Crustacean zooplankton Cladocera are highly abundant in freshwater bodies worldwide. These Cladocera communities are sensitive to changes in the environment and climate (Korhola and Rautio, 2001; Szeroczyńska and Sarmaja-Korjonen, 2007; Pawłowski et al., 2015; Cheng et al., 2020a). The Bosminidae family belongs to Cladocera communities and is characterized by small body sizes (0.2–1.0 mm). They are ubiquitous on lake surfaces where the concentration of nutrients is relatively high (Zaret and Kerfoot, 1975; Jiang and Du, 1979; Zaret and Kerfoot, 1980; Threlkeld, 1981; De Melo and Hebert, 1994). The different species of the Bosminidae family exhibit unique adaptability to different nutritional environments (Jiang and Du, 1979; Szeroczyńska and Sarmaja-Korjonen, 2007). For example, Bosmina longirostris is commonly reported in eutrophic lakes, warming waters, and metal-contaminated lakes (Boucherle and Züllig, 1983; Balcer et al., 1984; Labaj et al., 2015; Adamczuk, 2016). Bosmina (E.) longispina can be used to indicate oligotrophic and mesotrophic environment changes (Deevey, 1942; Boucherle and Züllig, 1983; Miroslaw-Grabowska et al., 2015). However, due to the destruction of Bosminidae chitin fossils in the process of deposition, it is difficult to distinguish all the specific species of Bosminidae. Recent studies showed that the total number of Bosminidae, including both the eutrophic species Bosmina longirostris and oligotrophic and mesotrophic species Bosmina (E.) longispina, shows clear survival advantages in lakes with high trophic levels (Cheng et al., 2019, 2020b). For example, a large number of Bosminidae (a relative abundance greater than 80% in the total concentration of Cladocera) have been found in shallow eutrophic lakes in the subtropical zone (Liu et al., 2008; Wang et al., 2019; Cheng et al., 2020b). Furthermore, the abundance of Bosmina longirostris is usually greater than that of the species Bosmina (E.) longispina (Cheng et al., 2019, 2021) in eutrophic lakes. Therefore, we studied whether the Bosminidae can be used as a new indicator of the evolution of eutrophication in freshwater lakes in a subtropical region.

Since entering the Anthropocene, the impact of human activities on freshwater environments such as lakes has been increasing (Lin et al., 2020). Under the combined effects of anthropogenic activities (such as rapid industrialization and urbanization) and climate change, lakes in the middle and lower reaches of the Yangtze River in eastern China, which is located in a subtropical region with a relatively dense population and developed economy, have undergone drastic deterioration over a few decades (Qin et al., 2013; Zhu et al., 2019). Currently, these freshwater shallow lakes in the middle and lower reaches of the Yangtze River are a prominent area of environmental deterioration in China (Qin et al., 2013; Zhu et al., 2019). Furthermore, most lakes in this area have entered either a mesotrophic stage or a eutrophic stage, or in between, and are suffering serious cyanobacteria outbreaks that the stability and balance in the lake ecosystem are seriously disturbed (Zhu et al., 2019). For example, the biological composition of lakes has changed significantly, including the miniaturization of fishery structure, the reduction of aquatic plant area, cyanobacteria outbreaks, and a significant decline in biodiversity (Mao et al., 2012; Zhang K. et al., 2018; Jenny et al., 2020).

Taihu Lake (severe eutrophication), Nanyi Lake (transition from mesotrophication to eutrophication), and Shengjin Lake (mesotrophication) are located in the middle and lower reaches of the Yangtze River. They show significant differences in trophic level, area, and local economic development level and are representative of the research on the relationship between the evolution of zooplankton community and eutrophication. Therefore, in this study, we chose the three shallow freshwater lakes as our research object. Based on the research methods of paleolimnology and limnology, we focused on the indicative significance of Bosminidae in lake eutrophication in the three lakes since the 1950s. We analyzed the temporal and spatial changes in Bosminidae density and focused on revealing the adaptability and sensitivity of Bosminidae to lake eutrophication.

The lake trophic status in the lower reaches of the Yangtze River from a recent study showed that most of the lakes have been categorized into the mesotrophic or the eutrophic status (Cheng and Li, 2006; Qin et al., 2013). The trophic levels of the three lakes, located in the middle and lower reaches of the Yangtze River, have also reached the mid-eutrophic level and above and are increasing from Shengjin Lake to Nanyi Lake and then to Taihu Lake, which is closely related to the distribution of economic development, population, and urbanization in each region (Qin et al., 2013; Zhang M. et al., 2018; Shi et al., 2019; Cheng et al., 2020c, 2021). An analysis of modern zooplankton compositions showed that Cladocera was dominant in the three lakes and that the abundance was gradually increasing from Shengjin Lake through Nanyi Lake to Taihu Lake (Figure 2). Furthermore, the abundances of Bosminidae in the Nanyi Lake and in the western and central areas of the Taihu Lake were greater than 90% (Figure 2). This showed that Bosminidae abundance increased corresponding to the increasing trophic level (Li et al., 2016; Cheng et al., 2020b; Li et al., 2021). However, a higher Copepod density was recorded in summer than that of Cladocera and there was a low abundance of Bosminidae in the composition of modern zooplankton in the Shengjin Lake, which might indirectly suggest that the Bosminidae did not have a reproductive advantage under low trophic levels. The subfossil Cladocera in the sedimental cores of the three lakes also showed that the Bosminidae was a broadly dominant species (Figure 5). Especially in Taihu Lake, the density of Bosminidae subfossils was close to 10,000 ind./cm³ (Cheng et al., 2019). In Nanyi Lake and Shengjin Lake, where trophic levels had increased significantly since the 1950s, the abundance of subfossil Bosminidae also increased (Figure 5). In addition, among the modern Cladocera in the three lakes, Bosminidae was the dominant species, which was consistent with the Cladocera subfossil results at the same location and also indirectly proved that Bosminidae subfossils were well preserved in lakes of the middle and lower reaches of the Yangtze River.

In terms of space, there were huge differences in the economic development level, the urbanization level, and population along the Yangtze River from west to east. Taihu Lake is located in the eastern delta of the Yangtze River, which has an extremely developed economy and a very large population (Qin et al., 2007). Because Taihu Lake is located near many developed cities such as Shanghai, Suzhou, and Wuxi, a large quantity of nutrients such as nitrogen and phosphorus flow into Taihu Lake on account of human activities, which are far greater in Taihu Lake than in Nanyi Lake and Shengjin Lake in the Anhui Province (Dai et al., 2016). Agricultural and fisheries development in Nanyi Lake is more adequate than in Shengjin Lake (Wang et al., 2013). As a national nature reserve, Shengjin Lake has a relatively good environment and low nutrient level compared with the other two lakes (Wang et al., 2015). The spatial gradient distributions of Bosminidae abundance in the three lakes were in line with the different economic development levels (Figure 5). Thus, it could be inferred that there were different types of interference of human activities around the three lakes.

The significant positive relationship between Bosminidae and eutrophic species B. longirostris with TN and TP further proved that Bosminidae had an advantage in the eutrophic process (Table 2). In particular, B. longirostris demonstrated strong adaptability and sensitivity in a wide range of water environments, such as the eutrophic status, warming waters, and metal-contaminated lakes in previous studies (Boucherle and Züllig, 1983; De Kluijver et al., 2012; Labaj et al., 2015; Kong et al., 2017; Cheng et al., 2020b). Our study showed that Bosminidae abundance increased with the increase in the outbreak intensity of cyanobacteria in eutrophic lake areas (Figures 3, 4). Especially in the west and central lake areas of Taihu Lake with serious eutrophication, the concentration of Bosminidae has increased to a relatively stable state. While Nanyi Lake and Shengjin Lake are in the stage of rising trophic levels, and the abundance of Bosminidae is also showing a synchronous rising trend (Figure 3). Although previous studies suggested that Bosminidae were too small to feed on Microcystis directly with a large size (Jiang and Du, 1979; Li and Chen, 2010), more studies showed that Microcystis tended to form large suspended aggregates with materials after cell death including dissolved organic carbon, dissolved inorganic carbon, and dissolved inorganic nitrogen and phosphorus in the water column and then were likely the main diet of Bosminidae (De Kluijver et al., 2012; Agasild et al., 2019; Cheng et al., 2020b). It could be speculated that cyanobacteria blooms might change the food preference of the zooplankton Bosminidae. At the same time, the water environment also changed greatly due to excessive reproduction of cyanobacteria; thus, Bosminidae made timely adaptive adjustments to the original living environment and food source changes (Agasild et al., 2019). For example, Cladocera’s size gradually became smaller to better escape the predation of zooplankton-feeding fish (Shurin, 2001; Jeppesen et al., 2003; Liu et al., 2009). Accordingly, in lake areas where cyanobacteria blooms were stronger, the density of small-size species of Bosminidae was greater and other species of zooplankton may have decreased or even gone extinct (Jiang et al., 2013; Li et al., 2016).

The present study revealed that Bosminidae could accelerate reproduction under rich food sources, resulting in excessive abundance (accounting for more than 90% of the total number of Cladocera) (Figure 2). However, water temperature also impacts the body size and community trophic structure of zooplankton (Gao et al., 2021). The three shallow freshwater lakes located in the middle and lower reaches of the Yangtze River in a subtropical zone had suitable temperature conditions that produced a favorable habitat for most lake creatures, including the zooplankton. However, a strong disturbance can easily occur in these shallow freshwater lakes, which can result in the release of sediment nitrogen and phosphorus and a large amount of exogenous nitrogen and phosphorus inputs from catchment by increasing human activities (Zhu et al., 2019). Excessive nitrogen and phosphorus inputs caused cyanobacteria blooms that seriously threatened the survival of most aquatic organisms such as fish. Large aquatic plants and other biodiversity significantly decreased, and this finally led to the imbalance of lake ecosystems (Qin et al., 2013). Surprisingly, the cyanobacteria outbreak provided favorable conditions for the expansion of the Bosminidae (De Kluijver et al., 2012; Cheng et al., 2020b). The changes in δ¹³C_bos values after 1950s also revealed the flow characteristics of carbon sources in the Bosminidae (Figure 6). In particular, after the 1980s (after China’s Reform and Open Policy), with increasing lake eutrophication, the δ¹³C_bos values exhibited a significant negative trend (Figure 6), which was consistent with the change in organic carbon isotopes in sediments (δ¹³C_org; Cheng et al., 2020b). The δ¹³C value of algae in Taihu Lake was similar to the value of δ¹³C in modern Bosminidae during the cyanobacteria bloom (Cheng et al., 2020b). This further indicated that the cyanobacteria outbreak provided a rich food source for Bosminidae. Bosminidae propagation in large numbers due to the outbreak of cyanobacteria also showed that Bosminidae had its own unique adaptability to the eutrophic environment and strong competitiveness compared with other zooplankton. The high adaptive ability of Bosminidae to eutrophication could indicate that it is more competitive than other larger Cladocera species.

Our data on subfossil Cladocera in the TH-5 core of East Taihu Lake showed that the total Cladocera and Bosminidae abundances were lower than those found in the core of other lake areas and tended to decrease after the 1950s (Figure 2). This was due to intensification of the swamping trend in East Taihu Lake, the water level reduction, aquatic macrophyte development, and water stagnation for prolonged periods of time caused by enclosed fish cultures and crab farming practices. These are extremely detrimental to the survival of the planktonic species Bosminidae but provide a more suitable habitat for the littoral Cladocera species (Yang et al., 2003; Li, 2004; Cheng et al., 2020a). The significant negative correlation between Bosminidae and TP also indirectly proved that the environment of the East Taihu Lake was not conducive to the survival of Bosminidae (Table. 2). It could be seen that the trophic level was not the only factor limiting the growth of Bosminidae, but it was the key factor behind the rapid expansion of Bosminidae, once certain restrictive conditions were exceeded. As shown in the western and central areas of Taihu Lake, Bosminidae reproduction expanded and abundance increased once the trophic level was enriched and the water level depth met the living conditions of the planktonic species Bosminidae (Figures 2, 5). Additionally, the significant positive correlations between oligotrophic species Bosminidae with TN and TP in Nanyi Lake were opposite of those in Taihu Lake, which was closely related to the fact that Nanyi Lake was in a critical period of transition from the mesotrophic to the eutrophic status (Cheng et al., 2021). Research by Dodson (1992) showed that the abundance of zooplankton usually increased with increasing nutritional levels within a certain range. The current trophic level of the Nanyi Lake is still increasing, but it has not reached the eutrophic level as in the central and western areas of Taihu Lake. Therefore, the abundance of oligotrophic species increased significantly with the increase in trophic level.

The spatial distribution of the three subtropical shallow freshwater lakes in the middle and lower reaches of the Yangtze River was characterized by gradually increasing nutrient levels from west to east. An analysis of the composition of zooplankton in the modern lake water of the three lakes and Cladocera subfossils from the sedimental cores revealed that the Cladocera planktonic species Bosminidae changed relatively consistently with the temporal and spatial distributions of the nutrient levels in the three lakes, indicating that the small planktonic Bosminidae species had unique sensitivity and adaptability during lake eutrophication. In addition, the significant correlation between Bosminidae and nutrient indicators such as TN and TP, as well as the gradually negative δ¹³C_bos values under increasing eutrophication, further proved that the abundance of Bosminidae changed with the change in eutrophication level. This reflected the change in food source preference of the Bosminidae and its strong adaptability to harsh environments during lake eutrophication. Bosminidae was more adaptive to the change in this environment, which showed that the genus was highly sensitive to changes in the lake environment and can indicate the evolution of the lake. This study offered a new alternative index for paleoecology research and also provided a new idea for mechanism research on modern lake eutrophication environments.

The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding authors.

LC: writing–original draft, validation, resources, and formal analysis. XG, GW, and JL: visualization and investigation. ZD: investigation and field work. BX: supervision, project administration, and funding acquisition. CZ: supervision, visualization, investigation, and writing–editing. QJ: software and resources. All authors contributed to the article and approved the submitted version.

This research was supported by grants from the Natural Science Foundation of China project (42002204 and 42177426), the National Key Research and Development Program of China (2019YFA0607100), and the Jiangsu Special Fund on Technology Innovation of Carbon Dioxide Peaking and Carbon Neutrality (BK20220016).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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