Environmental Changes in Chaohu Lake (Southeast, China) Since the Mid 20Th Century: the Interactive Impacts of Nutrients, Hydrology and Climate

Limnologica 43 (2013) 10–17

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Limnologica

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Environmental changes in Chaohu Lake (southeast, China) since the mid 20th century: The interactive impacts of nutrients, hydrology and climate

Xu Chen a,b, Xiangdong Yang a,∗, Xuhui Dong a, Enfeng Liu a a State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing 210008, People’s Republic of China b Faculty of Earth Sciences, China University of Geosciences, Wuhan 430074, People’s Republic of China article info abstract

Article history: Chaohu Lake, the fifth largest freshwater lake in the Yangtze floodplain, is faced with multiple stresses Received 21 June 2011 from anthropogenic disturbances and climate change. To explore the ecological changes in Chaohu Lake Received in revised form 31 October 2011 since the mid 20th century, we examined diatoms, geochemical indicators and particle size in 210Pb- Accepted 6 March 2012 dated sediment core from the lake. Diatom succession revealed that the lake had switched to a eutrophic Available online 11 June 2012 state since the late 1970s. Redundancy analysis using limnological data, hydrological and meteorological variables showed that sedimentary total phosphorus (TP) and total organic carbon (TOC), annual mean Keywords: temperature, annual mean wind velocity, and water-level amplitude (WLA) were five significant factors Diatoms Nutrient loading influencing diatom succession. Diatom assemblages from 1950 till 1978 were driven by WLA and wind. Hydrological alteration The establishment of Chaohu Dam baffled hydrological connectivity between the lake and the Yangtze Climate warming River in 1962, and reducing water exchange-induced flow. Meanwhile, weak wind velocity reduced the Eutrophication wind-induced flow in the 1960s. Due to the weak hydrodynamic intensity, the dominant species (Aulaco- Shallow lake seira granulata, a species with high sinking rate) became less important during this period. From 1979 till Yangtze floodplain 2006, diatom assemblages were mainly driven by TP, TOC and temperature, which were highly correlative. Increasing nutrient loading promoted the blooms of eutrophic species (e.g., Cyclostephanos dubius). In addition, rising temperature would indirectly influence diatom assemblages by mediating nutrient release process. As a consequence, multiple stresses in concert have caused the lake switch to a further eutrophic state indicated by prominent increases in more eutrophic species (e.g., Stephanodiscus parvus) since 2000. This study provided information on complex trajectories of aquatic ecosystem shifts driven by increasing nutrient loading, hydrological alteration and climate warming in the Yangtze floodplain lake. © 2012 Published by Elsevier GmbH.

Introduction (Scheffer et al. 2001; Carpenter 2003). In fact, regime shift of freshwater ecosystems may be due to different mechanisms that vary Human activities, such as fertilizer usage, impoundments, inten- according to their initial conditions and sites. In temperate regions, sive fishing as well as global environmental variability such as considerable effort has been devoted to understand the effects of climate change are exposing lake ecosystems to a wide range of climate warming and increased nutrient supply on ecosystem pro- pressures (Williamson et al. 2008). One of the foremost problems cesses (Jeppesen et al. 2010). In the floodplains, there is increasing resulting from these stresses is eutrophication, particularly over awareness about the impacts of hydrological condition changes the last century (Schindler 2006; Smith and Schindler 2009). Often, (e.g., water level fluctuation) on the structure and function of lake lake ecosystems can switch from clear to turbid water states once ecosystems (Coops et al. 2003; Wantzen et al. 2008; Mihaljevic´ nutrient level reach a critical range (Scheffer et al. 1993). Recent et al. 2010). However, less is known about ecological trajectories studies argue that none of environmental drivers alone can force of the shallow floodplain lakes in response to synchronous stress- regime shift of lakes, but that multiple stresses in concert are neces- ors that include increased nutrient loading, hydrological alteration sary to initiate a state shift (Hargeby et al. 2004; Bozelli et al. 2009; and climate change. Ormerod et al. 2010). Each driver may undermine the resilience of In the Yangtze floodplain, hundreds of lakes are of oxbow or a freshwater ecosystem until new perturbation can trigger the shift riverine types, which had open hydrological connections with the Yangtze’s main tributaries before the 1950s (Yang et al. 2002). The maintenance of natural hydrological connectivity is of great impor- ∗ Corresponding author. Tel.: +86 025 86882149. tance to ecological equilibria of these lake ecosystems (Liu and E-mail addresses: [email protected], [email protected] (X. Yang). Wang 2010). However, stresses associated with human occupancy

0075-9511/$ – see front matter © 2012 Published by Elsevier GmbH. http://dx.doi.org/10.1016/j.limno.2012.03.002 X. Chen et al. / Limnologica 43 (2013) 10–17 11 and use of catchment resources have exerted great pressures on falling from ∼4.3 m to ∼2.9 m (Editorial Board of the Chaohu Lake these lake ecosystems during the last 50 years (Jin 2003). Firstly, Annals 1989). Due to large amount of nutrient loading from indus- intensive land reclamation and construction of dams and dykes trial, agricultural and domestic sewage, the lake has experienced have altered natural hydrological conditions, causing shrinkage serious eutrophication since the late 1970s (Shang and Shang 2005; of water exchange volumes between lakes and the mainstream, Xie 2009). Between 1984 and 2006, the average concentrations of decline in annual water-level amplitude and other water qual- total phosphorus (TP), total nitrogen (TN), and chlorophyll a (Chl ity changes (Nakayama and Watanabe 2008). Secondly, human a) were 256 ␮gl−1, 2850 ␮gl−1, and 20–40 ␮gl−1 respectively (Xie activities are producing significant increases in nutrient loading. 2009). Statistical data show that China has experienced rapid expansion of chemical fertilizer usage, from 12.69 million tons in 1980 to 41.46 Laboratory methods million tons in 2000 (Gao and Zhang 2010). Thirdly, meteorological data demonstrate that annual mean temperature has increased A 120-cm long sediment core was collected at a water depth of by more than 1 ◦C during the last 50 years in the Yangtze basin 3.2 m using a UWITEC piston corer in 2007 from the central part (Yang et al. 2009). And rising temperature stimulates not only alga of western Chaohu Lake (Fig. 1). The core was sectioned at 0.5-cm biomass but also phosphorus release from the sediments (Jiang intervals in the field. Sedimentary proxies were analyzed in Nan- et al. 2008). Thereby, multiple pressures from hydrological alter- jing Institute of Geography and Limnology, Chinese Academy of ation, increased nutrient supply and climate warming coincide. A Sciences, including activities of radionuclide (i.e., 210Pb, 226Ra, and recent investigation shows that ca. 85% of surveyed lakes in the 137Cs), TN, TP, total organic carbon (TOC), heavy metal (i.e., Cu and Yangtze floodplain are in eutrophic states (Yang et al. 2010). How- Pb), particle size and diatoms. Upper sediments (0–20 cm depth) ever, there is little information regarding the interactive impacts of were analyzed at 0.5-cm intervals; deeper samples were analyzed nutrient, hydrology and climate on these sites. every 1-cm. The activities of 210Pb and 137Cs were measured by Because water chemistry and biota data sets extended back less direct gamma spectrometry using the Ortec HPGe GWL series of than three decades in all of the Yangtze floodplain lakes, proba- well type, coaxial, low background, and intrinsic germanium detec- ble causes of ecological shifts could not be assessed using these tors. The CE-440 elemental analyzer (EAI Company) was used for data. Fortunately, paleolimnological proxies can document ecolog- the determination of TN and TOC content of the samples. The ele- ical trajectories of these lakes in response to multi-stresses. For ment concentrations (i.e., P, Cu, and Pb) in the sediments were example, geochemical proxies (e.g., total organic carbon and total measured by the Inductively Coupled Plasma-Atomic Emission phosphorus) can provide a continuous history of trophic state (Wu Spectrometry (ICP-AES). Particle size spectra of the samples were et al. 2008; Zhang et al. 2010). Variability in particle size fraction determined using a Malvern automated laseroptical particle-size also reflects hydrological alteration in these lakes (Liu et al., 2012). analyzer (Mastersixer-2000). The diatom suspension was mounted Diatom assemblages are diverse and acutely sensitive to a range of on slides after treatment with HCl and H2O2 (Battarbee et al. 2001). environmental factors, including water quality (Yang et al. 2008; Diatom taxonomy mainly followed Krammer and Lange-Bertalot Dong et al. 2008), hydrological condition (Liu et al., 2012), and (1986–1991). A minimum of 200 valves was counted for each sam- climate variation (Tsugeki et al. 2010). ple. Chrysophycean stomatocysts were counted concurrently with Here, we examine probable causes of recent eutrophication pro- diatoms in order to calculate a cyst: valve ratio (Smol 1985). cess of Chaohu Lake in the Yangtze floodplain. Some meteorological and hydrological data can be tracked back to 1950, whereas con- Documentary records tinuous data on water chemistry and biota have a much shorter history (Tu et al. 1990; Shang and Shang 2005; Xie 2009). Therefore, Hydrological data of the Chaohu Dam Station were gathered we select sedimentary geochemical indicators and diatoms as the from the State Hydrological Yearbook (1951–1987), Historical proxies for nutrient loading and the aquatic environment, respec- Hydrological Handbook of Anhui Province (unpublished data) and tively. We use canonical ordination-based redundancy analysis to the related references (1988–2006) (Editorial Board of the Chaohu quantify relationships between fossil diatoms and environmental Lake Annals 1989; Chi 2007). Meteorological data (i.e., temperature, factors (i.e., nutrient, hydrology, and climate) that have influenced rainfall, and wind speed) were gleaned from the Hefei weather sta- the lake. We hypothesize that multiple stressors in concert have tion. Hydrological data included annual mean water level and water accelerated nutrient enrichment of Chaohu Lake. level amplitude, annual total runoff, and annual mean sediment discharge. Climate data contained annual mean temperature, annual total rainfall, and annual mean wind velocity. Historical records of Materials and methods fertilizer usage in Anhui Province and urban population of Hefei City were gathered from Agricultural Statistics Summary of Anhui Study area Province (1949–1980) (unpublished data) and the annual Census of Anhui Province (1984–2006). Chaohu Lake is the fifth largest freshwater lake in China. It has an area of ca. 770 km2, an average depth of 3.0 m, and a mean water Data analysis level of 8.0 m. Chaohu Lake basin is located in the lower reach of the Yangtze floodplain, southeast China (Fig. 1), and it is characterized Diatom zones in the core were identified using the constrained by subtropical monsoon climate with an annual mean tempera- incremental sum of squares (CONISS) facility within the computer ture of 15–16 ◦C, an annual mean rainfall of 1100 mm (Tu et al. programs TILIA and TILIAGRAPH (Grimm 1991). Detrended corre- 1990). Among the 33 tributaries in the watershed, the three main spondence analysis (DCA) was applied to the diatom percentage rivers (i.e., the Fengle River, the Hangbu River and the Nanfei River) data to explore the temporal patterns of species changes. All sta- account for more than 60% of the volume of runoff. The Yuxi River tistical analyses of diatom assemblages were based on percent is the only outflow, connecting to the Yangtze River. The hydrolog- abundances and included 32 diatom taxa with ≥1% abundance in ical conditions of the lake has been altered since the establishment at least one sample. DCA of the diatom data showed that the gra- of Chaohu Dam on the Yuxi River in 1962, including the amount of dient length of axis 1 was 1.62 standard deviations (<2 SD units), annual water exchange volume decreasing from 13.6 × 108 m3 to indicating that a linear method (redundancy analysis, RDA) was 1.6 × 108 m3 (Tu et al. 1990), and the annual water-level amplitude suitable for ordination analysis (Jongman et al. 1995). The 210Pb 12 X. Chen et al. / Limnologica 43 (2013) 10–17

Fig. 1. Map of Chaohu Lake showing the core site and the location of Hefei Meteorological Observatory and Chaohu Dam Hydrological Observatory. dating allowed comparison of sedimentary proxies with moni- during the last 50 years, and showing a low peak between 1965 toring data. Because our interests were to investigate controls of and 1973 (Fig. 2). long-term biological changes rather than interannual variability, the meteorological and hydrological data were smoothed using an Diatom succession unweighted 3-year running mean. In addition, indicators of nutrient inputs included sedimentary TP, TN, and TOC. In the RDA, to A total of 64 diatom taxa were identified in the upper sam- identify a minimum subset of environmental variables that signif- ples (0–26 cm) of the Chaohu core. Diatom assemblages were icantly explained variance in the diatom data, redundant variables characterized by planktonic species such as Aulacoseira granulata, were removed by a stepwise forward selection procedure, together Cyclostephanos dubius (Fig. 3). In zones CH1 and CH2 (between 1940 with Monte Carlo Permutation tests (P < 0.05; n = 38 restricted per- and 1978), A. granulata was the dominant species, and its abun- mutations for time series). 39 samples were included in the RDA, so dance declined generally. Meanwhile, the abundance of C. dubius there were 38 permutations to be generated under such a scheme. was fluctuating with less than 17%. The abundance of epiphytic Then a series of partial RDAs were also performed to calculate vari- and benthic diatoms (e.g., Cymbella sp., Eunotia sp., Fragilaria sp., ance in diatom data explained by the unique effects of each of and Navicula sp.) had increased gradually since the early 1960s the forward-selected variables. In this step, ordinations of each of the forward-selected variables were run with the remaining variables as covariables. The significance of the relationship between explanatory variables and diatom data was tested in each trial by a Monte Carlo Permutation test (n = 38 restricted permutations for time series). The ordinations were performed using the program CANOCO version 4.5 (ter Braak and Smilauerˇ 2002).

Results

Chronology

Sediments of the Chaohu core were dated using 210Pb and application of the constant rate of supply (CRS) dating model (Appleby 2001). The 210Pb dates were veriﬁed using the 137Cs activity peak. Detail information of the core chronology is presented in the reference (Liu et al. 2009). For comparison with the monitoring data since 1950, only the upper samples (0–26 cm) were used (Fig. 2). Fig. 2. The age-depth model for the upper samples of the Chaohu core, with dry − − Dry mass accumulation rate ﬂuctuated around 0.2 g cm 2 year 1 mass accumulation rates (DMAR) shown (referring to Liu et al., 2009). X. Chen et al. / Limnologica 43 (2013) 10–17 13

Fig. 3. Diatom assemblages in the Chaohu core between ca. 1940 and 2006. Only the major taxa (species with ≥2% in at least one sample) are shown. and reached the peak in 1978. In zone CH3, the abundance of C. population of Hefei City had expanded from less than 0.2 million dubius increased dramatically to 41% around 1978, and then varying to 1.96 million from 1950 till 2006. Meanwhile, fertilizer usage in from 17% to 46% in the following 22 years. Meanwhile, an increase Anhui Province began in the late 1950s, and it had increased over was observed in other eutrophic species (e.g., Aulacoseira alpi- tenfold during the last 40 years (Fig. 5e). gena and Thalassiosira visurgis). In contrast, epiphytic and benthic diatoms decreased gradually. In zone CH4, the diatom assemblages Ordination analysis have been dominated by C. dubius since 2000, accompanied by prominent increases in Cyclostephanos tholiformis, Stephanodiscus The results revealed that TP, TOC, wind velocity, annual mean minutulus and Stephanodicus parvus. temperature, and water level amplitude (WLA) were five significant variables influencing diatom succession. In the RDA biplot (Fig. 6), Sedimentary indicators there were two distinct groups. Samples between 1950 and 1978 were driven by water level amplitude and wind, and they moved The first two DCA axes explained 37.6% of variance in the species from the ordination space characterized by effects of high water data. Sample scores in DCA axis 2 and DCA axis 1 showed signifi- level amplitude toward the space characterized by effects of low cant declines since 1962 and 1978, respectively (Fig. 4). In addition, water level amplitude and low wind velocity. And then samples the ratio of chrysophyte cysts to diatom valves also showed a clear from 1979 till 2006 were mainly driven by nutrient and tempera- decreasing trend since 1978. Geochemical indicators (i.e., TP, TN, ture, and they moved to the space characterized by effects of high TOC, Pb, and Cu) showed a similar trend in the core, and they nutrient level (i.e., TP and TOC) and high temperature. In addition, increased slowly since the late 1950s. The content of TP, Pb, and temperature significantly correlated with TP (R = 0.539, n = 39) and Cu increased gradually in the late 1970s, and they retained high TOC (R = 0.829, n = 39). values after 1990. In contrast, TN and TOC increased rapidly since the late 1980s. Fine particle fraction increased by 10% from ca.1940 Discussion to 1970, and then it increased slightly after 1970. Response to external nutrient supply Historical records Several studies have identified anthropogenic nutrient loading The most marked trend of meteorological data was an obvious as a strong process affecting the Yangtze floodplain lakes (Wu et al. climate warming since 1985. Annual mean temperature increased 2008; Dong et al. 2008; Zhang et al. 2010). Congruent with the by more than 1 ◦C(Fig. 5a). Precipitation was highly variable dur- previous studies, this study revealed that nutrient loading (i.e., TP ing the last 50 years (Fig. 5a). The wind velocity decreased during and TOC) had made a major impact on diatom succession. Before the mid-1950s to the late 1960s, and tended to increase from the 1978, gradual increases in heavy metal (i.e., Cu and Pb), urban 1970s to the late 1990s, and then decreased thereafter (Fig. 5b). The population, and fertilizer usage were indicative of the develop- variation of annual total runoff was similar to the trend of annual ment of industry, urbanization and agriculture in Chaohu Lake total precipitation. Annual mean water level increased gradually basin. Nutrient effluents from urban area and overfertilized soil after the establishment of Chaohu Dam in 1962 (Fig. 5c). Annual are important diffuse sources of phosphorus and nitrogen in lakes average sediment discharge showed a similar curve with annual (Carpenter 2005; Schindler 2006). As a result, sedimentary prox- water level amplitude (Fig. 5d). Both of the two variables declined ies for trophic state (i.e., TP, TN, and TOC) increased gradually. In apparently after 1962. The documentary records showed that urban contrast, low abundance of C. dubius, one of the reliable diatom 14 X. Chen et al. / Limnologica 43 (2013) 10–17

Fig. 4. Sedimentary proxies in the Chaohu core between ca. 1940 and 2006, including sample scores in the first two DCA axes, a cyst: valve ratio (C:D), geochemical indicators (TP, TN, TOC, Pb, and Cu), and fine particle fraction. indicators of lake eutrophy (Bradshaw and Anderson 2003), Due to the hydrological regulation for irrigation in the drought reflected that diatom assemblages displayed hysteresis to nutri- period and flood prevention in the flood episode, WAL declined ent enrichment during this period. This may be attributed to two dramatically in Chaohu Lake after its impoundment in 1962. The reasons. Firstly, fast hydraulic flushing would reduce hydraulic res- significant WAL decline was indicative of the obstruction of hydro- idence time and nutrient accumulation before its impoundment in logical connectivity between the lake and the Yangtze River. Hence 1962. Secondly, a slight increase in nutrient concentrations gen- a weakening of hydrodynamic intensity was indicated by a marked erally benefited to the development of host macrophytes, and increase in fine particle fraction (Fig. 4) and a visible reduction in then non-planktonic taxa increased in diatom assemblage (Bennion sediment discharge (Fig. 5d). Furthermore, wind velocity played 1994). For example, increased nutrient enrichment resulted in a an important role on lake ecosystem (Table 1 and Fig. 6). In shal- significant stimulation of submerged macrophyte productivity in low lakes, wind-driven flow is one of the critical factors that affect Groby Pool. Subsequently, a marked increase in Cocconeis plancen- water-mixing regimes (Hargeby et al. 2004). The decreased wind tula was observed (Sayer 2001). In the Chaohu core, non-planktonic velocity during the 1960s would also reduce hydrodynamic inten- taxa (e.g., C. placentula var. lineata, C. affinis, and G. acuminatum) had sity (Tsugeki et al. 2010). Due to the weakening in-lake flow, heavily increased during the 1960s and the 1970s, and these diatom species silicified taxa (i.e., A. granulata) could be expected to stay shorter in were adapted to mesotrophic condition in the Yangtze floodplain the water column than before (Hotzel and Croome 1996) and thus lakes (Yang et al. 2008). became less important in the assemblages after the 1960s. How- Synchronous increases in sedimentary proxies (i.e., TP, Cu, and ever, accompanied by a rise in annual mean wind velocity through Pb), fertilizer usage and urban population indicated that enhanced the 1980s to the 1990s, the abundance of A. granulata increased. human disturbances in the basin had aroused large amount of Therefore, A. granulata is sensitive to water exchange driven flow nutrient inputs in the 1970–1980s. Gradual enrichment starting and wind driven mixing in Chaohu Lake. from low nutrient levels would cause the ecosystem to proceed toward a turbid state (Scheffer and van Nes 2007). Subsequently, Impacts from climate warming the blooms of eutrophic species (e.g., C. dubius and A. alpigena) indicated that the lake switched abruptly to a eutrophic state in 1978. In Monitoring data of annual mean temperature in Chaohu Lake addition, the presence of stomatocysts in sedimentary record gen- basin show a significant warming process similar to global pat- erally characterizes oligotrophic conditions (Smol 1985). Therefore, terns. The annual mean temperature in the basin had an average the marked decline in the ratio of chrysophycean stomatocysts to increase of 0.686 ◦C per decade (R = 0.764, n = 28, P < 0.001) from diatom valves since 1978 also indicated the rapid eutrophication 1979 to 2006 (Fig. 5). Rising temperature exerted a significant process. Thereafter, different from continuing increases in nutrient effect on diatom succession. On the first RDA axis diatom assem- inputs, the fluctuant abundance of C. dubius suggested that the lake blages from 1979 till 2006 were driven by temperature, TOC and TP, should be in a hysteresis state between 1978 and 2000. However, which were highly correlative. The results suggested that diatom continuing enrichment gradually causes the stability of the state succession should be attributed to the combined effects of rising to decline, making it more and more vulnerable to other perturba- tions and allowing a switch to an alternative state (Scheffer et al. Table 1 1993). Significant variables in redundancy analyses and their unique percentage contribu- tions to total variance in diatoms.

The effects of altered hydrodynamic condition Explanatory variables Code Unit Post-1950 Explained% P-value Except for nutrient enrichment, water level amplitude (WLA) Sedimentary total phosphorus TP mg/g 5 0.0256 was another signiﬁcant factor controlling diatom assemblages in Sedimentary total carbon TOC % 5.6 0.0256 post-1950 analysis (Table 1 and Fig. 6). Annual WLA is the differ- Water level amplitude WLA m 2.9 0.0256 ◦ ence between maximum and minimum levels, depending largely Annual mean temperature Temp C 3.7 0.0256 on regional climatic features and human use (Coops et al. 2003). Annual mean wind velocity Wind m/s 4.4 0.0256 X. Chen et al. / Limnologica 43 (2013) 10–17 15

Fig. 5. Historical records for the Chaohu Lake basin during the last 50 years. Historical records include meteorological data (three-year running mean): (a) temperature and rainfall (b) wind; hydrological data (three-year running mean): (c) runoff and water level and (d) sediment discharge and water level amplitude; social factors: (e) fertilizer usage and urban population. temperature and nutrient loading. In the shallow lakes, raised monsoon climate. In Taihu Lake, Jiang et al. (2008) revealed that the temperatures usually cause high rates of nutrient release from activity of bacteria, benthic alga and phytoplankton was enhanced sediments and renew nutrient supplies into the sediment pore as temperature increased, and then enhanced biological activities water (Jensen and Andersen 1992; Schindler 2006). Thus, ris- stimulated the removal of phosphorus from the sediments. Further- ing temperature would indirectly promote the development of more, monitoring data showed that a multi-annual warming trend nutrient-tolerant species by stimulating nutrient release process. extended the Microcystis bloom period and ampliﬁed its severity in During the recent years, increasing studies have addressed the Taihu Lake (Qin et al. 2010). relationship between climate warming and eutrophication in the As the rapid economical development during the last three Yangtze ﬂoodplain lakes, which are characterized by the subtropic decades, strong anthropogenic disturbances (e.g., industrial 16 X. Chen et al. / Limnologica 43 (2013) 10–17

his helpful comments and suggestions on the manuscript. This study was supported by National Basic Research Program of China (2012CB956104) and by the National Natural Science Fund of China (40972217) and an institutional funding (NIGLAS2010QD01).

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