999. Alkaline phosphatase activity and utilization of dissolved organic phosphorus by algae in subtropical coastal waters. Marine Pollution Bulletin 39 (1–12), 205–211. Karthikeyan, K.G., Tshabalana, M.A., Wang, D., Kalbasi, M., 2004. Solution chemistry effects on orthophosphate adsorption by cationized solid wood residues. Environmental Science & Technology 38, 901–911. Khoi, C.M., Guong, V.T., Merckx, R., 2006. Growth of the diatom Chaetoceros calcitrans in sediment extracts from Artemia franciscana ponds at different concentrations of nitrogen and phosphorus. Aquaculture 259, 354–364. Kuang, Q., Bi, Y., Xia, Y., Hu, Z., 2004. Phytoplankton community and algal growth potential in Taipinghu Reservoir, Anhui Province, China. Lakes and Reservoirs, Research and Management 9, 119–124. Lau, S.S.S., Chu, L.M., 1999. Contaminant release from sediments in a coastal wetland. Water Research 33 (4), 909–918. Lebo, M.E., 1991. Particle-bound phosphorus along an urbanized coastal plain estuary. Marine Chemistry 34, 225–246. Mainstone, C.P., Parr, W., 2002. Phosphorus in rivers — ecology and management. The Science of the Total Environment 282–283, 25–47. Neill, M., 2005. A method to determine which nutrient is limiting for plant growth in estuarine waters—at any salinity. Marine Pollution Bulletin 1–11. Olsen, S.R., Sommers, L.E., 1982. Phosphorus. Methods of Soil Analysis, Part 2, Chemical and Microbiological Properties — Agronomy Monograph no. 9, 2nd Edition, pp. 403–427. Paludan, C., Morris, J.T., 1999. Distribution and speciation of phosphorus along a salinity gradient in intertidal marsh sediments. Biogeochemistry 45, 197–221.

280

C.M. Khoi et al. / Aquaculture 274 (2008) 275–280

Reddy, K.R., DeLaune, R.D., DeBusk, W.F., Koch, M.S., 1993. Long-term nutrient accumulation rates in the everglades. Soil Science Society of America Journal 57, 1147–1155. Rowland, A.P., Haygarth, P.M., 1997. Determination of total dissolved phosphorus in soil solutions. Journal of Environmental Quality 26, 410–415. Suzumura, M., Kokubun, H., Arata, N., 2004. Distribution and characteristics of suspended particulate matter in a heavy eutrophic estuary, Tokyo Bay, Japan. Marine Pollution Bulletin 49, 496–503. Twist, H., Edwards, A.C., Codd, G.A., 1998. Algal growth responses to waters of contrasting tributaries of the river Dee, North-East Scotland. Water Research 32 (8), 2471–2479.

Van Wazer, J.R., 1973. The compounds of phosphorus. In: Griffith, E.J., Beeton, A., Spencer, J.M., Mitchell, D.T. (Eds.), Environmental Phosphorus Handbook. John Wiley & Sons, Inc., pp. 169–177. Yin, K., Song, X., Sun, J., Wu, M.C.S., 2004. Potential P limitation leads to excess N in the Pearl River estuarine coastal plume. Continental Shelf Research 24, 1895–1907. Zwolsman, J.J.G., 1994. Seasonal variability and biogeochemistry of phosphorus in the Scheldt Estuary, South-west Netherlands. Estuarine, Coastal and Shelf Science 39, 227–248.