Introduction

Rotifers constitute a high proportion of the freshwater zooplankton population and contribute significantly to maintaining the structure and function of aquatic ecosystems and secondary productivity (Hu 2000). With their small size, short development time, high turnover rate, and large numbers (Herzig 1987), rotifers form a vital link in the aquatic food chain and thus play an important role in energy flow and nutrient cycling in aquatic ecosystems. They can act as predators, capable of regulating the populations of phytoplankton, protozoan, and bacteria, and as an appropriate food source for a variety of fish and aquatic creatures (Offem et al. 2009; Fernando 1994). Their quick response to environmental changes, short generation time, and rapid population reconstruction make them ideal biological indicators of water quality and nutritional status, and they thus play an important role in these areas (Mäemets 1983; Duggan et al. 2001). The temporal and spatial variations in rotifer community structure may be affected by biological factors such as food source, predation, and competition and non-biological factors such as temperature, pH, and dissolved oxygen (DO) (Arnott and Vanni 1993; Yoshida et al. 2003; Yang et al. 2009).

Shengjin Lake (116° 55′–117° 15′ E and 30° 15–30° 30′ N) is lying on the south bank of the Yangtze River in the Anhui Province, China. The lake has a surface area of 13,300 hm2 and consists of three parts, upper, middle, and lower, covering areas of 5800, 5200, and 2300 hm2, respectively. The lake climate is subtropical monsoonal, with annual average precipitation of about 1600 mm and most rain falling from May to August (Hu et al. 2004). This region is subject to monsoonal flooding in summer followed by low water levels during autumn and winter. The variable hydrological cycle creates an expansive area of multiple shallow ephemeral wetlands, with their ecosystems significantly affected by the temporally alternating flooding and drying (Cheng et al. 2009). Furthermore, the periodic hydrological changes could significantly affect phytoplankton community structure by influencing water transparency, nutrient concentrations, water thermocline, and aquatic plant communities. Usually, there is a gradual increase in the water temperature of Shengjin Lake from February to July, reaching a peak in July. The water level rises from May onwards, reaching a peak at the end of July and into August (Zhu and Zhou 2010); thus, these shallow wetlands are usually inundated in June.

Previous studies, however, have focused primarily on the behavior of the wintering waterbirds and the structure of the rotifer community. For example, Zhou et al. (2009) investigated the community structure and territorial behaviors of the lake’s Grus monacha population in 2007–2008, while Zong et al. (2008) reported on rotifer community structure.

It is reported that seabirds can transport large quantities of nutrients in Arctic ponds and the seabird-derived nutrients played a dominant role in driving aquatic primary production (Michelutti et al. 2010). Ptacnik et al. (2008) also indicated that the large amount of droppings from penguins in Antarctic provided abundant nutrients for the lakes and influenced the lake trophic levels and the phytoplankton community structure. During the low-water-level season each year (from December to March), the upper part of Shengjin Lake has shallow muddy or grassy zones (Fig. 1). More than 11 km2 of shallow zones provide a habitat for wintering waterbirds (Yang et al. 2011). More than 70,000 waterbirds dwell on these zones in the winter, among which 86 % are Anatidae. The central and southern areas of the upper lake are the most important regions for waterbirds, hosting 70–90 % of the birds inhabiting Shengjin Lake (Cheng et al. 2009) (Fig. 1). On average, there are about 873.6 t of droppings during the whole wintering period (from November to March) from those waterbirds in the central and southern areas of the upper lake, according to the correlation coefficient of ducks provided by the State Environmental Protection Administration of China No. 43 (Liu et al. 2011), Therefore, the emissions of total phosphorus (TP), NH4 +-N, chemical oxygen demand (COD), and biochemical oxygen demand (BOD) from their droppings are nearly 5.4, 0.7, 40.4, and 26.2 t, respectively. Therefore, it clearly shows that waterbird droppings could influence rotifer growth and community structure.

Fig. 1
figure 1

Key waterbird areas identified during the wintering period (Cheng et al. 2009)

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In this study, we monitored Shengjin Lake’s rotifer species composition, dominant species, rotifer density and biomass, species diversity, and environment parameters from February to July 2014 in the upper region of Shengjin Lake. We then analyzed the main environmental factors affecting rotifer community structure and also discuss the influence of environmental factors including migratory birds on the rotifer community and biomass. The results may provide some insights into the evaluation of the water environment, rational utilization of fishing resources, and environmental protection in Shengjin Lake.

Materials and methods

Study site

The Shengjin Lake National Nature Reserve (116° 55′ E–117° 15′ E, 30° 15′ N–30° 30′ N) is a wetland area located in Dongzhi and Guichi counties in Anhui province, China. Connected to the Yangtze River by the Huangpen Channel, it covers an area of approximately 133 km2 in the wet season and only 33 km2 in the dry season. The area has a subtropical monsoon climate with a hot and humid summer and a cold and dry winter; its average annual temperature is 16.14 °C. Rainfall and surface runoff are abundant, with an annual average precipitation of 1600 mm (Zong et al. 2008; Xu et al. 2008). In addition to its role as a winter habitat for migratory waterbirds, the lake also serves as an important flood storage/discharge reservoir and natural fishing ground. Topographically, it can be divided into three parts: the upper lake to the south of Xiaoluzui, the lower lake to the north of Babaizhang, and the middle lake located between these two villages.

Sample collection and treatment

Samples were collected at 13 stations in the upper Shengjin Lake monthly from February to July in 2014 (Fig. 2). For qualitative analysis, rotifer samples were collected by slowly dragging a plankton net, mesh size 64 μm in a fig. 8 (∞) shape, for 3 min, 0.5 m below the water surface. The water in the plankton net was then concentrated to 50 mL and fixed with 4 % formaldehyde solution. For quantitative analysis, a water sampler was used, from the lake surface to the bottom at intervals of 1 m. One-liter samples of mixed water were fixed with 1 % Lugol’s iodine solution, precipitated in our lab for 48 h, concentrated to 50 mL, and kept with several drips of 4 % formaldehyde solution (Deng et al. 2012).

Fig. 2
figure 2

The geographic location of Shengjin Lake and the distribution of sampling point

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The number and biomass of rotifers were determined as previously described (Zhang and Huang 1991).

Determination of physicochemical factors

A multi-parameter water quality analyzer (HI9828) was used for the field measurement of dissolved oxygen (Hach, America), pH (EL2; Mettler Toledo, Switzerland), conductivity (EL2; Mettler Toledo, Switzerland), turbidity (Hach, America), and water temperature (T) at each sampling station. Samples were taken back to the lab and tested for the following:

  • Total nitrogen (TN), using the UV spectrophotometric method with alkaline potassium persulfate digestion

  • TP, using the UV spectrophotometric method with potassium persulfate digestion

  • Ammonia nitrogen, using the Nessler’s reagent spectrophotometry

  • Nitrite and nitrate nitrogen, using the UV spectrophotometric method

  • Phosphate (PO3 −4), using the molybdenum blue method

  • COD, using the potassium dichromate method

  • Five-day BOD (BOD5), using the dilution and seeding method

  • And chlorophyll a, using the 90 % acetone extraction method according to the Surface Water Environment Quality Standard (GB3838-2002)

Data processing and statistical analysis

The dominant species of rotifers were determined based on the following formula:

$$ Y=\frac{n_{\mathrm{i}}}{N}\times {f}_{\mathrm{i}} $$
(1)

where n i is the total number of individuals species i, f i is the occurrence frequency of species i, and N is the total number of rotifers in all samples.

Species with Y ≥ 0.02 is considered to be the dominant species (Xu et al. 1995).

Rotifer diversity can be indicated by the Shannon-Wiener index (H′):

$$ H\hbox{'}=-{\displaystyle \sum_{i=1}^s{P}_i{ \log}_2{P}_i} $$
(2)

where S is the number of rotifer species and P i is the ratio of rotifer species density i to total density (Yang et al. 2014).

Correlations between rotifer species and environmental factors were determined using multivariate analysis with Canoco for Windows 4.5. Detrended correspondence analysis (DCA) was performed from February to July to calculate the lake’s rotifer gradient distribution. The largest gradient length of the DCA ordination axis was greater than 3 (3.405); thus, canonical correspondence analysis (CCA) was then performed.

Results

Physicochemical factors

Table 1 shows the mean environmental factor values along with the range of the sites investigated in 2014. The water is slightly alkaline with a pH ranging from 7.84 to 9.41. Water temperature ranges from 10.6 °C in February to 34 °C in July; depth ranges from 0.28 to 7.20 m, with a mean depth of 2.27 m; water transparency ranges from 0.25 m in February to 1.97 cm in July. A high level of DO (range 7.38–13.73 mg/L; mean 10.71 mg/L) is observed. The highest average concentration of chlorophyll a is recorded in June (18.135 μg/L) and the lowest in February (0.279 μg/L). The average concentration of TN and TP is 5.01 and 0.072 mg/L, respectively, with the highest concentration of TN and TP recorded in March and April, respectively (Table 1).

Table 1 Mean and range of physicochemical factors of Shengjin Lake
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Temporal and spatial variations in the main water quality indicators of the five sections of the upper lake are displayed in Fig. 3. During the study period, nutrient concentrations in sections A, B, and E were higher than in other sections, perhaps because of inputs of human sewage discharge and droppings from poultry and wintering waterbirds.

Fig. 3
figure 3

Temporal variations of sections A–E in the main water quality indicators in the upper lake of Shengjin Lake in 2014. WD water depth, TP total phosphorus, NH 4 + -N ammonia nitrogen, BOD 5-day biochemical oxygen demand, COD chemical oxygen demand, DO dissolved oxygen

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Species composition and Shannon-Wiener index (H′) of rotifers

A total of 17 genera and 31 species of rotifers were identified, including 8 species of Brachionus that accounted for approximately 18.3–86.9 % of the total rotifer density. Brachionus calyciflorus, Brachionus angularis, A. priodonta, and Polyarthra trigla were observed throughout the survey, with B. angularis always dominant. The degree of dominance by the dominating species in each month is shown in Table 2. The Shannon-Wiener index (H′) was lowest (1.49) in March, when the dominance values of B. calyciflorus and B. angularis were 0.634 and 0.199, respectively. Dominance in the other months ranged from 2.03 to 2.31, with the highest (2.31) observed in May.

Table 2 Dominant species and their degree of dominance
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Rotifer density and biomass

The lowest biomass (11.92 mg/L) and density (14.0 ind./L) were observed in April. The highest biomass (793.10 mg/L) was observed in July, 94.7 % of which could be attributed to A. priodonta. The highest density (176.0 ind./L) was observed in June, with 36.8, 27.0, and 17.1 % attributed to Brachionus forficula, B. angularis, and Trichocerca cylindrica, respectively (Fig. 4).

Fig. 4
figure 4

Average density and biomass of rotifers from February to July in Shengjin Lake

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Sampling stations 2, 5, 8, 11, and 13 were located in the deep water of the central part of the lake, whereas stations 1, 3, 4, 6, 7, 9, 10, and 12 were located in the shallow lakeshore waters. Figure 5 clearly shows that rotifer density was slightly higher in the lake center than near the shores.

Fig. 5
figure 5

Average rotifer density and biomass from February to July in different parts of Shengjin Lake

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These 13 sampling stations fall into five cross sections: stations 1–3, 4–6, 7–9, 10–11, and 12–13 were selected and classed as sections A, B, C, D, and E, respectively. Rotifer density in each section was low in February and decreased from sections A to E; in March, rotifer density was the highest in section E, followed by sections A and B and then by sections C and D. In April, the density in each section was very low, whereas in May, it increased slightly from sections A to E. In June, rotifer density was high and comparable in all sections. In July, it was higher in section A, but relatively lower in the other sections (Fig. 6).

Fig. 6
figure 6

Average rotifer density and biomass from February to July in different parts of Shengjin Lake

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Relationship between rotifers and environmental factors

The changes in environmental factors from February to July and the CCA biplot with rotifers are shown in Table 1 and Fig. 7. A total of 14 environmental factors and 16 rotifer species were included in the analysis (Table 2). The CCA ordination results showed that the eigenvalues of the first two CCA ordination axes were 0.456 and 0.306, respectively, with a correlation coefficient between rotifer species and environmental factors being as high as 0.965 and 0.914, respectively, indicating that the CCA ordination biplot provided an adequate description of the relationship between rotifer species and environmental factors in Shengjin Lake.

Fig. 7
figure 7

CCA biplot of rotifer species and environmental factors

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Arrow length in Fig. 7 was proportional to correlation strength between environmental factors and rotifer species. During the survey period from February to July, rotifers showed a strong response to water transparency, temperature, and depth and to pH, suspended matter, and nitrate nitrogen. The correlation coefficients of suspended matter, temperature, depth, pH, and transparency with the first CCA ordination axis were 0.5173, −0.9128, −0.6929, −0.6022, and −0.6090, respectively, while the coefficients of nitrate and nitrite nitrogen with the second axis were 0.6898 and 0.4005, respectively. Brachionus falcatus correlated positively with transparency, water depth, and temperature. B. forficula and T. cylindrica correlated positively with chlorophyll a and pH and negatively with nitrate nitrogen. Brachionus urcens and Brachionus capsuliflorus correlated negatively with nitrite nitrogen, while Keratella quadrata, Keratella valga, and Notholca labis correlated negatively with transparency, water depth, and temperature.

Rotifer density correlated positively with BOD, COD, and Secchi depth (SD) (P < 0.05) and with chlorophyll a, temperature, pH, and water depth (P < 0.01), though negatively with NO3-N (P < 0.01). Rotifer biomass correlated positively with BOD, chlorophyll a, temperature, DO, pH, SD, NO2-N, and water depth (P < 0.01), but negatively with suspended solids (SS) (P < 0.01).

Discussion

Rotifer community structure in Shengjin Lake

A total of 17 genera and 31 species of rotifers were identified in Shengjin Lake during the survey, which was 8 species fewer than in 2006 (Zong et al. 2008). The major species included eurytopic Brachionus, Triarthridae, and Keratella. The indicator rotifer species for the eutrophic lake include Brachionus, Anuraeopsis fissa, Pompholyx sulcata, Pompholyx complanata, T. cylindrica, Trichocerca pusilla, Filinia longiseta, Keratella cochlearis, K. quadrata, and Polyarthra euryptera (Gannon and Stemberger 1978; Hacerman 1998; Geng et al. 2003). Brachionus was the most dominant genera, and B. angularis the dominant species in each survey from February to July, indicating that Shengjin Lake was becoming increasingly eutrophic. The average Shannon-Wiener index from February to July is 2.04, with the dominant species B. calyciflorus at 0.634, with a Shannon-Wiener index of 1.49 in March. It is noteworthy that low rotifer diversity does not necessarily indicate instability of the rotifer community structure, but rather the scarcity of suitable niches. Rotifer density is highest in June, the dominant species being B. angularis, B. forficula, and T. cylindrica, with a dominance of 0.270, 0.368, and 0.170, respectively. The low individual biomass results in a low biomass of the entire rotifer community in June.

Due to their habits that induce them to move towards the deep waters of the center of the lake, rotifers are generally more numerous there than in the shallow lakeshore zones, a phenomenon also observed by Preißler (1977). It has been suggested that a difference in one or more environmental factors may result in a significant difference in rotifer community structure (Rao et al. 2013; Du et al. 2014). Various findings in this direction have been published:

  • Temperature, DO, and pH have been found to be the main factors influencing zooplankton community structure in the Songhua River in Harbin (Li et al. 2014a, b).

  • Temperature, DO, chlorophyll a, and nutrient salt concentration appear to be the main factors influencing the rotifer community structure in Hongze Lake (Du et al 2014).

  • Temperature, organic content, pH, and nutrient salt concentration have been identified as the main factors influencing the community structure and spatial and temporal distribution of rotifers in Mingcui Lake (Qiu et al. 2012).

In this study, CCA analysis showed that SD, temperature, water depth, pH, SS, and nutrient salt concentration had a considerable effect on rotifer community structure in Shengjin Lake, thus indicating a significant relationship between rotifer distribution in Shengjin Lake and environmental factors. The ecological distribution of rotifers also helps to explain the adaptability of different rotifer species to different aquatic environments.

Effect of overwintering waterbirds on rotifer community structure in Shengjin Lake

Rotifer density in Shengjin Lake is affected primarily by physicochemical conditions and food resources. Consisting mainly of grasslands, intertidal zones, and shallows formed in the dry season (Chen and Zhou 2011), the lake area is inhabited by several hundred thousand overwintering waterbirds from the early October to the end of April the following year (Jiang et al. 2007).

The sampling stations in section E are near the habitat of the migratory birds, where their abundant droppings provide an important source of nutrient salt for the lake. These droppings in the grasslands and intertidal zones are brought into the lake by water runoff, resulting in a further increase in nutrient salts in the lake water. The levels of COD, DO, NO3-N, SS, BOD5, and TP are highest in section E (Fig. 3), thus promoting additional growth and development of phytoplankton (Gong et al. 2012). In sections A–E, the chlorophyll a content is 3.63, 2.51, 1.02, 2.23, and 9.35 μg/L, respectively. Chlorophyll a content is an important indicator of the standing crop of algae (Chen et al. 2009) which, in turn, provides abundant food for rotifers; thus, rotifer density is the highest in section E. B. calyciflorus, B. angularis, K. quadrata, and K. valga correlated positively with NO3-N, TP, DO, SS, and COD (Fig. 7). B. calyciflorus, B. angularis, K. quadrata, and K. valga were the dominant species in March (Table 2).

The Shannon-Wiener index is 1.06 in this section, which is far lower than the mean of 1.49, and the density of the dominant species B. calyciflorus is 161 ind./L, which is far greater than the mean of 67 ind./L. B. calyciflorus is usually present in waters with a temperature >13–15 °C, a low concentration of ammonia, and a high concentration of dissolved oxygen (Roche 1995). In this study, the ammonia concentration in section E (0.61 mg/L) is lower than the mean (0.95 mg/L) and the concentration of DO (13.08 mL/L) is higher than the mean (11.38 mL/L), probably due to the droppings produced by the overwintering birds. This contributes significantly to the growth and development of B. calyciflorus in spring. With the increased level of bird droppings from grassland and tidal zone runoff in May and June, rotifer density rises in all sections. In May, the population increases very rapidly in waters at a temperature >20 °C and more than 2 m deep. In June, the lake water is well mixed; thus, rotifer density is high and comparable across all the sections.

Effect of aquaculture on the rotifer community structure

Rotifers can serve as the primary food source for a variety of fish and aquatic creatures; thus, any change in the fish type may have a considerable effect on the community structure (Yang et al. 2011; Offem et al. 2009; Fernando 1994). The predation of fish appears to be a critical determinant in the density, structure, and succession of the zooplankton community (Li et al. 2014a, b). In addition, fish farms may pose a significant threat to the survival of rotifers due to large stocks and long growth time (Yang et al. 2008). Ecological aquaculture is practiced in the upper Shengjin Lake, with no supplementary artificial diet. The main types of fish are the filter-feeding bighead carp and silver carp, with phytoplankton and rotifers serving as the main food source with an annual output of approximately 2000 tons (Mou et al. 2012). A large number of minnows are released into the Shengjin Lake in April, resulting in a significant reduction in the average density of rotifers that month and indicating that predation by fish has a significant effect on rotifer community structure.

Conclusions

Shengjin Lake is an important wintering and stopover habitat for migratory birds en route from East Asia to Australia. In this study, a total of 17 genera and 31 species of rotifers were identified, the dominant species being B. angularis, B. calyciflorus, A. priodonta, and S. diversicornis. The highest density (176.0 ind./L) was recorded in June, the lowest (14.0 ind./L) in April. Rotifer density was slightly higher in the lake center than near the shores. Canonical correspondence analysis (CCA) and correlation analysis showed that some environmental factors, such as temperature, pH, water depth, SD, and chlorophyll a concentration had a considerable effect on the lake’s rotifer community structure. Rotifer density and the nutrient salt content were higher in the areas inhabited by migratory birds. The sampling stations in section V are near the habitat of the migratory birds, where their rotifer density is the highest. A large number of minnows are released into the Shengjin Lake in April, resulting in a significant reduction in the average density of rotifers that month and indicating that predation by fish has a significant effect on rotifer community structure.