Effect of ecological engineering on the nutrient content of surface sediments in Lake Taihu, China

Effect of ecological engineering on the nutrient content of surface sediments in Lake Taihu, China

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Effect of ecological engineering on the nutrient content of surface sediments in Lake Taihu, China Yong-Xia Gao a,b , Guang-Wei Zhu a,∗ , Bo-Qiang Qin a , Yong Pang c , Zhi-Jun Gong a , Yun-Lin Zhang a a

State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 73 East Beijing Road, Nanjing 210008, Jiangsu, China b Graduate School of Chinese Academy of Sciences, Beijing 100039, China c College of Environmental Science and Engineering, Hohai University, Nanjing 210098, China

a r t i c l e

i n f o

a b s t r a c t

Article history:

Ecological engineering was carried out in Meiliang Bay of Lake Taihu beginning in 2003 in

Received 7 March 2007

order to improve water quality. There were two main objectives: to improve the growth envi-

Received in revised form

ronment for macrophytes, and to restore macrophyte assemblages. We examined surface

20 February 2008

sediments once per month beginning in April 2005 to study the response of sediment nutri-

Accepted 7 July 2008

ent content to the ecological engineering. Average total nitrogen (TN) and total phosphorus (TP) concentrations in the surface sediments were 7043 and 1370 mg kg−1 , respectively, in May 2005, while after 1 year, TN concentration was reduced to 2929 mg kg−1 and TP concen-

Keywords:

tration was reduced to 352 mg kg−1 . We conclude that ecological engineering can lower the

Ecological engineering

nutrient content in surface sediments when it is used to improve water quality.

Surface sediments

© 2008 Elsevier B.V. All rights reserved.

Nitrogen Phosphorus Internal pollution

1.

Introduction

Multiple stable states occur when more than one type of community can stably persist in a single environmental regime, while two-species competitive interaction is characterized by unstable coexistence (Knowlton, 1992). The alternative stable states theory is commonly applied to aquatic ecosystems such as shallow lakes, which may be dominated alternately by macrophytes or phytoplankton, under clear water and eutrophic conditions, respectively (Davis et al., 2003). The theory predicts that high nutrient concentrations increase the probability of shallow lakes switching from a state dominated by macrophytes to one dominated by phytoplankton



Corresponding author. Tel.: +86 25 8688 2186; fax: +86 25 5771 4759. E-mail address: [email protected] (G.-W. Zhu). 0925-8574/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2008.07.002

(Morris et al., 2003). A clear-water state is most often observed in lakes with high cover of submerged vegetation, because macrophytes play an important role in stabilizing and maintaining the clear-water state (Mjelde and Faafeng, 1997). In shallow eutrophic lakes, reduction of nutrient concentrations as the sole method of restoration may not give ideal results. However, bio-manipulation as an additional measure can be highly effective, provided that nutrients have been sufficiently reduced to allow the existence of a stable clear-water equilibrium (Scheffer, 1990). Lake Taihu has a surface area of 2338 km2 , mean depth of 2.6 m, and is located in the Yangtze River Delta (Qin et al., 2004). The volume of Lake Taihu is 4.4 billion m3 , 70% of which is supplied by the Tiaoxi River in the southwest

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and the Nanxi River in the west. About 60–70% of its outflow goes into the Taipu River through eastern Lake Taihu, which connects the East China Sea via the Huangpu River (Sun and Huang, 1993). Therefore, the retention time in southern Lake Taihu is much shorter than in the north, which may be one of the causes of poor water quality in northern Lake Taihu (Qin et al., 2006). Meiliang Bay is located in the north of Lake Taihu with an area of 110 km2 , and is phytoplanktondominated. Since 1990, research monitoring has documented cyanobacteria blooms in the northwestern part of the lake including Meiliang Bay between May and October, particularly in July and August (Wang and Dou, 1998). In order to switch from the phytoplankton-dominated state to one dominated by macrophytes, thus ensuring drinking water safety, ecological engineering was undertaken in Meiliang Bay in 2003, covering an area of 4 km2 within the water resource protection region (7 km2 ) near the Qianlongkou water supply plant. Knowledge about ecological engineering in large shallow lakes is generally lacking, and most previous lake restorations have used wetlands and marshes for nutrient uptake (Mitsch and Wang, 2000; Pietro et al., 2006; Kadlec, 2006; Hadad and Maine, 2007). The ecological engineering in Meiliang Bay of Lake Taihu was based on the multiple stable states theory and included three connected phases: improving the lake condition → restoring aquatic macrophytes → transforming aquatic ecosystem from a phytoplankton-dominated state to one dominated by macrophytes. The overall objective was to improve water quality around the drinking water intake (Qin et al., 2005). Sediments play an important role in the overall nutrient dynamics of shallow lakes. In lakes where the external loading has been reduced, internal phosphorus loading may prevent improvements in lake water quality (Søndergaard et al., 2003). Therefore, lake phosphorus concentration might not decrease roughly in proportion to reductions in phosphorus input as predicted. This is due to the release of phosphorus from surface sediments (Marsden, 1989). Lake sediments are usually highly enriched compared to the overlying water, and can act as an internal source driving eutrophication and algae blooms (Pu et al., 2000). Many studies have shown that the sediments of shallow lakes are an internal pollution source (Søndergaard et al., 1992; Sfriso et al., 1995; Nixdorf and Deneke, 1997; Chmielewski et al., 1997). Taihu is a shallow lake; therefore, dynamic disturbances can release nutrients from the sediments through resuspension leading to increased concentrations of suspended solids, TN and TP in the water (Qin et al., 2006). In order to improve the water quality at Meiliang Bay, ecological engineering was undertaken in 2003. We investigated the surface sediments once per month beginning in April 2005 to study the response of sediment nutrient content to the restoration effort.

2.

Materials and methods

2.1.

Study sites

The sampling sites were located in the region of the ecological engineering (herein referred to as “engineering”) in Meiliang Bay of Lake Taihu. The engineering included two

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phases: firstly, improving the growth environment for macrophytes (herein “the structural part”) and secondly, restoring the aquatic ecosystem from a state dominated by phytoplankton into a macrophyte-dominated state (“the biological part”). The engineering is described in detail by Qin et al. (2007). The structural part included an enclosure belt to keep algae out of the engineering region and direct current, a cement stake wave dissipation belt and a bamboo raft wave dissipation belt. Wave dissipation belts can weaken wind-induced waves, thus reducing wave-induced sediment resuspension and increasing water transparency, so as to create a more stable growth environment for macrophytes. The biological part included restoring macrophytes, including floating macrophytes, floating-leaved macrophytes, emergent macrophytes and submerged macrophytes, as well as breeding and stocking filter-feeding fishes in order to graze algae. Additionally, the biological part also included large amounts of biomimetic mesh (total length is about 130,000 m) in different areas of the engineering region, especially in the area of weak windwaves in summer and autumn, intended to adsorb suspended substance, organic matter and as substrate for periphyton. Periphyton can be an important short-term sink for P (Pietro et al., 2006; McCormick et al., 2006). There is an intake of the Qianlongkou water supply plant in the engineering region (Fig. 1), surrounded by a bamboo raft wave dissipation belt (Fig. 1c), cement stake wave dissipation belt (Fig. 1b) and enclosure belt (Fig. 1a). The enclosure belt is made up of buoys, PVC fabric, a fortified band and anchors. The cement stake wave dissipation belt is made up of 9134 cement stakes (each cement stake has a size of 30 cm × 30 cm × 5 m) and is 3.6 km long. The bamboo raft wave dissipation belts have a total length of 4.5 km and are 10 m wide. The distance between the two lengths of bamboo rafts (Fig. 1c) is less than 400 m, which is effective for weakening wind-wave disturbance. Bamboo raft wave dissipation belts also provide habitat for floating macrophytes. The filter-feeding fishes silver carp (Hypophthalmichthys molitrix), bighead carp (Aristichthys nobilis), lea (freshwater mussel—Hyriopsis cumingii), and leach (Cristaria plicata) were stocked in the area between the enclosure belt and cement stake wave dissipation belt (Fig. 1). Floating macrophytes (Alternanthera philoxeroides), floating-leaved macrophytes (Trapa sp., Nymphoides peltata and Nelumbo nucifera), emergent macrophytes (Acorus calamus and Typha angustifolia) and submerged macrophytes (Patamogeton malaianus, Potamogeton maackianus, MyriophYllum verticillatum, Vallisneria spiralis, Potamogeton crispus and Elodea nuttallii) were planted in the area from the cement stake wave dissipation belt to the intake of the Qianlongkou water supply plant (Fig. 1). Floating macrophytes (A. philoxeroides) wrapped in mesh with a 2–3 cm aperture were planted on the bamboo raft wave dissipation belt. There were three planting methods for floating-leaved and submerged macrophytes: (1) seeds (Trapa sp.) were sown in the silty areas, (2) Trapa sp. was wrapped with gravel in a mesh bag, then placed in areas with harder sediments and (3) seedlings (N. peltata) were bundled with a stake, then inserted 20–50 cm deep into the thicker sediments. Emergent macrophytes were transplanted along the bank. Aquatic macrophytes have several intrinsic properties, such as stabilizing the surface of sediment beds, providing

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Fig. 1 – Location of the study sites. Note: (a) stands for enclosure belt, which is made up of buoys, PVC fabric, fortified band and anchors (from upside to downside). Enclosure belt is used mainly to keep algae out the engineering area and channel current. (b) Stands for cement stake-wave dissipation belt, which is made up of 9134 cement stakes (each cement stake has a size of 30 cm × 30 cm × 5 m) and is 3.6 km long. It is used to weaken wind-wave disturbance. (c) Stands for bamboo raft-wave dissipation belts. They have a total length of 4.5 km and are 10 m wide. The two circles of bamboo raft-wave dissipation belts have a distance of less than 400 m, which is effective for weakening wind-wave disturbance. They also offer a habitat for floating plants. The filter-feeding fishes silver carp (Hypophthalmichthys molitrix), bighead carp (Aristichthys nobilis), lea (freshwater mussel—Hyriopsis cumingii), and leach (Cristaria plicata) were stocked in the area between (a) and (b). Floating macrophytes (Alternanthera philoxeroides), floating-leaved macrophytes (Trapa, Nymphoides peltata and Nelumbo nucifera), emergent macrophytes (Acorus calamus and Typha angustifolia) and submersed macrophytes (Patamogeton malaianus, Potamogeton maackianus, MyriophYllum verticillatum, Vallisneria spiralis, Potamogeton crispus and Elodea nuttallii) were planted in the area from (b) to the intake.

good conditions for physical filtration, providing a large surface area for microbial growth, and providing habitat for other wildlife (Brix, 1994). Perhaps the most important functions here are the uptake of nutrients from sediments and lake water (Smart and Barko, 1985) and competition with

algae for resources. The effects of submerged macrophytes on nutrient cycling are most pronounced in shallow lakes (Barko et al., 1991). A study by Barko and Smart, 1980 indicated that plant tissue P concentrations were high, with few exceptions, and cumulative P released from plant shoots during the study represented less than 10% of the total P mobilized. This mobilization of sediment P by submerged macrophytes represents an important aspect of the P cycle and may affect the overall metabolism of lacustrine systems. N and P were readily mobilized from the sediments and concentrated in plant shoots at levels well above those required for growth, while considerable quantities of these nutrients can be released to the water due to plant senescence and associated decay. Harvesting and use of the plant material was planned in the ecological engineering, which is a step in the direction of a holistic solution where waste products are utilized as a resource. Filter-feeding fishes were used to reduce suspended solids and phytoplankton. The ultimate objective of the ecological engineering was to drive a complete switch from the turbid state dominated by phytoplankton to a clear state dominated by macrophytes, and to enhance the self-sustainability of the clear-water state. The 10 sampling sites (#1 to #10) are shown in Fig. 1. Site #1 is outside the enclosure belt and serves as a comparison with the sites inside the engineering region, #2 and #5 are between the enclosure belt and the cement stake wave dissipation belt, where there are filter-feeding fishes, mussels and leaches. Sites #3, #7, and #9 are among the bamboo raft wave dissipation belts where many macrophytes were planted, including Trapa sp., P. malaianus, M. verticillatum and some N. peltata, #4 and #10 are around the Qianlongkou water supply plant where P. maackianus, Potamogeton malaianus, A. philoxeroides, A. calamus, T. angustifolia, N. nucifera and some N. peltata were distributed.

2.2.

Sampling and analysis methods

Usually, 2 cm of the top-layer sediments is collected for analysis. According to Søndergaard et al. (2003), many factors are involved in the release of phosphorus, particularly important are microbial processes and redox sensitive mobilization from the anoxic zone a few millimeters or centimeters below the sediments surface. Hu et al. (2006) study on sediment resuspension in Lake Taihu also indicated that the thickness of the sediment layer that is set in motion by wind-wave-induced current is in the order of millimeters (Hu et al., 2006). Therefore, 2 cm of the top-layer sediments cannot reflect changes on a monthly time scale. In this study, we used a columnar organic glass core sampler (0.5 m long with a diameter of 52 mm) to collect sediment cores. Most overlying water in the core sampler was then carefully drawn off, leaving about 100 mL water in the sampler. The remaining water was then disturbed enough to churn up a few millimeters of the top-layer sediments, and the turbid liquid immediately transferred into 100 mL acid-rinsed polyethylene bottles for analysis of total nitrogen (TN), total phosphorus (TP) and loss on ignition (LOI). These variables were used to investigate changes in the surface sediments of the engineering region since the ecological engineering was implemented. Some samples were filtered on the spot through 0.45 ␮m pore size filtration membranes (Whatman

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GF/F) for analysis of dissolved nutrients. All samples were kept in an icebox for transport to the laboratory for analysis. In the laboratory, 25 mL of the turbid liquid samples was filtered through Whatman GF/C filtration membranes that had been previously ignited at 550 ◦ C for 3 h and weighed. The filtrate and filter were then dried at 105 ◦ C for 4 h and weighed. The weight of solid substance (SS) in the turbid liquid was determined by subtracting the final weight from the weight of the filter paper. The concentration of organic matter in the sediments was determined by loss on ignition (LOI)—the weight difference of the filtrate and filter before and after ignition at 550 ◦ C for 3 h. Samples used to analyze TN, TP, dissolved total nitrogen (DTN) and dissolved total phosphorus (DTP) were digested with alkaline potassium persulphate. TN and DTN were determined by the UV spectrophotometric method, and TP and DTP were determined using the acidic molybdate–ascorbic acid spectrophotometric method (Jin and Tu, 1990).

3.

Results and discussion

3.1. Seasonal variations of TN, TP and LOI/SS in the surface sediments The monthly investigation was carried out for one whole year beginning in April 2005. June to August 2005 was considered to be summer, September to November 2005 autumn, December 2005 to February 2006 winter, and March to May 2006 spring. Concentrations of TN, TP and organic matter percent (LOI/SS) in the surface sediments at different sampling sites can be seen in Fig. 2. Seasonal changes of TP concentration in the surface sediments were more regular than for TN. TP concentration in different seasons had the order of summer > autumn > winter > spring (Fig. 2b), and TN concentration was also highest in summer and lowest in spring (Fig. 2a). Percent organic matter of the surface sediments showed little change with season (Fig. 2c). Empirical modeling of the relative contribution of sediments and open water to the P economy of submerged macrophytes predicts that more than 50% of the supply of P is from sediments. N can be supplied to the submerged macrophytes readily from both the sediments and the open water (Barko et al., 1991), a possible reason that the change of TP concentration in the surface sediments was more regular than that of TN concentration in our study (Fig. 2). Fig. 2(a–b) shows that nutrient content in the surface sediments was reduced (Table 1), for which there are several reasons. Adsorbing of suspended substance, organic matter and periphyton by biomimetic net is one potential reason, as the biomimetic nets can adsorb suspended substance at a rate of 191.46 t a−1 SS, 6.42 t a−1 TN, and 2.52 t a−1 TP from lake water according to a regular survey in the engineering region. Harvesting macrophytes is another possible reason for the reduction in nutrient content of the surface sediments. For example, floating-leaved macrophytes brought 12.99 t TN and 1.532 t TP out of the lake in 2004, 4.78 t TN and 0.56 t TP in 2005. Floating macrophytes brought 490 kg TN and 55.5 kg TP

Fig. 2 – Concentrations of TN, TP (mg/L) and LOI/SS (%) in the surface sediments as well as chl a concentration in the overlying water. Note: The monthly investigation was carried out for one whole year beginning in April 2005. June to August 2005 was considered to be summer, September to November 2005 autumn, December 2005 to February 2006 winter, and March to May 2006 spring. In this way, (a) shows “seasonal” change of TP concentration in the surface sediments; (b) shows “seasonal” change of TN concentration in the surface sediments; (c) shows “seasonal” change of organic matter percent (LOI/SS) in the surface sediments; (d) shows “seasonal” change of chl a concentration in the overlying water.

out of the lake. Another potential reason is the filter-feeding fishes and mussels. Filter-feeding fishes consumed 2780 t a−1 algae and mussels consumed 15 t a−1 algae, thus reducing the transfer of nutrients and organic matter to the sediments. Generally speaking, macrophyte biomass in summer and autumn is greater than that of other seasons. It could, therefore, be expected that nutrient content in the surface sediments would be lowest in summer or autumn. This is contrary to the study results (Fig. 2a–b). Hadad and Maine (2007) found that total P in rooted species did not show seasonal variations. It might be that the change of nutrient content in surface sediments relied more on the effect of the ecological engineering and less on seasonal effects. After the ecological engineering was implemented, nutrient content in the surface sediments changed with time rather than with season. It is possible that increased deposition of dead algae on sediments

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Table 1 – The change of TN and TP concentrations in the surface sediments during the study period (take the concentration of May 2005 as the primary value) Sampling date

Average TN concentration (mg/kg)

Primary value (May 2005) Summer (June 2005 to August 2005) Autumn (September 2005 to November 2005) Winter (December 2005 to February 2006) Spring (March 2006 to May 2006)

during summer and autumn contributed to higher nutrient concentrations in summer and autumn. Further research will seek to resolve these questions. For all the sampling sites, LOI/SS (%) in the surface sediments showed little change with seasons (Fig. 2c). When compared with the other sampling sites, LOI/SS of #1 and #2 had lower values, 6.4 and 6.8%, respectively (#3 was 8.4%, #4 was 8.8%, #5 was 7.4%, #7 was 8.2%, and #9 was 8.2%). Organic matter in surface sediments comes mainly from benthon and planktonic debris. #1 and #2 are exposed to frequent southwestern wind and strong turbulence, which disrupt the establishment of benthon. This is most likely responsible for the lower organic fraction in surface sediments of #1 and #2. Chlorophyll a (chl a) concentration in the overlying water (Fig. 2d) had its highest values in summer and autumn—similar to TP concentration in the surface sediments (Fig. 2b). Particulate and other unavailable forms of phosphorus can be transformed into bio-available forms in the sediments (House, 2003), although the main source of nutrients to algae is the water column. Intense photosynthesis of phytoplankton increases the pH value of lake water and may in turn increase the pH value of the surface sediments, leading to enhanced P release from the sediments. The selective pump of P (but not N) from the sediments by algal blooms can accelerate phytoplankton growth, thus worsening water quality (Xie, 2006). Therefore, the reduction of TP concentration in surface sediments is significant for limiting cyanobacteria blooms. Chl a concentration was closely related to TP concentrations in autumn and spring (R2 = 0.75, p = 0.005 in spring; R2 = 0.50, p = 0.048 in autumn), while there was no correlation during the other seasons (R2 = 0.006, p = 0.853 in summer; R2 = 0.0004, p = 0.996 in winter). Therefore, it is still not clear whether there is some direct link between chl a concentration of the overlying water and TP concentration of the surface sediments.

3.2.

7043 5805 4332 4483 2929

Average TP concentration (mg/kg) 1370 1159 744 538 352

ter enable comparison between sites, we considered nutrient concentrations and OM at May 2005 as baseline concentrations, and all subsequent results were adjusted by subtracting the baseline values. Positive (+) differences mean an increase and negative (−) values means a decrease in concentration relative to initial concentration (Fig. 3). Most differences of TN, TP and OM in surface sediments of the sampling sites are negative except #1 and #2 (Fig. 3), which indicates that nutrient content and organic matter percent reduced with time over the study period. Nutrient content of the overlying water was also reduced after the ecological

Comparison among different sampling sites

In the study, we chose sampling sites in different sections of the ecological engineering. #1 was outside the enclosure belt and serves as a comparison with the other sampling sites, #2 and #5 were between the enclosure belt and the cement stake wave dissipation belt, #7 and #9 were between the cement stake wave dissipation belt and the bamboo raft wave dissipation belt, #3 and #10 were between the bamboo raft wave dissipation belts, and #4 was near the Qianlongkou water supply plant (Fig. 1). Different sampling sites had different initial nutrient contents and organic matter percent (OM) in the surface sediments, therefore, it is not appropriate to directly compare concentrations between sites. In order to bet-

Fig. 3 – Changes of TN (a), TP concentrations (b) and organic matter percent (OM) (c) in surface sediments of different sampling sites. Note: Different sampling sites had different initial nutrient contents and organic matter percent (OM) in the surface sediments, therefore, it is not appropriate to directly compare concentrations between sites. In order to better enable comparison between sites, we considered nutrient concentrations and OM at May 2005 as baseline concentrations, and all subsequent results were adjusted by subtracting the baseline values. Positive (+) differences mean an increase and negative (−) values means a decrease in concentration relative to initial concentration.

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Fig. 4 – Comparison of TN (a) and TP (b) concentrations in overlying water of different years.

engineering was carried out (Fig. 4). It can be concluded that the reduction of nutrient content in surface sediments did not lead to increase of nutrients in the overlying water. Site #4 is near the Qianlongkou water supply plant and is in the most protected area of the engineering region, which may account for the observed lowest values of nutrients and OM (Fig. 3). Sites #2 and #5 are in the same section of the engineering region, so their values were consistent (Fig. 3a and b), and the same applies to sites #9 and #10. Site #7 and #4 had very low nutrient content. No suitable explanation was found. Between sites #1 and #4, there is an enclosure belt, cement stake wave dissipation belt and bamboo raft wave dissipation belts (Fig. 1) as well as bio-manipulation. Theoretically, water quality should improve at #4 relative to #1, and this should be reflected in the surface sediments. Fig. 3 shows that nutrient content and organic matter percent in the surface sediments were indeed declining from #1 to #4 during the study period, suggesting that the ecological engineering contributed to a reduction in nutrient content and organic matter in the surface sediments (internal pollution) of Meiliang Bay.

3.3.

Comparison of same months in different years

Surface sediment nutrient concentrations in April-2006, May2006 and June-2006 were clearly lower than those of April2005, May-2005 and June-2005, and OM demonstrated a slight reduction (Fig. 5). The average TN concentration of May 2005 was 7043 mg kg−1 , while that of May 2006 was 2585 mg kg−1 . The average TP concentration of June 2005 was 1642 mg kg−1 , while that of Jun 2006 was 551 mg kg−1 . The biggest changes in nutrient content over the year were TN 4458 mg kg−1 and TP 1091 mg kg−1 , respectively. Biomimetic mesh included in the biological part of the engineering adsorbed enough suspended substance, organic matter and periphyton that it reduced the suspended substance quantity and nutrient content in the overlying water. As a result, nutrients that would normally settle down to the bottom of the lake were also reduced. The structural

Fig. 5 – (a)–(c) Comparison of nutrient content and organic matter percent (%) in surface sediments in same months of different years.

part of the engineering created a stable growth environment for macrophytes that possess an outstanding ability for assimilating nutrients from sediments, and created favorable conditions for microbial decomposition of organic matter (Brix and Schierup, 1989). Finally, macrophytes and filter-feeding animals used in the biological part of the engineering further removed nutrients out water through harvesting. Therefore, ecological measures played an important role in the reduction of nutrients contents and OM (Fig. 5).

4.

Conclusions

Ecological engineering is an effective measure for long-term improvements in water quality. The whole-year investigation results show that: (a) TN and TP concentrations in the surface sediments decreased with time, and organic matter percent (LOI/SS or OM) showed little change during the study period. Comparison among different sampling sites and comparison in the same months of adjacent years show that the nutrient content of surface sediments decreased with the implementation of the ecological engineering. (b) Chl a concentration in the overlying water was higher in summer and autumn, as was TP concentration. While chl a concentration was closely related to TP concentrations in autumn and spring (R2 > 0.7), there was no correlation during the other seasons.

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(c) Adsorption of biomimetic mesh and absorption of macrophytes were important for lowering nutrients contents in surface sediments. These results indicate that the ecological engineering in Lake Taihu did improve water quality. Furthermore, it has also had the effect of reducing the internal pollution in Meiliang Bay.

Acknowledgements This research was supported by The Key Project of Chinese Academy of Science (KZCX2-YW-419), National Natural Scientific Foundation of China (No. 40730529) and the Science and Technology Ministry of China (2002AA601011). The authors want to thank Dr. Lu Heng for his help in drawing the figure of study sites and Research Assistant Chris McBride in Department of Biological Sciences, The University of Waikato for his valuable comments and correcting English.

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