Effects of benthic algae on release of soluble reactive phosphorus from sediments: a radioisotope tracing study

* Corresponding author.



Effects of benthic algae on release of soluble reactive phosphorus from sediments: a radioisotope tracing study

Xiu-feng Zhanga,Xue-ying Meia,b,*

aDepartment of Ecology and Institute of Hydrobiology,Jinan University,Guangzhou 510632,PR ChinabCollege of Resources and Environment,Anhui Agricultural University,Hefei 230036,PR China

Received 10 December 2013; accepted 17 March 2015 Available online 6 May 2015

如其反是，則星辰凌犯，彗孛衝破，遂生刀兵，水旱流離，凶虋以致，死亡兆庶也。（《太上說玄天大聖真武本傳神呪妙經註》卷一，《中华道藏》30/532）

* Corresponding author.

Abstract

To evaluate the effect of benthic algae on soluble reactive phosphorus (SRP)release from sediments in shallow lakes,experiments on SRP release with and without benthic algae in sediment cores and an experiment on SRP uptake by benthic algae were conducted using the radioisotope (32P)tracing method.The dissolved oxygen (DO)concentration in sediment cores was also investigated.The results show that benthic algae effectively reduce the release of SRP from sediments to overlying water.The uptake of SRP by benthic algae,which is the direct way in which benthic algae affect the SRP release from sediments,is low in filtered water and increases with the SRP concentration.However,in the experiment,the increased uptake rate lasted for a short time (in one hour),and after that it returned to a low rate.Benthic algae make the DO concentration and the oxic layer thickness increased,which can indirectly reduce the SRP release from sediments.These findings indicate that benthic algae can reduce the SRP release from sediments in both direct and indirect ways.It seems that the indirect way also plays an important role in reducing the SRP release from sediments.©2015 Hohai University.Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords:Sediment; Benthic algae; Soluble reactive phosphorus release; Soluble reactive phosphorus uptake; Shallow lake

This work was supported by the National Natural Science Foundation of China (Grant No.31100339)and the Special Program of the China Postdoctoral Science Foundation (Grant No.2012T50494).

E-mail address: qxxmxy@163.com (Xue-ying Mei).Peer review under responsibility of Hohai University.

实例工程位于福建省泉州港秀涂港区。码头建设面积约56000m2，共设置6个散货泊位、2个件杂货泊位和2个待泊泊位。码头采用钢管板桩结构，码头当涂高度21m，钢管桩直径2m，壁厚0.02m，码头设计荷载为150kN/m2。码头典型断面图见图1。

http://dx.doi.org/10.1016/j.wse.2015.04.008

The32P activity was almost at the same level in the control group and in the uptake treatment group (p > 0.05),suggesting that little SRP was directly taken up by benthic algae.Compared with the32P activity in the control group,the32P activity in the uptake treatment group with high SRP concentration significantly decreased (p < 0.05),with a decrease rate of 14% in the first hour (Fig.2).However,the decrease rate did not change much with time.After three hours,the32P activity in the water was still at the same level.

1.Introduction

In shallow lakes,sediments play an important role in determining water quality due to the fact that a unit volume of water with a larger amount of sediment has a larger sediment surface.Internal release from sediments can maintain high nutrient levels in water even after dramatic reductions in external loading (van der Molen and Boers,1994; Søndergaard et al.,2003).Phosphorus (P)in sediments,especially soluble reactive phosphorus (SRP),is significant to the internal release of nutrients in shallow lakes (Holdren and Armstrong,1986).The SRP release in shallow lakes must be considered because it will considerablyaffect pelagic algae production (Søndergaard et al.,2003; Smolders et al.,2006).

Benthic algae can affect the SRP release from sediments in shallowlakesindirectandindirectways(Dodds,2003;Tylerand McGlathery,2003).Benthic algae can take up SRP from sediments and reduce the SRP release from sediments (Stevenson and Stoermer,1982; McCormick and O'Dell,1996),which is the direct way in which the SRP release from sediments is affected.Benthicalgaecanalsoindirectlyreducethe SRPrelease from sediments by altering biogeochemical conditions of sediments,suchasthedissolvedoxygen(DO),becauseofthe algae's location above the sediments.The oxygen produced by benthic algae during the photosynthetic process causes an increased conversion of the Fe2þions to Fe3þions in sediments,which forms an insoluble compound with phosphate ions.As a result,theSRPreleasefromsedimentsisreduced(Dodds,2003;Carlton and Wetzel,1988).In previous studies,sediments withoutbenthic algae activity have been observed to exhibit a P release rate of 1 mg/(m2$d),whereas those with benthic algal activity have been observed to exhibit a P release rate of 0.1 mg/(m2$d)(van Luijn et al.,1995).

Although numerous studies of the effect of benthic algae on the nutrient cycle in sediments and water have been conducted (Dalsgaard,2003; Tyler and McGlathery,2003; Koschorreck et al.,2007; Spears et al.,2008),and the effect of benthic algae on P release from sediments has been examined (Zhang et al.,2013),few investigations on the effect of benthic algae,grown directly on the sediment surface,on the SRP release from sediments have been conducted.The direct and indirect effects of benthic algae on the release of SRP from sediments have not been well studied,but an understanding of these phenomena would be beneficial to planning for environmental protection relating to P control.Quantitatively separating the processes of benthic algae directly and indirectly affecting the SRP release from sediments using traditional methods is extremely difficult,as they occur simultaneously and at very small scales (Poulíckova et al.,2008).

A carrier-free32P radiotracer,in the form ofoffers a sensitive marker of the32P activity that can be used to demonstrate the P cycle in the aquatic ecosystem (Noe et al.,2003).In this study,experiments on SRP release with and without benthic algae in sediment cores and an experiment on SRP uptake by benthic algae were conducted.A32P radiotracer was used to evaluate the SRP release from sediments and the uptake of SRP by benthic algae.The direct and indirect effects of benthic algae on SRP release from sediments in shallow lakes could thereby be evaluated.

将新鲜的油梨剖去核取果肉称量，置于一定量的护色液中水浴恒温80 ℃浸泡10 min，然后连同护色液打浆，按配方添加白砂糖、柠檬酸、稳定剂、蒸馏水进行调配，再通过均质机均质，灌装密封，巴氏杀菌，冷却成品[7-8]。同时用蒸馏水代替护色液作空白试验。

2.Experimental setup

2.1.Description of sampling lake

合作小组组长不仅要有管理，还要有示范。既然是示范，就要有一定标准。为此，我要求小亮做3个工作：一是对自己进行“全身体检”，检查自己存在哪些问题，必要时做全面整改；二是密切注意其他3位成员的表现，在看得见的地方，不能做得比他们差；三是做人做事要有底线，不能突破底线。

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Sediment and water samples were collected from the center of Nanhu Lake,a sub-lake of Huizhou West Lake,which is located in Huizhou City,Guangdong Province,in South China.The lake covers an area of about 120 000 m2,with an average depth of 1.5 m.The average concentrations of chlorophyll a (Chl a),total phosphorus (TP),and total nitrogen (TN)in the lake are 6.1 mg/L,0.023 mg/L,and 0.531 mg/L,respectively.The concentration of SRP in the lake water is very low and exceeds the limit of detection.The depth of sediments in the lake is about 20e50 cm.The TP concentration in sediments was 1.047 mg/g in dry weight and the TN concentration in sediments was 1.883 mg/g in dry weight during the study period.In the pore water of sediments,the concentrations of TP and SRP were 0.683 mg/L and 0.015 mg/L,respectively.

2.2.Sediment and water sampling

Twelve sediment samples were collected by hand on March 24,2010 from the center of Nanhu Lake,using perspex core tubes with lengths of 15 cm and internal diameters of 6.5 cm.Each perspex core tube had an injection hole at 4 cm from the bottom,whose diameter was 5 mm.The sediment core samples,with overlying water,were about 10 cm in thickness.All the perspex core tubes were immediately sealed at the top and bottom with silicone rubber bungs to keep the sediment structure intact.These tubes were then placed into boxes with ice and transported to the laboratory in Jinan University.The bungs on the top of the perspex core tubes were immediately removed when they arrived at the laboratory to allow the gas in the tubes to be exchanged with air.Overlying water in the sediment cores was siphoned from the tubes in order to regulate the thickness of sediment cores to 5 cm from the bottom of the tube,which kept the sediment surface 1 cm above the injection hole in the tube (Zhang et al.,2013).When needed,a32P radiotracer,in the form ofwas injected into the sediments through the injection hole.One hundred and twenty five liters lake water were collected using plastic buckets from the center of Nanhu Lake for the experiments.

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2.3.Benthic algae culture

Benthic algae used in the SRP release experiment were cultured in a laboratory and grown in the twelve sediment core samples.Two-hundred milliliters of lake water were carefully poured into each sediment core tube.Four sediment cores were kept in the dark,where no benthic algae would grow.Eight sediment cores were kept in a lightedark cycle of 12 L:12 D,with an average light intensity of 15.8±9.4 mmol/(m2$s)in daytime and darkness at night,which would lead to abundant benthic algae in two weeks.After the culture of the eight sediment cores,four of these cores with benthic algae were used to measure the Chl a concentration and determine the dominant taxa.The Chl a concentration was measured after the Chl a was extracted by ethanol from the sediment cores at room temperature according to a spectrophotometrical analysis technique from Jespersen and Christoffersen (1987),and the average Chl a concentration was 86±4 mg/m2.The dominant taxa were found,using a microscope (Hu and Wei,2006),to be Oscillatoria tenuis Ag.and Navicula spp.(class Diatom).The other four sediment cores with benthic algae were combined with the four sediment cores without benthic algae to examine the effect of benthic algae on the SRP release rate from sediments.

Benthic algae used in the uptake experiment was grown on sixteenroundedplasticgauzesinaglasstank (50 cm 30 cm 40 cm)containing 50 L of lake water.The diameter of each plastic gauze was 65 mm and the mesh size was 2 2 mm; the plastic gauzes were suspended below the water surface in the glass tank and formed a substrate for algae growth.To promote algae growth,the calculated doses of 1.5 mg N,as sodium nitrate,and 0.1 mg P,as sodium dihydrogen phosphate,were added into the glass tank per liter water per week (Wolfe and Lind,2010).The water in the glass tank was kept at 30 C and in a lightedark cycle of 12 L:12 D,with an average light intensity about 100 mmol/(m2$s)in daytime and darkness at night.After four weeks,there were abundant benthic algae on the plastic gauzes.At the end of the four-week culture period,the benthic algae were transferred toanother glass tank with 50 L of lake water and cultured for another 24 h in order to adapt to the experimental water conditions.Prior to the initiation of the experiment,the algaeencrusted plastic gauzes were washed gently with lake water to remove any nutrients adhering to the surface of the algae.

After the culture period,four plastic gauzes were used to measure the Chl a concentration and three plastic gauzes were used to identify the dominant algae taxa.The Chl a concentration was 201±52 mg/m2.The dominant taxa were Oscillatoria tenuis and Lyngbya limnetica (class Cyanophyceae),and Rhizoclonium hieroglyphicum and Oedogonium spp.(class Chlorophyceae).

2.4.Experiment design

2.4.1.SRP release experiment

Eight prepared sediment cores,of which four had benthic algae and four were without benthic algae,were used to examine the effect of benthic algae on the SRP release rate from sediments.The four sediment cores without benthic algae were considered the control group.The four sediment cores with benthic algae were considered the release treatment group.All sediment cores were injected with 4through the injection hole using a syringe (Zhang et al.,2013).Thereafter,0.5 mL of water was extracted from the overlying water of each sediment core at the twelfth hour,first day,second day,third day,and seventh day to determine the32P activity.

At the seventh day,the oxidation status of sediments was examined in the daytime,with a light intensity of 15.8±9.4 mmol/(m2$s),by measuring the DO concentration in the upper sediment layer,using an Unisense microsensor (PA2000,Denmark).

2.4.2.SRP uptake experiment

Poulíckova,A.,Hasler,P.,Lysakova,M.,Spears,B.,2008.The ecology of freshwater epipelic algae: an update.Phycologia 47(5),437e450.http://dx.doi.org/10.2216/07-59.1.

2.4.3.Sample analysis

Tomeasure the32Pactivity inthewater,each0.5mLofwater sample (from the SRP release experiment and the SRP uptake experiment)was transferred to a scintillation vial containing a10mLscintillationcocktail,including5.0gof2,5-diphenyloxa zole,0.5 g of 1,4-bis (5-phenyloxazol-2-yl)benzene,1000 mL of dimethylbenzene,and 400 g of tritonX-100.The32P activity of each sample was counted for one minute using a liquid scintillation counter (Beckman Coulter Model LS6500,Inc.,Fullerton,CA),and expressed as cpm/mL (Hansson,1988).The results were corrected for a standard32P decay rate.

One-way analysis of variance (ANOVA)was performed to detect differences in the mean of32P activity in water samples from control and experimental treatments.The DO concentration of sediments in the control group and treatment groups were also analyzed.The threshold significance level (p)was 0.05 in this study.

3.Results and discussion

3.1.SRP release from sediments

A large amount of external P loads that enter shallow lakes is in particulate form,which is hardly available to algae.SRP released from sediments to water is completely available to algae.Thus,sediment release plays an important role in affecting the pollutant level and the eutrophication in shallow lakes.The results indicate that benthic algae effectively decrease the SRP release from sediments.

The32P activity in water samples in the release treatment group was lower than that in the control group (p < 0.05),indicating that less SRP released from sediments with benthic algae in the sediment cores.At the seventh day,the32P activity of the water samples in the release treatment group was 4% of that in the control group,suggesting a significant reduction in the SRP release from sediments affected by benthic algae (Fig.1).

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Fig.1.32P activity in control group and release treatment group over time in release experiment.

(3)The indirect way of oxidizing the upper layer of sediments through the photosynthesis of benthic algae plays an important role in reducing the SRP release from sediments.In addition,loss of benthic algae due to eutrophication increases the potential negative effects on water quality.

1674-2370/©2015 Hohai University.Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

The direct mode in which benthic algae reduces the SRP release from sediments is biotic uptake (Hansson,1989).SRP released from sediments can be directly sequestrated by the biotic uptake of benthic algae (Stevenson and Stoermer,1982; McCormick and O'Dell,1996).The uptake rate varies with different conditions,such as the SRP concentration,forms of available P,growth stages of benthic algae,and benthic algae biomass (Sand-Jensen,1983; Dodds,2003).In this study,little SRP was directly taken up by benthic algae when the SRP concentration was low in water,as in the control group and uptaketreatmentgroup.Atahigh SRPconcentration,more SRP was taken up by benthic algae,suggesting that the SRP uptake rate increased with the SRP concentration.However,the32P activitywasnotsignificantlydecreasedfromthefirsthourtothe third hour,indicating that SRP was quickly taken up by benthic algae (in one hour),and,after that,the uptake ratewas kept low,because the benthic algae could have been saturated with SRP.

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3.3.DO in sediments

In the SRP release experiment,the DO concentration in the release treatment group was higher than in the control group (p < 0.05)(Fig.3).The average DO concentration at 1.5 mm depth in sediment was 1.05±0.47 mg/L in the control group and 4.08±0.97 mg/L in the release treatment group.The maximal depth of the oxic layer in sediment cores was about 4.0 mm in the release treatment group and about 2.0 mm in the control group.

The indirect way that benthic algae affected the SRP release from sediments was through oxidizing the upper layer of sediments.The increased oxygen caused an increasing conversion of the Fe2þions to Fe3þions in the upper layer of sediments,which,together with phosphate ions,formed an insoluble complex.As a result,the SRP release from sediments to water was reduced.In this study,the DO concentration in sediment cores was higher in the release treatment group than in the control group and the thickness of the oxic layer was deeper in the release treatment group than in the control group,indicating that benthic algae made the DO concentration and the thickness of the oxic layer increased due to the photosynthesis.This indirectly reduced the potential release of SRP from sediments,which indicated that the indirect way also plays an important role in reducing the SRP release from sediments.

Benthic algae can rapidly respond to the changes in water quality (Gaiser,2009; Larned,2010).Given that human activities profoundly affect the global biogeochemical cycles of nutrients (Vitousek et al.,1997; Ashley et al.,2011),the loading of nutrients into aquatic ecosystems at an excessive amount can stimulate the growth of phytoplankton.The growth of phytoplankton leads to the increase of the light attenuation into water.If the light attenuation into water increases severely,light becomes a limiting factor of the growth of benthic algae (Hansson,1988).The loss of benthic algae due to eutrophication or enhanced benthic algae growth caused by restoration of eutrophic shallow lakes will markedly change the nutrient release from sediments (van Luijn et al.,1995; Vadeboncoeur et al.,2003; Zhang et al.,2015).Enhanced growth of benthic algae,in the context of eutrophic shallow lake restoration,can reduce the nutrient availability for phytoplankton and enhance the water clarity (Zhang et al.,2014),which may in turn stimulate the benthic primary production in the lake (Liboriussen and Jeppesen,2003; Vadeboncoeur et al.,2003).Consequently,benthic algae can reduce the SRP release from sediments and reinforce the oligotrophication process (Hansson,1989),indicating that benthic algae increase can serve as a measure for improving water quality.

Fig.2.32P activity in control group,uptake treatment group,and uptake treatment group with high SRP concentration over time in uptake experiment.

Fig.3.DO concentration in upper sediment layer in release experiment.

4.Conclusions

In this study,SRP release and uptake experiments were conducted,and a32P radiotracer was used to evaluate the direct and indirect effects of benthic algae on the SRP release from sediments.The following conclusions were drawn:

(1)Benthic algae could effectively reduce SRP release from sediments.At the seventh day in the SRP release experiment,the32P activity in the water of the release treatment group with benthic algae was only 4% of that in the control group.

McCormick,P.V.,O'Dell,M.B.,1996.Quantifying periphyton responses to phosphorus in the Florida Everglades: a synoptic-experimental approach.J.North Am.Benthol.Soc.15(4),450e468.

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3.2.SRP uptake by benthic algae

References

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Carlton,R.G.,Wetzel,R.G.,1988.Phosphorus flux from lake sediments: effects of epipelic algal oxygen production.Limnol.Oceanogr.33(4),562e570.http://dx.doi.org/10.4319/lo.1988.33.4.0562.

Dalsgaard,T.,2003.Benthic primary production and nutrient cycling in sediments with benthic microalgae and transient accumulation of macroalgae.Limnol.Oceanogr.48(6),2138e2150.http://dx.doi.org/10.4319/lo.2003.48.6.2138.

Dodds,W.K.,2003.The role of periphyton in phosphorus retention in shallow freshwater aquatic systems.J.Phycol.39(5),840e849.http://dx.doi.org/10.1046/j.1529-8817.2003.02081.x.

孤独症儿童和正常儿童在区分愿望任务上的成绩差异无统计学意义；孤独症儿童在区分信念和错误信念任务上的平均成绩都很低，且均显著的低于正常儿童（P值均＜0．01）。两组儿童在各任务上的平均成绩见表2。

Gaiser,E.,2009.Periphyton as an indicator of restoration in the Florida Everglades.Ecol.Indic.9(6),37e45.http://dx.doi.org/10.1016/j.ecolind.2008.08.004.

Hansson,L.A.,1988.Effects of competitive interactions on the biomass development of planktonic and periphytic algae in lakes.Limnol.Oceanogr.33(1),121e128.

Hansson,L.A.,1989.The influence of a periphytic biolayer on phosphorus exchange between substrate and water.Arch.fu¨r Hydrobiol.115,21e26.

Holdren,G.C.,Armstrong,D.E.,1986.Interstitial ion concentrations as an indicator of phosphorus release and mineral formation in lake sediments.In: Sly,P.G.,ed.,Proceedings of the Third International Symposium on Interactions Between Sediments and Water.Springer New York,New York,pp.133e147.http://dx.doi.org/10.1007/978-1-4612-4932-0_12.

Hu,H.J.,Wei,Y.X.,2006.The Freshwater Algae of China: Systematic,Taxonomy and Ecology.Science Press,Beijing,pp.79e285.

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Jespersen,A.M.,Christoffersen,K.,1987.Measurements of chlorophyll a from phytoplanktonusingethanolasextractionsolvent.Arch.fu¨r Hydrobiol.109,445e454.

Koschorreck,M.,Kleeberg,A.,Herzsprung,P.,Wendt-Potthof,K.,2007.Effects of benthic filamentous algae on the sediment-water interface in an acidic mining lake.Hydrobiologia 592(1),387e397.http://dx.doi.org/10.1007/s10750-007-0776-5.

Larned,S.T.,2010.A prospectus for periphyton: recent and future ecological research.J.North Am.Benthol.Soc.29(1),182e206.http://dx.doi.org/10.1899/08-063.1.

Liboriussen,L.,Jeppesen,E.,2003.Temporaldynamicsin epipelic,pelagicand epiphytic algal production in a clear and turbid shallow lake.Freshw.Biol.48(3),418e431.http://dx.doi.org/10.1046/j.1365-2427.2003.01018.x.

(2)In the SRP uptake experiment,large amounts of SRP were taken up by benthic algae in the first hour when the SRP concentration was high,and the decrease rate of the32P activity was 14%.However,the decrease rate did not change with time,indicating that the benthic algae were saturated with SRP in a short time.

Noe,G.B.,Scinto,L.J.,Taylor,J.,Childers,D.L.,Jones,R.D.,2003.Phosphorus cycling and partitioning in an oligotrophic Everglades wetland ecosystem: a radioisotope tracing study.Freshw.Biol.48(11),1993e2008.http://dx.doi.org/10.1046/j.1365-2427.2003.01143.x.

Benthic algae grown on plastic gauzes were used to evaluate the uptake rate of SRP with different concentrations by benthic algae.Nine perspex vessels (10 cm 10 cm 5 cm)were used in the uptake experiment,and divided equally into three groups.Filtered water was obtained by removing suspended particles from the original lake water sample through filter membranes with a pore size of 0.45 mm.For each vessel in the first group,200 mL of filtered water were added and a piece of plastic gauze without benthic algae was put in,and this experiment group was considered the control group.For each vessel in the second group,200 mL of filtered water were added and a piece of plastic gauze with benthic algae was put in,and this experiment group was considered the uptake treatment group.For each vessel in the third group,200 mL of filtered water and SRP with a concentration of 0.015 mg/L,which was the same concentration as that of the pore water in sediments,were added and a piece of plastic gauze with benthic algae was put in,and this experiment group was considered the uptake treatment group with high SRP concentration.

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综合看我国石油整个储量-产量系列各组成单元，全国第二轮战略展开提出的任务基本完成。这意味着应适时开展第三轮油气勘探的战略开拓。

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