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Environmental Sciences ProcediaProcedia Environmental Environmental Sciences Sciences 8 (2011 13) 1126(2012)–1136 1099 – 1109 www.elsevier.com/locate/procedia

The 18th Biennial Conference of International Society for Ecological Modelling Structure of the zooplankton community in Hulun Lake,

X.P. Ana, Z.H. Dub, J.H. Zhangb, Y.P. Lib, J.W. Qia*

a College of Animal Science in Agricultural University, hohhot 010018,China b Station for Agricultural Technique Popularization in Inner Mongolia, hohhot 010018,China

Abstract

The study investigated the composition, community structure and diversity of zooplankton in Hulun Lake from January to October in 2009. The water quality and the type of nourishment of the lake were analyzed. The results showed forty one species of zooplankton were found, of which eighteen species were rotifera (43.9%), fourteen species were protozoa (34.1%), five species were copepoda (12.2%), three species were cladocera (7.3%), one species was ostracoda (2.4%). Among zooplankton, particularly protozoa were the dominant group throughout the study period and highest count was recorded in June while low incidence was observed in October. Zooplankton community is also correlated with physicochemical parameters. According to the dominant species and the ShannanWeiner diversity index, Hulun Lake was mesotrophic water.

© 20112011 Published Published by by Elsevier Elsevier B.V. Ltd. Selection and/or peer-review under responsibility of School of Environment, Beijing Normal University. Key words: Hulun lake, Zooplankton, Dominant species, mesotrophic water;

1. Introduction

Zooplankton plays an important role in aquatic ecosystem. They perform several vital functions within lake ecosystems including the transference of energy and nutrients from producers to secondary consumers, the sequestration of nutrients, and the removal of phytoplankton from the water column. The filtering capacity of zooplankton has significant implications for the eutrophic state of a lake. Zooplankton community structure (species density and species composition) is potentially affected by both “natural” lake water chemistry and lake morphology, and anthropogenic changes in lakes and watersheds [1-3].

* Corresponding author. Tel.: 13804746541 E-mail address: [email protected].

1878-0296 © 2011 Published by Elsevier B.V. Selection and/or peer-review under responsibility of School of Environment, Beijing Normal University. doi:10.1016/j.proenv.2012.01.103 1100 X.P.X.P. An Anet al. et/ al. Pr ocedia/ Procedia Environmental Environmental Sciences Sciences 8 (2011 13 (2012)) 1126 1099–1136 – 1109 1127

Thus, the zooplankton heterogeneity and community structure are an important focus in aquatic ecological research. From a management perspective, a diverse and plentiful zooplankton community is desirable for the maintenance of a lake‟s aesthetics. However, there has been no hydrobiological study of the Hulun Lake and its development for conservation requires the completion of such study. Hulun Lake (48°31′- 49°20′N, 116°58′- 117°48′E) lies in the south of City, Inner Mongolia, China. It is the fifth largest fresh-water lake in China, and also the largest lake in the furthest north China, with the size of 2339 km2, and the deepest water level of 9 m [4]. The lake is located the arid/semiarid areas and being threatened by severe drought, desertification and dust, sand storm [5]. The lake is fed by direct precipitation, most of which is focused in July and August all around the year although the lake lies beyond the present Pacific monsoon limits, and over 80 rivers, of which the largest three are the Crulen, Orshun and Hailaer Rivers. The Crulen River originates in Mongolia, the Orshun River flows from the nearby Buirnur Lake on the Sino-Mongolian border, and the Hailaer Riveris from the east part of the Hulun Basin. There is an outflow from Hulun Lake via the Erguna River. Ice usually forms in the first half of November and melts in the first half of May in Hulun Lake. In recent years, with climate changing and the regional economy developing, this water body is under constant threat due to scanty rains and increased human activities. To avoid potential misuse of the resources of the lake, it has been declared as a protected area by the national government, thus enabled to monitor and control the amount of human activity in the lake. In the present study, we investigated the pelagic zooplankton to assess the lake‟s trophic status and to determine the best way to use and protect it. Zooplankton composition and abundance are excellent indicators of trophic status. Studying the taxonomic composition and abundance of zooplankton populations will provide a basis for sustainable development of fishery resources and water protection of Hulun Lake.

2. Materials and Methods

The study was continued for a period of one year from January to October in 2009. The samples were taken from eight stations, which were defined to characterize whole Hulun Lake (Fig 1). Water samples collected for the purpose of estimation of various parameters were brought to the laboratory and subjected to analysis immediately as fast as possible. Standards Methods for Estimation of Water and Wastewater were referred for estimation of parameters viz., Water temperature, pH, Alkalinity, Total Hardness, + - 3- Salinity, Ammonical Nitrogen (NH4 -N), Nitrate Nitrogen (NO3 -N), Phosphorus (PO4 ) and Biochemical Oxygen Demand (COD) [6].

Fig.1 Map of Hulun Lake, indicating the eight sampling sites

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Collecting and processing the zooplankton samples followed established standards [7]. For qualitative analysis of zooplankton, samples were collected by means of horizontal haul, using plankton net (No.25) with a mesh size of 64 μm. Collected samples were transferred to labeled vial bottles containing 4% formalin. Zooplankton samples were identified to the lowest taxonomic units possible. Identification of zooplankton species was based on relevant literatures [8, 9]. Statistical analyses were done for zooplankton density at each sampling point and months as well as a correlation analyses (r-Pearson, p < 0.05) with physicochemical data. ShannonWeinner index was analyzed for zooplankton community diversity.

3. Results

3.1. Physico-chemical environment

Table 1 presents the values recorded for physicochemical variables in the samplings carried out in the study period. Temperature is an important factor which controls all chemical reactions and biological processes in a water body. During the current study period, water temperature varied between 3.7 and 21.2 °C, with high values in Aug. and low Jan. The pH values indicated an alkaline condition, with pH ranging between 8.89 and 9.29. The higher pH value was observed after ice-bound period could be attributed to enhanced rate of evaporation and photosynthetic activity. The maximum value of alkalinity was observed in January while minimum in October. Alkalinity ranged between the lowest value of 867 and the highest value of 1790 mg/l. Total hardness values were between 62.0 and 190.7 mg/l. The Hulun Lake water is moderate hard water conditions, which in turn useful for the higher productivity. During the study period, the salinity of the Hulun Lake ranged from 2076.6 to 3149.7 mg/l. The highest value caused by ice-sheet was recorded in January. The values of COD varied between 14.80 and 22.74 mg/l, the high value of COD was probably due to the addition of waste [10]. The concentration of ammonia nitrogen content was ranged between 0.64 mg/l and 0.81 mg/l. Average nitrate nitrogen content was ranged between 0.03 mg/l to 0.04 mg/l. Average phosphate values were ranged between 0.06 mg/l to 0.23 mg/l. The annual mean value of the N: P (nitrate nitrogen: phosphate ratio) was 0.33.

Table 1 Average values of physico-chemical variables

Parameters Jan. June Aug. Oct. Water Temp. °C 3.7 16.1 21.2 5.8 pH 8.89 9.08 9.32 9.29 Alkalinity (mg/l) 1499.3 1035.3 1035.8 998.1 Total Hardness (mg/l) 166.3 116.7 126.7 115.9 Salinity (mg/l) 3149.7 2153.1 2157.0 2076.6 COD (mg/l) 22.51 14.80 22.74 20.93 + NH4 -N (mg/l) 0.81 0.81 0.64 0.79 - NO3 -N (mg/l) 0.04 0.03 0.04 0.04 3- PO4 (mg/l) 0.20 0.23 0.06 0.14

3.2. Zooplankton community

The zooplankton of Hulun Lake was composed of protozoa, rotifera, copepod, cladocera and ostracods, and the total 41 species were recorded during the present study (Table 2). Out of 41 species, 18 species

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belongs to rotifera, 14 species belongs to protozoa, 5 species belongs to copepoda, 3 species belongs to cladocera and 1 species belongs to ostracoda. The density of zooplankton varied from 0.5×103 ind./l to 28.1×103 ind./l (Fig 2). It is apparent from the result that protozoa obtained a mean density superior to the other zooplankton groups, except in the Site3, Site4 and Site7, during October (Copepoda). The concentration of zooplankton was observed to change with seasons. The observation indicates that the highest density of total zooplankton was recorded in January while biomass of total zooplankton was maximum value during October. Biomass of zooplankton ranged between 0.32 mg/l and 19.10 mg/l. The mean biomass was almost equal in January, June ﹠ August (1.13 mg/l, 1.02 mg/l ﹠ 1.57 mg/l) and was highest in October (6.33 mg/l). In general, the biomass of zooplankton was largely dominated during this study by copepod (average 2.11 mg/l).

Table 2 Occurrence of zooplankton sampling in different months.

Month Month Nbr species Nbr species Jan. Jun. Aug. Oct. Jan. Jun. Aug. Oct. Protoza(14) 7 4 4 13 Keratella valga + + + + Tintinnidium fluviatile + + + + Filinia longiseta + + + + Askenasia sp + + + + Polyarthra trigla + + + Cyclotrichium sp. + + + Asplanchna sp. + + + + Vorticella sp. + + Asplanchna priodonta + + + Urotricha sp. + + Brachionus angularis + + + + Diffugia sp. + + Brachionus calycif lorus + + + + Amoebida sp. + + Pedalia sp + + + + Didinium sp. + + Brachionus urceus + Centropyxis sp. + + Brachionus leydigi + Arcella sp. + Monostyla closterocerca + Zoothamnium sp. + Monostyla bulla + Tintinnopsis sp. + Lepadella sp. + Stentor sp. + Lepadella patella + Strobilidium sp. + Lecane luna + Copepoda(5) 3 3 4 5 Schizocerca diversicornis + Mesocyclops leuckarti + + + + Gastropus hyptopus + Cyclops vicinus + + + + Cladocera(3) 2 2 2 3 Boeckella orientalis + + + + Moina micrura + + + + Mesocyclops pehpepiensis + + Bosmina . coregoni + + + + Arctodiaptomus rectispinosus + Daphnia hyalina + Rotifera(18) 8 9 9 17 Ostracoda(1) + Keratella cochlearis + + + +

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Jan. Protozoa Copepoda Jan. Protozoa Copepoda Rotifera Cladocera 1.6 Rotifera Cladocera 20000 1.4 1.2 15000 ) 1 mg/L

10000 ( 0.8 0.6 Density(ind/L) 5000 Biomass 0.4 0.2 0 0 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8

Protozoa Copepoda Jun. Protozoa Copepoda Jun. 1.6 30000 Rotifera Cladocera Rotifera Cladocera 1.4 25000 ) 1.2 20000 1

15000 ( mg/L 0.8 0.6 10000 Density(ind/L) 0.4 Biomass 5000 0.2 0 0 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8 Protozoa Copepoda Aug. 3.5 Protozoa Copepoda Rotifera Cladocera Aug. 12000 Rotifera Cladocera 3

10000 ) 2.5 8000 2 ( mg/L 6000 1.5 4000 1 Density(ind/L) Biomass 2000 0.5 0 0 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8

Oct. Protozoa Copepoda Rotifera Oct. Protozoa Copepoda Rotifera 25 Cladocera Ostracoda 2500 Cladocera Ostracoda 20

2000 )

1500 15 ( mg/L 1000 10 Density(ind/L) 500 Biomass 5

0 0 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8 St 1 St 2 St 3 St 4 St 5 St 6 St 7 St 8

Fig 2 Seasonal variation of the density and biomass of zooplankton at eight sampling sites in Hulun Lake in 2009.

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3.3. Distribution of protozoa

The density of protozoa was observed to vary between 0.3×103 ind. /l and 28.0×103 ind. /l (annual average 8515ind. /l). On the basis of density it is worth observing that protozoa was the dominant group and contributed more than 97% to the total zooplankton from January to August, except at Site1 during August. The contribution of protozoa was varying from 35.1% to 90.9% of the total density during October. The highest average density of protozoa was noticed in June, while low incidence was recorded in October. The percentage contribution of protozoa to zooplankton biomass was found to range between 0.1% and 60.7%, and it was maximum value in the month of January and June. Among protozoa, Tintinnidium fluviatile and Askeuasia sp. were dominated in the present investigate. A significant correlation was found between protozoa density with pH (P<0.01, r=0.48), Alkalinity (P<0.01, r=0.48), Total hardness (P<0.05, r=0.44), Phosphate (P<0.01, r=-0.74) and COD (P<0.05, r=-0.49) of water (Table 3). The ShannanWeiner diversity index of the protozoa was 1.631, maximum value was 2.183 (in October) and minimum value was 1.258 (in January) respectively.

Table 3 Correlation coefficients between zooplankton density and environmental variable

+ 3- Parameters pH Alkalinity Total Hardness Salinity COD NH4 PO4 Total zooplankton -0.73** 0.45* 0.45* 0.24 -0.48* 0.20 0.49** Protozoa -0.74** 0.46** 0.44* 0.25 -0.49* 0.19 0.48** Rotifera 0.43* -0.46** -0.02 -0.23 0.00 -0.19 -0.21 Cladocera 0.41 -0.22 -0.15 -0.18 0.35 -0.05 0.04 Copepdoa 0.29 -0.25 -0.15 -0.05 0.33 0.16 0.24 *for P<0.05, **for P<0.01

3.4. Distribution of copepods

Copepoda were generally the second most representative group in terms of density and biomass. Fifty one percent of the copepods recorded were nauplii. Copepoda was represented by 5 species belonging to 3 genera, their contribution varied between 29.0% and 99.8% towards the total biomass of zooplankton. The copepoda group obtained a mean biomass usually superior to the other zooplankton groups at all sites in August and October, except in the Site8 (October). Mean copepoda biomass varied between 0.1mg/l and 19.0mg/l and was maximum in Site7 in October. While the mean density of copepoda was recorded from 3ind./l to 1350ind./l. Copepoda densities were greater than both protozoa and Rotifer combined at Site3, Site4 and Site7 in October. Mean densities at all sites were below1.6 ind. /l from January to August except Site1, Site2 and Site3 in August. In the copepoda group, the numerical predominance was nauplii, and Mesocyclops leuckarti, Cyclop vicinus and Boeckella orientalis were higher frequency in the present study. Statistically copepoda showed no significant correlation with these abiotic factors. The ShannanWeiner diversity index of the copepoda was 0.398, maximum value was 1.405 (in October) and minimum value was 0.023 (in January) respectively.

3.5. Distribution of rotifera

The rotifera was represented by 18 species, their contribution varied between nil and 37.8% of the total density and was maximum at Site1 in August. The maximum number of species was recorded in October while the density of rotifera was maximum value in August, and the densities of rotifera followed the

1132 X.P.X.P. An An et al.et al./ Procedia/ Procedia Environmental Environmental Sciences Sciences 13 8 (2012) (2011 )1099 1126 –– 11311096 1105 order: August > June > October > January (Fig. 2). Among rotifera, Keratella quadrato, Keratella valga, Filinia longiseta, Arplanchna spp., Brachionus angularis, Brachionus calyciflorus and Pedalia sp. were found in year-round. Statistically rotifera showed positive correlation with correlation with pH (P<0.05, r=0.43) and Alkalinity (P<0.01, r=-0.46). The ShannanWeiner diversity index of the rotifera was 0.193, maximum value was 0.388 (in August) and minimum value was 0.019 (in January) respectively.

3.6. Distribution of cladocera and ostracoda

The cladocera was represented by 3 species, comprising nil to 0.64% of total zooplankton population. Among cladocera, Bosmina. coregoni and Moina micrura were dominant. Statistically cladocera showed no significant correlation with these abiotic factors. The ShannanWeiner diversity index of the cladocera was 0.033, maximum value was 0.119 (in October) and minimum value was 0.001 (in January) respectively. Ostracoda was only recorded at Site6, Site7 and Site8 in October, which indicated that they were tolerant to the extreme environmental conditions prevailed in this region.

4. Discussion

During the study period, protozoa comprised 97.0% of average zooplankton density, while copepoda and rotifera contributed 1.6% and 1.3% of the density, respectively. Thus, the densities of various zooplanktons in Hulun Lake were as follows: protozoa > copepoda > rotifera > cladocera > ostracoda. The zooplankton density was primarily characterized by predominance of protozoa in all seasons of the year. In terms of biomass, the copepoda contributed 83.4% of the total, while the protozoa made up 1% (Table 4). This pattern which micro-zooplankton (protozoa) density dominated zooplankton and the biomass of zooplankton was mainly composed of macro-zooplankton (copepoda) was also observed in many other Chinese water bodies [11-14]. Zooplankton community structure is influenced strongly by biotic-abiotic factor (water temperature, competition and predation) in freshwater ecosystems [15-17].

Table 4 The density and biomass of zooplankton groups in Hulun Lake

Density(ind./l) Biomass(mg/l) zooplankton Jan. Jun. Aug. Oct. Average Jan. Jun. Aug. Oct. Average Protozoas 14100 14560 4910 490 8515 0.42 0.44 0.15 0.01 0.25 Rotifera 27 132 288 19 117 0.04 0.08 0.16 0.01 0.07 Cladocera 1 2 4 2 2 0.05 0.07 0.12 0.05 0.07 Copepdoa 37 38 97 388 140 0.55 0.47 1.18 6.24 2.11 Ostracoda 0 0 0 6 1 0.00 0.00 0.00 0.07 0.02 Total 14164 14732 5299 905 8775 1.05 1.05 1.61 6.39 2.53

The protozoa density was observed a significant seasonal variation, which may be caused temperature changes and zooplankton competition. In June, after ice-break, water temperature was near 16 °C that was the optimal temperature for survival of protozoa [18], and the protozoa density was at the highest peak. However, the density of protozoa was decreasing between August and October, but they reached their autumn minimum when the number of copepoda was maximum value. It is known that protozoa serve as major food items for the macro-zooplankton [19]. Godhantaraman and Uye [20] reported the dominance of microzooplankton to their ability to exploit smaller food particles unavailable to most mesozooplankton, particularly copepods. Modenutti et al. [21] found that the presence of some rotifers

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and copepod species depressed the numbers of ciliates in Lake Rivadavia, Argentina. In the present study, the density of protozoa was recorded to annual average 8515ind./l in the lake. In general, smaller protozoan species such as Tintinnidium fluviatile and Askeuasia sp. dominated the protozoan community of Hulun Lake. Protozoa is regarded by many authors as being a good indicator of organic pollution [22- 24]. Whink et al. reported the shift to smaller zooplankton in Lake Victoria to increased eutrophication, resulting in a shift from diatoms to cyanophytes[25]. Copepoda was the most dominant group among zooplankton on the basis of biomass in Hulun Lake. In populations of copepoda, the numerical predominance of young forms, especially nauplii, is the most common pattern, as observed in different freshwater habitats [26-28] and as also found in the present study. The high densities of the immature forms are generally a result of the continuous reproduction of these organisms [29]. The existence of young forms is of great importance for zooplankton community structure, with regard to population dynamics and also trophic aspects, since in the early phases, the organisms can occupy trophic niches different from those of the adults. A classic example is that of the nauplii and first copepodite instars of the cyclopoida, which have a filtration feeding habit and are predominantly herbivorous, while the later copepodite stages and the adults have raptorial feeding habits and are predominantly carnivorous. In the present study, adult copepoda participation was relatively small in Hulun Lake. Rotifera was the maximum number of species and the second most abundant group in June and Augest. Rotiferia showed seasonal fluctuation. Paulose et al. considered the peak of rotifera being coinciding with higher water temperature, pH and nutrient concentration [30]. The rotifers are the most important animal group belonging to the ecological niche of small filters. The rotifers are able to ingest small particles such as bacteria and organic detritus that are often abundant in eutrophic environments. The result, a strong representation of rotifers in aquatic freshwater can be considered as an indicator of a high biological trophic level [31]. Previous studies have used rotifer abundance and occurrence as efficient bioindicators of higher trophic levels [32, 33]. Among rotifera, B. angularis, B. calyciflorus, F. longiseta and Lecane spp. indicate semipolluted waters [27], the dominance of Brachionus sp. and F. longiseta in the lake designate eutrophy and are usually recorded in mixotrophic waters [34, 35]. Furthermore, the relationship has been observed between a high number of the genus Brachionus and a high trophic level [36]. Thus the quantitative and qualitative distribution and species composition of rotifers in Hulun Lake indicated its highly eutrophic and polluted conditions. Moreover, rotifera prefer more alkaline waters [37]. This agrees with the present data where the total alkalinity of the lake water ranged from 867 - 1790 mg/l with an average of 1115 mg/l. The low density of cladocera wase observed in Hulun Lake. The absence of cladocera was observed could be due to the effects of fish predation. Zooplankton is influenced strongly by both bottom-up and top-down processes and is often used as models for ecological paradigm. In order to effectively utilize water resources, some fish fries (including carp and silver carp) are released by relevant government department. It is likely that fish predation limits the biomass of macro-zooplankton in productive lakes. Lakes with intense fish predation typically have only small species of cladocera, which was found to be the major factor structuring zooplankton assemblages in several studies [38-40]. The above conclusion was also observed substantial reductions in macrozooplankton biomass with gradients of fish predation [41]. In winter, it is biotic interaction operating through feeding pressure rather than water quality. It seems to affect the zooplankton diversity and density particularly the stocked fish species which play an important role in harvesting species of zooplankton, thereby reducing their predatory pressure on other groups. The ShannanWeiner diversity index (H) is probably the most widely used index in community ecology, and measures the average degree of uncertainty in predicting to what species an individual chosen at random from a collection of species and N individuals will belong. In present study, The ShannanWeiner

1134 X.P.X.P. An An et al.et al./ Procedia/ Procedia Environmental Environmental Sciences Sciences 13 8 (2012) (2011 )1099 1126 –– 11311096 1107 index for the total zooplankton was observed highest 3.99 in October and lowest 1.301 in January where as average 2.26 (Fig.3), and the average value of H was in the order: protoza > copepoda > rotifera > cladocera. In addition, the maximum number of species was also recorded in October. Therefor, this lake had rich species diversity and even individual distruibution in October, and these ShannanWeiner index values indicated that this lake was at medium level of eutrophication in all the year round except autumn. protozoa 5

4 copepods 3

2 rotifera

1 cladocera 0 Shannan Weiner diversity Weiner Shannan Jan. Jun. Aug. Oct. total zooplankton

Fig.3 ShannanWeiner diversity indexes of zooplankton in different seasons in Hulun lake.

Summarizing the available information on the biological indicators of trophic status, we suggest that 3- Hulun Lake was nutrient rich. In our research, average PO4 value was measured as 0.020-0.957 mg/l, with average 0.157 mg/l. This value is over the derigueur limit values for eutrophic lakes [42]. Based on the nutrient data, Hulun lake can be regarded mesotrophic and eutrophic. There are numerous studies indicating the importance of phosphates and nitrates in controlling the abundance of phytoplankton and thereby, zooplankton. A better indicator of nutrient status of lakes appears to be the ratio of nitrate nitrogen to orthophosphates (N: P). It has been shown that a ratio less than 10 results in nitrogen limitation which favors cyanobacterial blooms [43]. In the present study, these ratios ranged from 0.03 to 2.0. However, the complete reliance on N: P ratios may not always be sufficient to explain autotroph succession in water bodies. In aquatic ecosystems zooplankton plays a critical role not only in converting plant food to animal food but also they themselves serve as source of food for higher organisms. Zooplankters provide the main food for fishes and can be used as indicators of the trophic status of water bodies [44]. The ecological approaches focusing on zooplankton community structure should be used to manage Hulun Lake.

Acknowledgments

The authors are thankful at the anonymous referees by theirs valuable suggestion. This research was supported physically by the Station for Agricultural Technique Popularization in Inner Mongolia and Hulun Lake Fishery Company.

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