Effects of environmental change on subfossil Cladocera in the subtropical shallow freshwater East Taihu Lake, China

Catena 188 (2020) 104446

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Effects of environmental change on subfossil Cladocera in the subtropical shallow freshwater East Taihu Lake, China

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Longjuan Chenga,b, Bin Xuea, , Edyta Zawiszac, Shuchun Yaoa, Jinliang Liua,b, Lingling Lia,b a

State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, No. 73 Beijing East Road, Nanjing 210008, China b University of Chinese Academy of Sciences, No. 19 Yuquan Road, Shijingshan District (A), Beijing 100049, China c Institute of Geological Sciences, Polish Academy of Sciences, Twarda 51/55, PL-00818 Warsaw, Poland

A R T I C LE I N FO

A B S T R A C T

Keywords: East Taihu Lake Subfossil Cladocera Water environment Eutrophication Paleoenvironment

East Taihu Lake (the south-eastern portion of Taihu Lake in China) suffers from eutrophication. The study of lacustrine subfossil zooplankton assemblages can be used to reconstruct the long-term evolution of lake water environments. In particular, the analysis of subfossil Cladocera can indicate historical changes in aquatic plants, water level, trophic states, and human disturbance in lakes. In this study, we correlated downcores changes in cladoceran assemblages with several geochemical proxies to identify the response of Cladocera to environmental change in East Taihu Lake over the past one hundred years. Redundancy analysis (RDA) and Pearson correlation analysis identified significant correlations between total phosphorus (TP) and Bosmina spp. (total), B. (E.) longispina, and Chydorus cf. sphaericus (correlation coefficients: −0.720 (P < 0.01), −0.646, and 0.667 (P < 0.05), respectively). We observed decreasing abundances of subfossil Bosminidae and increases in littoral cladoceran species and TP after the 1960s, coinciding with the introduction of land reclamation for fish and crab farming. These anthropogenic pressures exacerbated eutrophication, which led to the rapid growth of submerged vegetation and subsequently altered the zooplankton assemblage.

1. Introduction Lakes are relatively closed natural systems with distinct positive and negative feedback mechanisms. They are an important part of the global aquatic ecosystems and are sensitive to global change (Philips et al., 1999; Dakos and Hastings, 2013). However, many lakes around the world have suffered ecological and environmental degradation in recent years in response to anthropogenic activity and climate change. In particular, eutrophication threatens and degrades many lacustrine ecosystems due to hypoxia from harmful algal blooms (Chorus and Bartram, 1999; Bullerjahn et al., 2016; Ma et al., 2016). The cyanobacterial blooms can also alter the composition and abundance of zooplankton in lakes. Larger zooplankton such as cladocerans therefore tend to benefit from the resulting increase in cyanobacteria (Jia et al., 2017). Zooplankton that consume phytoplankton play an important role in the carbon and energy flow to the upper trophic levels of the food web (Dahms et al., 2012). Cladocera are a dominant lacustrine zooplankton component sensitive to changes in a wide range of environmental variables, such as trophic state, temperature, salinity, pH, and water level (Krause-Dellin

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and Steinberg, 1986; Hyvarinen and Alhonen, 1994; Korhola et al., 2005; Milecka and Szeroczyńska, 2005; Pawłowski et al., 2015; Çakıroğlu et al., 2016; Summers et al., 2017; Cremona et al., 2018). Studies of subfossil cladoceran remains have been applied in a number of fields, including paleoclimate reconstruction, food web analyses, and nutritional change (Duigan and Birks, 2000; Bos and Cumming, 2003; Chen et al., 2010; Nováková et al., 2013; Nevalainen et al., 2015; Zawisza et al., 2016). For example, Amsinck et al. (2003) used subfossil cladoceran remains to identify long-term changes in the trophic dynamics of brackish lakes in Denmark. Further, Kong et al. (2017) studied climate variability over the past two hundred years using alpine lake records of subfossil Cladocera from the south-eastern Tibetan Plateau. However, most of these studies have focused on lakes located in the boreal, temperate, and subarctic zones, and only a small number of studies have focused on zooplankton assemblages in shallow freshwater lakes in the Asian subtropical zone (Liu et al., 2008; Zhang et al., 2019). The middle and lower reaches of the Yangtze River Basin are rich in shallow freshwater lakes, many of which are under threat from environmental degradation (Qin et al., 2013). Taihu Lake is located in the

Corresponding author. E-mail address: [email protected] (B. Xue).

https://doi.org/10.1016/j.catena.2019.104446 Received 8 October 2019; Received in revised form 20 December 2019; Accepted 23 December 2019 0341-8162/ © 2019 Elsevier B.V. All rights reserved.

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Taihu Lake—located at the south-eastern side of the lake—has different ecologically characteristics to the other lake areas. East Taihu Lake has an area of ca. 130 km2 with an average water depth of < l m (max. 2 m). East Taihu Lake is dominated by large areas of aquatic plants such as Potamogeton malaianus, Nymphoides peltatum, and Zizania caduciflora (Yang et al., 2003; Yao et al., 2013), and the water is stagnant for prolonged periods of time (Wu et al., 2000; Yao et al., 2013; Zhao et al., 2017). Over the past 30 years, the annual average concentrations of TN and TP in East Taihu Lake were estimated to be 1.48 ± 0.03 mg/L and 0.053 ± 0.001 mg/L, respectively, which are lower than other areas of Taihu Lake (Yang et al., 2003; Dai et al., 2016). The Taipu River is East Taihu Lake’s largest outflow and an important factor in the lake’s ecological development. Additionally, large areas of the lake have been reclaimed for fish and crab farming (Wu et al., 2000).

southern region of the Yangtze River Delta and supplies water and aquatic products to several large cities and regions, such as Shanghai, Suzhou, and East Zhejiang Province. Furthermore, the lake provides a wide range of ecosystem services to the region (Yao et al., 2013). However, Taihu Lake also suffers from a number of environmental issues, including eutrophication, swamp conversion, and deteriorating water quality (Yang et al., 2003), which threaten its ecology and impact the zooplankton community. However, the response in the composition and abundance of zooplankton (such as cladocerans) to environmental perturbations in Taihu Lake over the past decades have not yet been investigated. In this study, we analysed the sedimentary records of subfossil Cladocera and several geochemical indices to identify the environmental factors that controlled Cladocera distribution in the eastern section of Taihu Lake (East Taihu Lake) over the last 100 years. Due to increasing anthropogenic impact on the lake environment, we aimed to identify changes in the cladoceran community in response to environmental change and determine the dominant causes and mechanisms of water quality deterioration. As such, our main objectives were to (1) determine the long-term changes in the cladoceran community, and (2) identify the response of subfossil Cladocera to anthropogenic impact over the last century.

3. Materials and methods 3.1. Field sampling A gravity corer was used to collect two (twin) 30 cm sediment cores (TH-5, TH-5-2) during autumn (November 2016) when the water depth had reached 1.84 m (31.08744°N, 120.51746°E) (Fig. 1). The sampling pipe (made of Polymethyl Methacrylate, PMMA) is 9 cm in diameter and 60 cm in length. The sediment cores were subsampled continuously at 1 cm intervals and stored at 4 °C in the laboratory of the Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences (NIGLAS). Samples from the TH-5 core were used for the analyses of subfossil cladoceran presence, water content, and loss on ignition (LOI), and samples from the TH-5-2 core were used for the measurements of total organic carbon (TOC), bulk δ13C (δ13Corg), total nitrogen (TN), total phosphorus (TP) and C/N.

2. Study site Taihu Lake experiences a subtropical monsoon climate with an average annual precipitation of 1010–1400 mm (most of which falls during summer) and an average annual temperature of 15–17 °C (Lin et al., 2019). Taihu Lake is the third largest freshwater lake in China covering an area of 2338 km2 with a shallow mean water depth of 1.89 m (Qin et al., 2007). More than 200 rivers flow into Taihu Lake with a combined total river length of ~120,000 km (Zhong et al., 2014). The lake is divided, ecologically, into five different basins (Fig. 1) (Dai et al., 2016). Increasing nutrient levels in Taihu Lake has led to reduced biodiversity and cyanobacterial blooms, particularly the emergence of non-N2-fixing Microcystis spp. cyanobacteria (Yang et al., 2008; Li and Chen, 2010; Deng et al., 2014; Paerl et al., 2014; Xu et al., 2016). These ecological shifts have caused a decrease in the richness of cladoceran species. The abundance of a single cladoceran taxon (Bosmina) had increased by 90% since the year 2000 in Taihu Lake (Liu et al., 2008; Li and Chen, 2010; Cheng et al., 2019). However, East

3.2. Geochemistry Approximately 10 g of wet sediment from each sample in TH-5 core were used for the LOI analysis. To remove organic carbon, the sediments were placed in crucibles, dried at 105 °C for 5 h, and then burned in a muffle furnace at 550 °C for 4 h (Heiri et al., 2001). Samples were weighed after each treatment and the percent water content and LOI were calculated. The TOC and δ13Corg were analysed by the removal of carbonates using 1 M HCl. We measured sediment TOC and TN using a

Fig. 1. The location of studied site and the sediment cores collection (TH-5 and TH-5-2) in the East Taihu Lake (SE China). 2

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We identified Bosmina at the species level based on their first antennule, head pore location, and mucro (Szeroczyńska and Sarmaja-Korjonen, 2007). 3.5. Statistical methods and graphical representations Ordination analysis and Pearson correlation analysis were used to determine the dominant environmental controls on the cladoceran assemblages over time. TOC, TN, TP, and C/N were selected as the environmental variables, and the cladoceran assemblages were the response variables. Ordination analysis was performed using the software Canoco 4.5 (ter Braak and Šmilauer, 2002). Redundancy analysis (RDA) was conducted based on the assumption that organisms respond linearly to changes in environmental variables (ter Braak and Šmilauer, 2002). Down weighting rare species reduced deviations in the ordination analysis after the data were square root transformed, and the significance of each environmental variable was examined using Canoco 4.5 (ter Braak and Šmilauer, 2002). Pearson correlation analysis of the geochemical and biological data (cladoceran data) was conducted in IBM SPSS 19.0 (Statistical Graphics Co., Princeton, USA). We applied the constrained incremental sum of squares (CONISS) cluster analysis using Tilia (Grimm, 1990) on the cladoceran data to identify the temporal variability of the dominant cladoceran assemblages.

Fig. 2. The comparison of LOI contents between the DQG core (Yao et al., 2013) and TH-5 core from East Taihu Lake. The age-depth model was adapted for TH-5 core from the DQG core (Yao et al., 2013).

CE-440 elemental analyser (EAI Company Ltd.), and an ICP-AES was used to determine TP concentrations. We measured the physical and chemical parameters of the lake surface water at the core retrieval site in autumn (November 2016), spring (April 2018), and summer (July 2018). The pH values were measured using a pH meter (model PHB-4-Shanghai Yidian Scientific Instrument Company Ltd.), and the dissolved oxygen (DO) and electroharmonix (Eh) levels were measured using a portable dissolved oxygen meter (model JPBJ-608- Shanghai Yidian Scientific Instrument Company Ltd.). Water transparency was measured using a Secchi disc and chlorophyll-a (Chl-a) concentrations were measured using a spectrophotometer (model RF-5301PC, Shimadzu, Japan) (Chen and Gao, 2000).

4. Results 4.1. Physical and chemical parameters of the water samples The physical and chemical parameters of the surface water in East Taihu Lake showed significant seasonal variability. The water depth in East Taihu Lake throughout the three seasons (spring (April 2018), summer (July 2018) and autumn (November 2016)) ranged between 1.5 and 2 m (Table 1). Water temperatures were 18.9 °C in spring, 30.5 °C in summer, and 15 °C in autumn. Water pH was slightly alkaline (~8) and remained generally stable between the seasons, with lowest values in autumn. Water transparency was high in autumn relative to spring and summer. The seasonal DO, saturation, and Eh values indicate limited water column oxygen (O2) levels during spring and summer. The Chl-a concentrations varied between seasons with the maximum concentration recorded in summer (Table 1).

3.3. Chronology Yao et al. (2013) determined the age-depth model of core DQG (collected from the same location as the cores in this study) based on the 210Pb, 226Ra, and 137Cs activity. To determine the age model of TH5, we correlated the downcore LOI contents of the DQG core (Yao et al., 2013) with the TH-5 core (Fig. 2). We then calculated the average sedimentation rate based on the correlation between the two profiles (DQG and TH-5). The average sedimentation rate for TH-5 was 0.27 cm/yr, and the approximate age of the core (at 30 cm) was ~100 years (1900s–2010s AD).

4.2. Composition and abundance of subfossil Cladocera A total of 19 taxa were identified in the sediments from TH-5 core, taxa belonging to the following 5 families: Bosminidae, Chydoridae, Sididae, Moinidae, and Daphniidae. The family with the highest species abundances was Bosminidae followed by Chydoridae (Fig. 3). The CONISS cluster analysis identified two distinct cladoceran assemblage phases from the 1900s to the present day: early stage (30–15 cm, ca. 1900s–1960s AD) and later stage (15–0 cm, 1960s–2010s AD) (Fig. 3). Early stage was characterised by 15 cladoceran taxa with an average

3.4. Subfossil cladoceran analysis We analysed 25 fresh sediment subsamples (from 0 to 20 cm long core at 1 cm resolution intervals, and from 20 to 30 cm long core at 2 cm resolution intervals, respectively) from TH-5 to determine the subfossil cladoceran assemblages. Sediments were treated with 100 ml 10% KOH solution and heated at 60 °C for 45 min. The samples were then sieved through a 38 µm mesh under running deionized water and transferred into 15 ml centrifuge tubes (Frey, 1986; Korhola and Rautio, 2001). We added a few drops of 95% alcohol to the residues for long-term preservation (Nevalainen et al., 2016) and a few drops of safranin for staining. The caldoceran remains were counted under a microscope at 200x magnification and identified according to the following publications: Goulden and Frey (1963), Jiang and Du (1979), Szeroczyńska and Sarmaja-Korjonen (2007), Xiang et al. (2015), and Ji et al. (2015). The cladoceran species were identified by their shells, headshields, postabdomens, and claws. The remains of at least 100 individuals were counted from each sample (Nevalainen et al., 2016).

Table 1 Physical and chemical water parameters collected from the core sites (TH-5 and TH-5-2) in East Taihu Lake.

3

Parameters

Spring (April 2018)

Summer (July 2018)

Autumn (November 2016)

Depth (m) Water temperature (°C) pH Transparency (cm) DO (mg/L) Saturation (%) Eh (mv) Chlorophyll-a (μg/L)

1.53 18.9 8.77 41 8.51 95 −98 22.31

1.73 30.5 8.66 28 7.98 106.6 −86 51.65

1.84 15 7.58 60 9.46 – −118 20.48

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Fig. 3. Abundance and assemblages of subfossil cladocerans identified in TH-5 core, from the East Taihu Lake.

individual concentration of ca. 2300 ind./cm3. The dominant taxa were the planktonic Bosmina spp. (contributing ~90%), which included B. (E.) longispina (40%) and B. longirostris (11%). Only planktonic taxa were abundant in this section of the core. Chydorus cf. sphaericus was the most abundant taxa after the Bosminidae family, contributing only ca. 2%. Later stage was characterised by 18 cladoceran taxa. The total abundance of cladoceran species significantly decreased (range: 1010 to 460 ind./cm3; average: 700 ind./cm3) in comparison to the early stage. We observed clear changes in the cladoceran species composition since 1960 AD, with significant increases in the percentage abundances of littoral taxa and decreases in planktonic taxa (total Bosmina spp. ranged from 10% to 50% with an average of 40%, which includes B. (E.) longispina ~5% and B. longirostris ~11%). The dominant littoral taxa were Chydorus cf. sphaericus (20%), Graptoleberis testudinaria (8%), and unidentified Alona spp. (7%).

similar to the early stage values, with average contents of 0.96% and 9.64, respectively. TOC remained constant with average values of 1.28%. The δ13Corg increased during the first part of the later stage (average value of −21.0‰) but began to decrease in the younger sediments. 4.4. Statistical analysis of the subfossil cladoceran assemblage and geochemical proxies Pearson correlation analysis identified significant correlations between the total abundance of the dominant cladoceran taxa (Bosmina spp., B. (E.) longispina, B. longirostris, and Chydorus cf. sphaericus) and TP (Table 2). Significant negative correlations were observed between TP and total Bosmina spp. and B. (E.) longispina with correlation coefficients of −0.720 (P < 0.01) and −0.646 (P < 0.05), respectively (Fig. 5). We observed a positive correlation between TP and Chydorus cf. sphaericus, with a correlation coefficient of 0.667 (P < 0.05) (Fig. 5). The response data were compositional with a gradient of 1.284 SD units. A linear method (redundancy analysis, RDA) was recommended (Table 3) (Birks, 1995). RDA ordination identified relationships between the downcore subfossil cladoceran assemblages and the measured geochemical proxies in East Taihu Lake (Fig. 6). TP showed the most significant correlation (P value < 0.05) with some cladoceran taxa (Table 3). TP was positively correlated with axis 1, which explained 39% of the variability. Axis 1 was associated with positive loadings from the littoral taxa, Chydorus cf. sphaericus, Graptoleberis testudinaria, Alona spp., and Camptocercus sp., which were also positively correlated with TP. In contrast, planktonic taxa— such as the Bosminidae family— were negatively distributed in axis 1 and showed negative correlations with TP (Fig. 6).

4.3. Geochemical proxies in the TH-5 and TH-5-2 cores TOC, LOI, TP, TN, C/N, δ13Corg, and water content showed significant variability over time in East Taihu Lake (Fig. 4). Throughout the study period, the percentage LOI ranged from 1.89% to 6.61% (average 4.33%), sediment water content ranged from 23.15% to 73.18% (average 49.37%), TOC ranged from 0.13% to 1.75% (average 1.15%), TN ranged from 0.92% to 1.02% (average 0.97%), C/N ratios ranged from 9.17 to 10.19 (average 9.71), TP ranged from 0.39 mg/g to 0.45 mg/g (average 0.42 mg/g), and δ13Corg ranged from −23.77‰ to −20.29‰ (average −21.60‰). We identified two stages between 1900 AD and 2010 AD based on the downcore geochemical trends: the early stage (30–15 cm, 1900s–1960s AD) and later stage ((15–0 cm, 1960s–2010s AD). We identified relatively low LOI, water content, TOC, and TP during the early stage. The average values of LOI, water content, and TP were 2.13%, 28.27%, and 0.40 mg/g, respectively, and TOC ranged from 0.2% to 1.8%. We observed a minor change in TN, with an average value of 0.98%. C/N ratios ranged from 9.62 to 10.19, with a mean value of 9.80. δ13Corg values increased going up, with an average value of −22.34‰. In comparison to the early stage, the later stage was characterised by increasing trends in LOI, water content, and TP, with average values of 5.66%, 62.03%, and 0.43 mg/g, respectively. TN and C/N were

4.5. P/L ratio The ratio of planktonic to littoral (P/L) species in the TH-5 core showed significant periodic variability coinciding with changes in lake area and submerged plant biomass in East Taihu Lake (Hofmann, 1998; Bos et al., 1999; Yang et al., 2003; Bigler et al., 2006). The natural logarithm (ln) of P/L (from now on referred to as “P/L”) was higher prior to 1960 AD (average 2.48) and declined markedly thereafter (average −0.33) (Fig. 7). Based on monitoring data (Yang et al., 2003), 4

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Fig. 4. Changes of geochemical components indices in TH-5 (LOI and water content) and TH-5-2 (TOC, TN, C/N, TP and δ13Corg) cores collected from East Taihu Lake.

low values of TOC, LOI, TN, and TP (Fig. 3, Fig. 4 and Fig. 7). Our results are in agreement with historical records indicating low lake trophic status prior to the 1960s (Yang et al., 2003). Historical records identified diatoms to be the dominant phytoplankton species during the 1960s, and aquatic vegetation was low in biomass but high in diversity (Yang et al., 2003). Macrophyte coverage was also found to be lower in East Taihu Lake during the first part of the twentieth century (Yang et al., 2003). The cladoceran zooplankton community of East Taihu Lake during the later stage (1960s–2010s AD) largely differed from the early stage. Cladoceran littoral taxa abundance, LOI, and TP increased significantly (Figs. 3 and 4), while the total abundance of subfossil Cladocera (from ~2300 to ~700 ind./cm3) and δ13Corg had decreased. These observations coincided with the occurrence of land reclamation which began in 1960 AD (Fig. 7), leading to a reduction in the depth, volume, and area of East Taihu Lake. Our results therefore infer increased abundances of aquatic vegetation and littoral cladoceran species in East Taihu Lake in response to swamp conversion (Figs. 3 and 7) (Yang et al., 2003). Further, the rapid development of fish and crab culture in East Taihu Lake in the 1960s increased nutrient (e.g. TP) deposition in lake sediments and accelerated the process of swamp conversion (Fig. 7). P/L had decreased significantly in 2000 AD (Fig. 7), coinciding with the rapid decline in the total biomass of submerged plants. These observations are consistent with findings from Yang et al. (2003), who identified increased abundances of emergent plants and floating-leaf vegetation in response to the implementation of fish and crab farming (Yang et al., 2003). Over the last century, the subfossil cladoceran composition was dominated by species from the Bosminidae family as well as Chydorus cf. sphaericus (Fig. 3). Pearson correlation analysis showed significant correlations between the dominant cladoceran taxa and TP. The Bosminidae species were significantly negatively correlated with TP, while Chydorus cf. sphaericus was significantly positively correlated with TP (Fig. 5). In agreement, RDA identified close relationships between TP and Chydorus cf. sphaericus and the Bosminidae species. TP and Chydorus cf. sphaericus shared positive loadings in axis 1, while Bosmina spp. were negatively loaded in axis 1 (Fig. 6). These findings demonstrate the strong influence of TP on the cladoceran community, which showed a clear shift from planktonic to littoral species from the early to the latter part of the twentieth century. The strong relationship between

Table 2 Pearson correlation analysis between the geochemical proxies and the dominant cladoceran taxa.

Bosmina spp. B. longirostris B. (E.) longispina Chydorus cf. sphaericus

TOC

TN

TP

C/N

−0.335 0.182 −0.556 0.321

0.376 0.154 0.330 −0.353

−0.720** −0.176 −0.646* 0.667*

0.375 0.161 0.324 −0.350

** Correlation is significant at P < 0.01. * Correlation is significant at P < 0.05.

the area of East Taihu Lake reduced significantly from 265 km2 in 1916 to 129 km2 in 2002. Since the 1960s, the trend in both lake area and P/ L reduced whereas the biomass of submerged plants increased significantly. 5. Discussion East Taihu Lake is a grass-type aquatic environment and experiences frequent occurrences of summer cyanobacterial blooms as a result of intense eutrophication (Yao et al., 2013). The annual average concentrations of TN and TP (1.48 ± 0.03 mg/L and 0.053 ± 0.001 mg/ L, respectively) in East Taihu Lake over the past 30 years were lower than in the other lake regions (Yang et al., 2003; Dai et al., 2016). However, our paleolimnological results from the TH-5 and TH-5-2 cores inferred significant variability in the trophic status of East Taihu Lake during the last 100 years. We identified clear shifts in the cladoceran community in response to changes in the water environment. Specifically, we identified two environmental stages based on the analysis of subfossil cladoceran assemblages (early and later stages). The early stage (1900s–1960s AD) was characterized by generally high abundances of subfossil Cladocera (max. 7520 ind./cm3; average. 2300 ind./cm3), but low abundances of littoral taxa. Zooplankton was dominated by the planktonic species B. (E.) longispina, which is typically characteristic of oligotrophic to mesotrophic environments (Deevey, 1942; Boucherle and Züllig, 1983). High P/L ratios (~2) and total Bosmina spp. (~90%) indicate open water conditions suitable for the growth of planktonic cladoceran. P/L ratios reached a maximum in the 1920s (~3) coinciding with high values of B. (E.) longispina and the 5

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Fig. 5. Pearson correlation analysis between the TP and the dominant cladoceran species (Bosmina spp., B. (E.) longispina and Chydorus cf. sphaericus).

water level, aquatic vegetation, and predators (e.g. fish) can also influence cladoceran populations in East Taihu Lake. Since the 1960s, the number of cladoceran species increased and the total cladoceran abundance significantly decreased in East Taihu Lake (Fig. 3). Additionally, P/L ratios were noticeably higher prior to the 1960s. These changes coincided with the introduction of land reclamation in the 1960s (Fig. 7) (Yang et al., 2003). Fish and crab farming practices in East Taihu Lake throughout the past 50 years have increased the number of cladoceran predators (Perga et al., 2010; Mao et al., 2012). Land reclamation for fish and crab farming in East Taihu Lake have intensified since the 1980s. Further, the East Taihu Lake area has significantly decreased from 265 km2 in 1916 AD to 129 km2 in 2002 AD as a result of human activities (Yang et al., 2003). A smaller lake area reduces wave intensity and prolongs the water stagnation period, which promotes the overgrowth of aquatic plants (Yao et al., 2013). In 1997

Chydorus cf. sphaericus abundance and nutrient level highlights the species’ applicability as an indicator for eutrophication (Hofmann, 1996; Brodersen et al., 1998; Shumate et al., 2002). The downcore trends in LOI, TP, and δ13Corg indicate significant water trophic changes since the 1960s. Increasing TP concentrations in this study confirms previous observations of increasing nutrient levels in East Taihu Lake (Lotter, 1998; Ma et al., 2014). High TOC and LOI values further indicate elevated sediment organic matter content. δ13Corg values gradually decreased following a peak in the 1960s (Fig. 4). This decrease may be linked to high nutrient flux to East Taihu Lake, which caused an imbalance in carbon isotope fractionation. This finding is consistent with observations of negative δ13Corg values in aquatic plants attributed to the increased plant uptake of 12C (Meyers, 1994; Shen et al., 2010). In addition to eutrophication, other environmental factors such as

Table 3 Redundancy analysis (RDA) of cladoceran species and geochemical proxies (TP, TN, C/N and TOC). Only species data available (DCA)

Species and environmental data available (RDA)

Axes

1

2

3

4

Total inertia

Eigenvalues Lengths of gradient Cumulative percentage variance of species data

0.178 1.284 56.9

0.027 0.557 65.4

0.007 0.458 67.6

0.001 0.466 68

0.314

Variable

P-value

F-ratio

TP TN C/N TOC

0.018* 0.856 0.638 0.664

5.55 0.38 0.54 0.58

* Correlation is significant at P < 0.05. 6

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Fig. 6. Redundancy analysis (RDA) ordination among the geochemical indices with the dominant species.

organic matter, which further promote the growth of submerged plants and reduce the lake area (Fig. 7). The growth of macrophyte vegetation in East Taihu Lake is known to directly influence the development of littoral cladoceran species (Whiteside et al., 1988; Gyllstrom and Hansson, 2004; Backer et al., 2012), which explains their increasing abundance since the 1960s (Fig. 3). The environmental changes observed in East Taihu Lake vary significantly to those reported from the western and central areas of the Taihu Lake (Liu et al., 2008; Cheng et al., 2019). Our results indicate that the largest environmental shift in East Taihu Lake began in the 1960s due to changes in eutrophication, fish and crab farming, siltation, macrophyte development, water level, and lake area. In contrast, the largest environmental shift occurred in the western and central areas of the lake, including the extinction of large aquatic plants and

AD, aquatic vegetation covered 95% of East Taihu Lake, and the average macrophyte biomass was approximately 3.8 kg m−2, with a range of 2.0–5.6 kg m−2 (Li, 2004). Increases in residual artificial bait and excrement as a result of fish and crab farming (Yang et al., 2003) has significantly contributed to the accumulation of carbon, nitrogen, and phosphorus in surface sediments since the 1980s. Elevated nutrients and organic matter stimulated siltation and macrophyte development, resulting in a shift in macrophyte succession from submerged to emergent and floating-leaf vegetation. Additionally, stagnant water facilitated the deposition of macrophyte detritus and other particles in sediments (Yang et al., 2003). Further, Taipu River—the major outflow of Taihu Lake— is located in East Taihu Lake, and thus particles from the surrounding catchment are transported eastwards and deposited in its sediments (Qin et al., 2007). Accordingly, these deposits are rich in

Fig. 7. The changes of P/L, submerged plant biomass and East Taihu Lake area. Note: the data of area of East Taihu Lake and submerged plant biomass referred to Yang et al. (2003). 7

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overbreeding of phytoplankton. These changes significantly reduced the species diversity of cladocerans, which was dominated by Bosmina spp., with an average relative abundance of ~80% (Liu et al., 2008; Cheng et al., 2019). Environmental changes similar to those in East Taihu Lake have been observed in nearby lakes in the middle and lower reaches of the Yangtze River, including the Liangzi, Dongting, and Changdang lakes (Chen et al., 2015; Ge et al., 2018; Zeng et al., 2018; Zhang et al., 2019). Combined, our results suggest that human activity over the past few decades has significantly intensified eutrophication in many of the lakes in the middle and lower reaches of the Yangtze River.

Maddy, D., Brew, J.S. (Eds.), Statistical modelling of quaternary science data. Quaternary Research Association, Technical guide 5. Cambridge University Press, Cambridge. Bos, D.G., Cumming, B.F., Smol, J.P., 1999. Cladocera and Anostraca from the Interior Plateau of British Columbia, Canada, as paleolimnological indicators of salinity and lake level. Hydrobiologia 392, 129–141. Bos, D.G., Cumming, B.F., 2003. Sedimentary cladoceran remains and their relationship to nutrients and other limnological variables in 53 lakes from British Columbia, Canada. Can. J. Fish. Aquat. Sci. 60 (60), 1177–1189. Boucherle, M.M., Züllig, H., 1983. Cladoceran remains as evidence of change in trophic state in three Swiss lakes. Hydrobiologia 103, 141–146. Brodersen, K.P., Whiteside, M.C., Lindegaard, C., 1998. Reconstruction of trophic state in Danish lakes using subfossil chydorid (Cladocera) assemblages. Can. J. Fish. Aquat. Sci. 55, 1093–1103. Bullerjahn, G.S., McKay, R.M., Davis, T.W., Baker, D.B., Boyer, G.L., D’Anglada, L.V., Doucette, G.J., Ho, J.C., Irwin, E.G., Kling, C.L., Kudela, R.M., Kurmayer, R., Michalak, A.M., Ortiz, J.D., Otten, T.G., Paerl, H.W., Qin, B., Sohngen, B.L., Stumpf, R.P., Visser, P.M., Wilhelm, S.W., 2016. Global solutions to regional problems: collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae 54, 223–238. Çakıroğlu, A.İ., Levi, E.E., Tavşanoğlu, Ü.N., Bezirci, G., Erdoğan, Ş., Filiz, N., Andersen, T.J., Davidson, T.A., Jeppesen, E., Beklioğlu, M., 2016. Inferring past environmental changes in three Turkish lakes from sub-fossil Cladocera. Hydrobiologia 778, 295–312. Chen, G., Dalton, C., Taylor, D., 2010. Cladocera as indicators of trophic state in Irish lakes. J. Paleolimnol. 44 (2), 465–481. Chen, X., McGowan, S., Xu, L., Zeng, L., Yang, X., 2015. Effects of hydrological regulation and anthropogenic pollutants on Dongting Lake in the Yangtze floodplain. Ecohydrology 9, 315–325. Chen, Y., Gao, X., 2000. Comparison of two methods for phytoplankton Chlorophyll-a concentration measurement. J Lake Sci. 12, 186–188 (in Chinese). Cheng, L., Yao, S., Xue, B., Li, L., Liu, J., 2019. Long-term change of the assemblages and abundance of cladocerans in different ecotypes of Lake Taihu. J. Lake Sci. 31 (in Chinese). Chorus, I., Bartram, J., 1999. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences. Monitoring and Management. E & FN Spon, London and New York. Cremona, F., Tuvikene, L., Haberman, J., Nõges, Peeter, Nõges, Tiina, 2018. Factors controlling the three-decade long rise in cyanobacteria biomass in a eutrophic shallow lake. Sci. Total Environ. 621, 352–359. Dahms, H.U., Tseng, L.C., Hsiao, S.H., Chen, Q.C., Kim, B.R., Hwang, J.S., 2012. Biodiversity of planktonic copepods in the Lanyang River (northeastern Taiwan), a typical watershed of Oceania. Zool. Stud. 51, 160–174. Dai, X.L., Qian, P.Q., Ye, L., Song, T., 2016. Changes in nitrogen and phosphorus concentrations in Lake Taihu, 1985–2015. J. Lake Sci. 28 (5), 935–943 (in Chinese). Dakos, V., Hastings, A., 2013. Editorial: special issue on regime shifts and tipping points in ecology. Theoret. Ecol. 6 (3), 253–254. Deevey, E.S.J., 1942. Studies on Connecticut lake sediments. III. The Biostratonomy of Linsley Pond. Am. J. Sci. 240, 233–264. Deng, J., Qin, B., Paerl, H.W., Zhang, Y., Wu, P., Ma, J., Chen, Y., 2014. Effects of nutrients, temperature and their interactions on spring phytoplankton community succession in Lake Taihu, China. Plos One 9 (12), e113960. Duigan, C.A., Birks, H.H., 2000. The late-glacial and early-Holocene palaeoecology of cladoceran microfossil assemblages at Kråkenes, western Norway, with a quantitative reconstruction of temperature changes. J. Paleolimnol. 23 (1), 67–76. Frey, D.G., 1986. Cladocera analysis. In: Berglund, B.E. (Ed.), Handbook of Holocene palaeoecology and palaeohydrology. John Whiley & sons, New York, pp. 667–692. Ge, Y., Zhang, K., Yang, X., 2018. Long-term succession of aquatic plants reconstructed from palynological records in a shallow freshwater lake. Sci. Total Environ. 643, 312–323. Grimm, E., 1990. Tilia and Tilia. Graph: pc spreadsheet and graphics software for pollen data. J. Mol. Struct. 12 (Newsletter 4), 159–165. Goulden, C.E., Frey, D.G., 1963. The occurrence and significance of lateral head pores in the genus Bosmina (Cladocera). Int. Rev. Gesamten. Hydrobiol. 48, 513–522. Gyllstrom, M., Hansson, L., 2004. Dormancy in freshwater zooplankton: Induction, termination and the importance of benthic-pelagic coupling. Aquat. Sci. 66, 274–295. Heiri, O., Lotter, A.F., Lemcke, G., 2001. Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol. 25 (1), 101–110. Hofmann, W., 1996. Empirical relationships between cladoceran fauna and trophic state in thirteen northern German lakes: analysis of surficial sediments. Hydrobiologia 318, 195–201. Hofmann, W., 1998. Cladocerans and chironomids as indicators of lake level changes in north temperate lakes. J. Paleolimnol. 19, 55–62. Hyvarinen, H., Alhonen, P., 1994. Holocene lake-level changes in the Fennoscandian treeline region, western Finnish Lapland: diatom and cladoceran evidence. The Holocene 4 (3), 251–258. Ji, G.H., Xiang, X.F., Chen, S.Z., Yu, G.L., Kotov, A.A., Dumont, H.J., 2015. Annotated Checklist of Chinese Cladocera (Crustacea: Branchiopoda). Part II. Order Anomopoda (families Macrotrichidae, Eurycercidae and Chydoridae). Zootaxa 4044 (2), 241–269. Jia, J., Shi, W., Chen, Q., Lauridsen, T.L., 2017. Spatial and temporal variations reveal the response of zooplankton to cyanobacteria. Harmful Algae 64, 63–73. Jiang, X., Du, N., 1979. Fauna of China-Arthropod Phylum-Crustacean-Freshwater Cladocera. Science Press, Beijing, pp. 41–42 (in Chinese). Kong, L., Yang, X., Kattel, G., Anderson, N.J., Hu, Z., 2017. The response of Cladocerans to recent environmental forcing in an Alpine Lake on the SE Tibetan Plateau.

6. Conclusion Our results demonstrate a shift in the ecosystem structure of East Taihu Lake towards a dominance of phytoplankton with frequent summer cyanobacteria blooms in response to ongoing eutrophication (Zhou and Zheng, 2008). Downcore changes in the composition and abundance of cladocerans in East Taihu Lake reflect changes in the lake environment caused by increasing anthropogenic disturbance. Specifically, the most prominent shifts in subfossil Cladocera assemblages occurred in response to the introduction of land reclamation for fish and crab farming in the 1960s, which increased eutrophication, stimulated the growth of submerged vegetation, and reduced the area of East Taihu Lake. Moreover, Pearson correlation analysis and RDA showed that TP was the dominant control on the cladoceran assemblage structure. To improve water quality, land reclamation for fish and crab farming has recently been banned by local government ministry in East Taihu Lake. Therefore, to track ecosystem health, changes in the abundance and composition of zooplankton—particularly cladocerans—should be continually monitored. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was funded by National Key Research and Development Program of China (2019YFA0607100), National Natural Science Foundation of China (NSFC) (41573129) and National Basic Science and Technology Special Project (2014FY110400). The original draft and experimental analysis were written and performed by Longjuan Cheng. Bin Xue provided funding acquisition and supervision. Edyta Zawisza assisted in manuscript modification. Shuchun Yao, Jinliang Liu and Lingling Li assisted in sample collection and processing. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.catena.2019.104446. References Amsinck, S.L., Jeppesen, E., Ryves, D., 2003. Cladoceran stratigraphy in two shallow brackish lakes with special reference to changes in salinity, macrophyte abundance and fish predation. J Paleolimnol. 29, 495–507. Backer, S.D., Teissier, S., Triest, L., 2012. Stabilizing the clear-water state in eutrophic ponds after biomanipulation: submerged vegetation versus fish recolonization. Hydrobiologia 689, 161–176. Bigler, C., Heiri, O., Krskova, R., Lotter, André F., Sturm, M., 2006. Distribution of diatoms, chironomids and cladocera in surface sediments of thirty mountain lakes in south-eastern Switzerland. Aquat. Sci. 68, 154–171. Birks, H.J.B., 1995. Quantitative palaeoenvironmental reconstructions 161-254. In:

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L. Cheng, et al.

25 years' research into the management of shallow lakes. Hydrobiologia 395 (396), 61–76. Qin, B.Q., Xu, P., Wu, Q., Luo, L., Zhang, Y., 2007. Environmental issues of Lake Taihu, China. Hydrobiologia 581, 3–14. Qin, B.Q., Gao, G., Zhu, G.W., Zhang, Y.L., Song, Y.Z., Tang, X.M., Xu, H., Deng, J.M., 2013. Lake eutrophication and its ecosystem response. Sci. Bull. 58 (9), 961–970. Shen, J., Xue, B., Wu, J.L., Wu, Y.H., Liu, X.Q., Yang, X.D., Liu, J., Wang, S.M., 2010. Lake Sediments and Environment Changes. Science Press, Beijing, China (in Chinese). Shumate, B.C., Schelske, C.L., Crisman, T.L., Kenney, W.F., 2002. Response of the cladoceran community to trophic state change in Lake Apopka, Florida. J. Paleolimnol. 27, 71–77. Summers, J.C., Kurek, J., Rühland, K.M., Neville, E.E., Smol, J.P., 2017. Assessment of multi-trophic changes in a shallow boreal lake simultaneously exposed to climate change and aerial deposition of contaminants from the Athabasca Oil Sands Region, Canada. Sci. Total Environ. 592, 573–583. Szeroczyńska, K., Sarmaja-Korjonen, K., 2007. Atlas of Subfossil Cladocera from Central and Northern Europe. Friends of the Lower Vistula Society, Swiecie, pp. 10–11. ter Braak, C.J.F., Šmilauer, P., 2002. CANOCO Reference manual and CanoDraw for Windows users’ guide, Software for Canonical Community Ordination (version 4.5). Microcomputer Power (Ithaca, NY, USA), 500 pp. Whiteside, M.C., Swindoll, M.R., 1988. Guidelines and limitations to cladoceran paleoecological interpretations. Palaeogeogr., Palaeoclimatol. Palaeoecol. 62, 405–412. Wu, Q.L., Hu, Y.H., Li, W.C., Chen, K.N., Pan, J.Z., 2000. Tendency of swampiness of East Taihu Lake and its causes. Aata Scientiae Circumstantiae 20, 275–279 (in Chinese). Xiang, X.F., Ji, G.H., Chen, S.Z., Yu, G.L., Xu, L., Han, B.P., Dumont, H.J., 2015. Annotated Checklist of Chinese Cladocera (Crustacea: Branchiopoda). Part I. Haplopoda, Ctenopoda, Onychopoda and Anomopoda (families Daphniidae, Moinidae, Bosminidae, Ilyocryptidae). Zootaxa 3904 (1), 1–27. Xu, D., Cai, Y., Jiang, H., Wu, X., Leng, X., An, S., 2016. Variations of food web structure and energy availability of shallow lake with long-term eutrophication: a case study from Lake Taihu, China. CSAWAC 44, 1261–1427. Yang, G., Pan, H., Liu, Z., Wang, W., Qin, B., 2008. A comparative study on seasonal variations of crustaceans in the different lake areas in Lake Taihu. China Environ. Sci. 28 (1), 27–32 (in Chinese). Yang, Z.F., Shi, W.G., Chen, L.Q., Chen, Y., Zhou, Z.L., 2003. Ecological environment succession and countermeasure of East Taihu Lake. China Environ. Sci. 23 (1), 64–68 (in Chinese). Yao, S., Xue, B., Tao, Y., 2013. Sedimentary lead pollution history: lead isotope ratios and conservative elements at east Taihu Lake, Yangtze Delta, China. Quatern. Int. 304, 5–12. Zawisza, E., Zawiska, I., Correa-Metrio, A., 2016. Cladocera community composition as a function of physicochemical and morphological parameters of dystrophic lakes in ne Poland. Wetlands 36 (6), 1131–1142. Zeng, L.H., McGowan, S., Cao, Y.M., Chen, X., 2018. Effects of dam construction and increasing pollutants on the ecohydrological evolution of a shallow freshwater lake in the Yangtze floodplain. Sci. Total Environ. 621, 219–227. Zhao, K., Zhou, Y.F., Jiang, Z.L., Hu, J., Zhang, X.S., Zhou, J., Wang, G.X., 2017. Changes of aquatic vegetation in Lake Taihu since 1960s. J. Lake Sci. 29 (2), 351–362 (in Chinese). Zhang, Q., Dong, X., Yang, X., Odgaard, B.V., Jeppesen, E., 2019. Hydrologic and anthropogenic influences on aquatic macrophyte development in a large, shallow lake in China. Freshwater Biol. 00, 1–14. Zhong, J., Liu, M., Wang, Y., Yang, X., Jiang, X., Xu, C., 2014. Spatial correlation of major water quality indices between the lake and rivers in Lake Taihu basin. Chinese J. Ecol. 33 (8), 2176–2182 (in Chinese). Zhou, B.H., Zheng, B.H., 2008. Evaluation of water quality and nutrition status of the different parts in Taihu Lake Based on GIS. Environ. Protect. 10, 34–38 (in Chinese).

Hydrobiologia 784, 171–185. Korhola, A., Rautio, M., 2001. Cladocera and other Branchiopod crustaceans. In: Smol, J.P., Birks, H.J.B., Last, W.M. (Eds.), Tracking Environmental Change using Lake Sediments. 4. Zoological Indicators. Kluwer Academic Publishers, pp. 5–41. Korhola, A., Tikkanen, M., Weckström, J., 2005. Quantification of Holocene lake-level changes in Finnish Lapland using a cladocera–lake depth transfer model. J. Paleolimnol. 34, 175–190. Krause-Dellin, D., Steinberg, C., 1986. Cladoceran remains as indicators of Lake Acidification. Hydrobiologia. 143, 129–134. Li, J., Chen, F., 2010. Preliminary analysis on population decline of Daphnia in summer and autumn in Lake Taihu. J. Lake Sci. 22 (4), 552–556 (in Chinese). Li, W., 2004. Tendency and reason for evolution toward mash in the East Taihu. In: Qin, B., Hu, W., Chen, W. (Eds.), Process and Mechanism of Environmental Changes of Lake Taihu. Science Press, Beijing, pp. 33–51 (in Chinese). Lin, Q., Zhang, K., Shen, J., Liu, E., 2019. Integrating long-term dynamics of ecosystem services into restoration and management of large shallow lakes. Sci. Total Environ. 671, 66–75. Liu, G., Chen, F., Liu, Z., 2008. Preliminary study on cladoceran microfossils in the sediments of Lake Taihu. J. Lake Sci. 20 (4), 470–476 (in Chinese). Lotter, A.F., 1998. The recent eutrophication of Baldeggersee (Switzerland) as assessed by fossil diatom assemblages. The Holocene 8 (4), 395–405. Ma, J., Brookes, J.D., Qin, B., Paerl, H.W., Gao, G., Wu, P., Zhang, W., Deng, J., Zhu, G.W., Zhang, Y., Xu, H., Niu, H., 2014. Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in lake Taihu, china. Harmful Algae 31, 136–142. Ma, J., Qin, B., Paerl, H.W., Brookes, J.D., Hall, N.S., Shi, K., et al., 2016. The persistence of cyanobacterial (Microcystis spp.) blooms throughout winter in Lake Taihu, China. Limnol. Oceanogr. 61 (2), 711–722. Mao, Z., Gu, X., Zeng, Q., Zhou, L., Sun, M., 2012. Food web structure of a shallow eutrophic lake (Lake Taihu, China) assessed by stable isotope analysis. Hydrobiologia 683, 173–183. Meyers, P.A., 1994. Preservation of elemental and isotopic source identification of sedimentary organic matter. Chem. Geol. 114 (3–4), 289–302. Milecka, K., Szeroczyńska, K., 2005. Changes in macrophytic flora and planktonic organisms in Lake Ostrowite, Poland, as a response to climatic and trophic fluctuations. The Holocene 15 (1), 74–84. Nevalainen, L., Rantala, M.V., Luoto, T.P., 2015. Sedimentary cladoceran assemblages and their functional attributes record late Holocene climate variability in southern Finland. J. Paleolimnol. 54 (2–3), 239–252. Nevalainen, L., Kivilä, E.H., Luoto, T.P., 2016. Biogeochemical shifts in hydrologically divergent taiga lakes in response to late Holocene climate fluctuations. Biogeochemistry 128, 201–215. Nováková, K., Van Hardenbroek, M., Van, d.K.W.O., 2013. Response of subfossil cladocera in Gerzensee (Swiss Plateau) to early Late Glacial environmental change. Palaeogeogr., Palaeoclimatol., Palaeoecol. 391, 84–89. Paerl, H.W., Xu, H., Hall, N.S., Zhu, G., Qin, B., Wu, Y., Rossignol, K.L., Dong, L., McCarthy, M.J., Joyner, A.R., 2014. Controlling cyanobacterial blooms in hypertrophic Lake Taihu, China: will nitrogen reductions cause replacement of non-N2 fixing by N2 fixing Taxa? Plos One 9, e113123. Pawłowski, D., Płóciennik, M., Brooks, S.J., Luoto, T.P., Milecka, K., Nevalainen, L., Peyron, O., Self, A., Zieliński, T., 2015. A multiproxy study of Younger Dryas and Early Holocene climatic conditions from the Grabia River paleo-oxbow lake (central Poland). Palaeogeogr., Palaeoclimatol. Palaeoecol. 438, 34–50. Perga, M.E., Desmet, M., Enters, D., Reyss, J.L., 2010. A century of bottom-up- and topdown-driven changes on a lake planktonic food web: a paleoecological and paleoisotopic study of Lake Annecy, France. Limnol. Oceanogr. 55, 803–816. Philips, G., Bramwell, A., Pitt, J., Stansfield, J., Perrow, M., 1999. Practical application of

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