Influence of Hydrological Heterogeneity on Rotifer Community Structure in Three Different Water Bodies in Shantou Area, Guangdong (China)

© 2019 Academia Sinica, Taiwan Open Access Influence of Hydrological Heterogeneity on Rotifer Community Structure in Three Different Water Bodies in Shantou Area, Guangdong (China) Diwen Liang1, Nan Wei1, Qing Wang1, Christian D. Jersabek2, Xuejia He3, and Yufeng Yang1,* 1Institute of Hydrobiology, Jinan University, 601 West Huangpu Avenue, Guangzhou, Guangdong, China. *Correspondence: E-mail: [email protected] (Yang). E-mail: [email protected] (Liang) 2Division of Animal Structure & Function, University of Salzburg, A–5020 Salzburg, Austria. E-mail: [email protected] 3Research Center for Harmful Algae and Aquatic Environment, Jinan University, Guangzhou, Guangdong, China. E-mail: [email protected] Received 15 October 2018 / Accepted 11 July 2019 / Published 16 September 2019 Communicated by Benny K.K. Chan Rotifers, small but essential invertebrates in aquatic ecosystems, are sensitive to environmental changes and are proposed to be indicators of trophic state. However, the effects of hydrological heterogeneity on the rotifer community and the ability of rotifer indices to reflect trophic state across different water bodies are still unclear. Here, we investigated rotifer community structure in different seasons in the three types of water bodies: Han river downstream (HD), Reservoir (RE) and Tidal creek (TC) in Shantou City, Guangdong, China. Our findings revealed that rotifer community structure differes significantly among the three water bodies, resulting from a dominance of Keratella cochlearis, Anuraeopsis fissa and Polyarthra vulgaris, who largely accounted for the differences in water bodies. Chlorophyll-a and transparency were the main environmental drivers in RE rotifer communities, while total nitrogen, total phosphorus and salinity were the main factors in HD and TC communities. Rotifer abundance and the rotifer trophic state index decreased in the order: RE > HD > TC. However, both the Sladecek’s B/T quotient and the Keratellaindex decreased in the order: HD > RE > TC, which was in accordance with the Carlson’s trophic index. We conclude that it is efficient to use rotifer composition in water quality assessments when comparing different water bodies. Alpha diversity of rotifers was the highest in HD, which is consistent with the intermediate disturbance hypothesis. Hydrological heterogeneity is the micro-factor that regulates rotifer community structures in the Shantou area. Key words: Rotifera, Different habitats, Environmental factors, Trophic state, Intermediate disturbance. Citation: Liang D, Wei N, Wang Q, Jersabek CD, He X, Yang Y. 2019. Influence of hydrological heterogeneity on rotifer community structure in three different water bodies in Shantou area, Guangdong (China). Zool Stud 58:23. doi:10.6620/ZS.2019.58-23. BACKGROUND Rotifers, a group of essential zooplankton in aquatic ecosystems, are sensitive to changes in the environment, acting as effective indicators of trophic conditions (Duggan et al. 2002; May et al. 2014; Sládeček 1983). Rotifers connect primary producers and secondary consumers, playing an important role not only in the food chain but also the microbial food web (Arndt 1993; Devetter and Sed’A 2003). Rotifers are also highly adaptive to changes in the environment and can occupy open niches quickly, and as such they are widely distributed in the world and live in all kinds of water bodies. Consequently, they are adapted to a variety of characteristics of different water bodies (Segers 2007). In the wide range of environments, rotifer community structure is influenced by the factors such as water temperature, salinity, transparency, trophic Zoological Studies 58: 23 (2019) doi:10.6620/ZS.2019.58-23 1 © 2019 Academia Sinica, Taiwan status and predators (Devetter 1998; Khaleqsefat 2013). As the biotic and abiotic environmental conditions vary seasonally, the community structure of rotifers also varies with season in a single water body, often with succession of different dominant species (El-Shabrawy and Germoush 2014) and changes in diversity and evenness (Bonecker et al. 2013). It has been shown that rotifer abundance in rivers varies periodically from the rainy season to the dry season (Rougier et al. 2005). While numerous studies of rotifer community structure have investigated seasonal or periodic changes in a single type of water body, few studies compared different water bodies in the same area. Hydrological regimes in different habitats is a more important factor diversifying the living conditions of zooplankton assemblages (Ginders et al. 2016). Tidal creek is a lotic water ecosystem that connects river and sea, similar to an estuary. It is affected by both terrigenous freshwater flow and tides so that the hydrological conditions and environmental factors change dramatically (Hackney et al. 1976). Reservoirs are artificial facilities at the narrow portion of the river, which can be used to generate electricity and for irrigation. Reduction in water velocity and increase in water transparency can result in replacement of lotic species by lentic species after stabilization of the system (Serafim-júnior et al. 2016). It was reported that the open lentic waters harbor a rich variety of rotifers because of the macrophytes (Arora and Mehra 2003). The river is a lotic water ecosystem that connects land and sea. Its water level and flow rate fluctuation have been correlated to precipitation and seasonal change (Rougier et al. 2005). Different water bodies have different hydrological characteristics, so the rotifer communities are expected to vary. The Shantou area contains different types of water bodies, such as reservoirs, rivers, tidal creeks, and these effect the hydrological heterogeneity of rotifer community structure. Rotifer species composition, total abundance, and diversity indices have been widely used as biological indicators for assessing water quality (May and O’Hare 2005; Wen et al. 2011; Gutkowska et al. 2013). Saprobic species and some rotifer composition indices such as the Brachionus: Trichocerca ratio (Sládeček 1983) and Keratella-index (Gopko and Telesh 2013) have been used as trophic state indicators. Also, the rotifer trophic state index (TSIROT) could be a useful tool for assessing the ecological quality of urban ecosystems (Jurczak et al. 2018). May and O’Hare (2005) claimed that rotifer total abundance is a more sensitive indicator of lake trophic status than species composition. However, there is limited knowledge about whether these indicators are capable of reflecting trophic state when comparing different water bodies. The aim of this study was to investigate the following questions: (1) which rotifer indicators are suitable to reflect trophic state of the three different water bodies? (2) Which factors are responsible for the difference of rotifer communities? (3) Which water bodies harbor the highest diversity? MATERIALS AND METHODS Study sites This study was conducted around Shantou, an eastern city in Guangdong province, China, which is affected by the subtropical monsoon climate. The Han River downstream (HD), which flows through the city, experiences a wet season (April to September) and a dry season (October to March). HD serves as the drinking water supply for the eastern cities of Guangdong province. Its downstream is divided into three main tributaries (northern stream, western stream and eastern stream), running through Shantou City and towards the South China Sea. The annual precipitation was 1496 mm in 2015, and 2110 mm in 2016 (Shantou annual climate bulletin). Nanao Island is about 6 km away from the mainland; it provided the reservoir and tidal creek sites. Our study was carried out at 12 sampling sites, including 5 Han River downstream sites (HD1, HD2, HD3, HD4, HD5), 5 reservoir sites (RE1, RE2, RE3, RE4, RE5) and 2 tidal creek sites (TC1, TC2) (Fig. 1). Among these, HD3 was located in the northern tributary, HD5 was in the eastern tributary and HD1, HD2, and HD4 were in the western tributary of the Han River, flowing through downtown Shantou. Apart from RE5, which was on the mainland, the other reservoir sites were located on Nanao Island as freshwater reserves. The tidal creek sites, located in Shenao Town of Nanao Island, receive domestic sewage discharges and are subject to tides. Sampling and analytical procedure Samples of rotifers were collected four times: in July 2015, November 2015, January 2016 and May 2016. Quantitative samples of rotifers were collected in triplicate each from 5 liters of surface water. These samples were concentrated over a 30 μm mesh. Qualitative samples for species identification were collected by dragging a plankton net with a mesh size of 30 μm on the surface and subsurface water horizontally. Both quantitative and qualitative samples were fixed with 5% formalin solution and preserved in a 50 mL polyethylene bottle immediately. Physical factors such page 2 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan as water temperature, dissolved oxygen, pH, and salinity were measured using a YSI-Plus calibrated multiprobe (USA). Water transparency was measured with a Secchi disc. Chlorophyll-a, total dissolved phosphorus (TP) and total dissolved nitrogen (TN) were determined in the laboratory following the standard analytical methods (GB3838-2002, MEE, China, 2002). Rotifer identification was based on the Koste (1978) classification system. Trophi were isolated from the qualitative samples for further identification and then the list of rotifer species from different water bodies in the Shantou area was tabulated. Quantitative samples were concentrated to 10 mL after sedimentation. One mL concentrated solution was taken randomly after mixing and analyzed in a Sedgewick-Rafter chamber. The abundance counts were converted to ind.·L-1. Statistical analysis The results were processed by ANOVA using the non-parametric Kruskal-Wallis and Dunn’s tests to determine significant differences in rotifer density, rotifer community indices, and physical-chemical factors among the three water bodies. In order to assess the relationship between rotifer abundance and environmental factors, we used SPSS 22.0 to perform the Pearson or Spearman correlation analysis. Correlation coefficients were calculated with Spearman ranks (P ≤ 0.05). Stepwise multivariate regression was performed to determine the main environmental factors that affected the abundance and rotifer community indices. The dataset of species was log transformed (log (n + 1)) and standardized, and rotifer community structures were processed using PRIMER 5 to obtain the following indices: Alpha diversity: Margalef species richness index, Simpson dominance index, Shannon–Weiner diversity index, Brillouin diversity index and Pielous evenness index were calculated to evaluate the diversity within water bodies. Beta diversity: Cluster analysis, non-metric multidimensional scaling (NMDS) and analysis of group dissimilarities (ANOSIM), based on Bray-Curtis distance, were analyzed to determine the differentiation among the three types of water bodies. Carlson’s trophic state index (Carlson 1977) was applied to evaluate the trophic status of the three water Fig. 1. Location of the study area and the sampling sites covered in Shantou City. Abbreviations used in the figures: HD, Han River downstream; RE, reservoir; TC, tidal creek. N page 3 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan bodies. Brachionus: Trichocerca ratio (Sladecek’s B/ T quotient) (Sládeček 1983), Keratella-index (KIN) (Gopko and Telesh 2013) and the rotifer trophic state index (TSIRot) (Ejsmont-Karabin 2012) were also used in the trophic state assessment. The response of rotifer community structures to environmental variables was analyzed with CANOCO 4.5, a multivariate statistical package. The dataset was log transformed (log (n + 1)) and centered on species. According to the length of gradient (4.53) performed by DCA, we used a CCA (Canonical Correlation Analysis) model to estimate the relationship between rotifer species and environmental factors. RESULTS Environmental characteristics The details on the physicochemical data and variations are presented in figure 2. During the study period (2015–2016), water temperatures were similar among all the sampling sites. The lowest temperature occurred in January 2016 at 16.1 ± 0.8°C, and the highest temperature occurred in July 2015 at 32.2 ± 1.4°C. In November 2015 and May 2016, temperatures were 23 ± 0.9°C and 25.3 ± 1.1°C, respectively. TC water was lotic water under tidal influence, and showed fluctuations in water level and salinity. The pH of all sites ranged from 6 to 9, and on average was slightly alkaline (pH 7.87 ± 0.41). The Secchi disc depth (SD) in RE was significantly higher than that in HD and TC (P < 0.05) (Fig. 2). The concentrations of chlorophyll-a recorded in RE were significantly higher than that in HD and TC (P < 0.05). However, the lowest concentration of TP and TN were found in RE (TP = 0.06 ± 0.05 mg·L-1; TN = 0.44 ± 0.20 mg·L-1), while the concentration in HD (TP = 0.12 ± 0.04 mg·L-1; TN = 1.65 ± 0.79 mg·L-1) and TC (TP = 0.20 ± 0.18 mg·L-1; TN = 1.31 ± 0.91 mg·L-1) were significantly higher than that in RE (P < 0.05). The lowest Carlson’s trophic state index average value was found in RE, while the highest value was found in HD in most seasons. According to the Carlson’s TSI, TC was oligotrophic, while RE and HD were oligotrophic except in July (mesotrophic). Species composition and abundance of rotifers A total of 61 species belonging to 23 genera were identified in all sampling sites during the study period, including subspecies and unidentified bdelloidea. The highest number of taxa occurred in RE (44 species), followed by HD (36 species), and lowest (11 species) in TC. The dominant genera were Brachionus (10 species) and Lecane (8 species). Keratella cochlearis, Polyarthra vulgaris and Anuraeopsis fissa were distributed in all types of water bodies (Table 1). The prevailing species K. cochlearis was widely distributed in all sampling sites of RE, while A. fissa and B. angularis dominated HD. B. donneri, P. euryptera and Hexarthra mira were only found in RE2, a reservoir on Nanao Island at an elevation of 384 m. The highest abundance of rotifers occurred at HD3 in July 2015(975 ind.·L-1), the rainy season of Guangdong, and the lowest abundance occurred at TC1 in January 2016(1 ind.·L-1), the dry season of Guangdong. In November, the highest abundance occurred in RE4 (198 ind.·L-1) and in May it occurred in RE2 (273 ind.·L-1) (Fig. 3). Differentiation of rotifer community structure among different water bodies A non-metric multidimensional scaling (NMDS) plot was used to reveal patterns in rotifer community structure in relation to different water bodies. The stress value of NMDS was 0.17 (< 0.2). The RE samples were mostly together and distributed below the First Axis and the HD samples tended to be above the First Axis. TC was mostly on the left, but with some points on far right. The result of NMDS revealed that the majority of values from each water body are located in a certain position in the plot and separated from each other, but with some exceptions (Fig. 4). The analysis of group dissimilarity processed by PRIMER using ANOSIM (one-way) demonstrated that rotifer communities were significantly different among three types of water bodies in the Shantou area (Global R = 0.416, P < 0.01). The ANOSIM test indicated that the differences between groups were significantly greater than those within groups, which demonstrated that it is meaningful to group by water bodies. Among them, rotifer community structure in RE was not only significantly different from that in TC (R = 0.698, P < 0.01), but also significantly different from that in HD (R = 0.348, P < 0.01). The seasonal differences in rotifer communities were relatively small (R = 0.106, P < 0.01) compared to different types of water bodies. This differentiation between HD and RE water bodies was caused by the abundances of their respective dominant species. According to the contribution rate of rotifers in different water bodies, we found that the variation between RE and HD, the lentic and lotic water, resulted from the abundances of the dominant species in each of the different communities. Keratella cochlearis, a dominant species in RE, with the mean abundance significantly higher than that in HD, made the greatest page 4 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan Fig. 2. Environmental factors and trophic states in the different water bodies. Letters indicate sample means that are similar (same letter) or significantly different (different letter) among different water bodies; blank represents no significant difference. Abbreviations used in the figures: HD, Han River downstream; RE, reservoir; TC, tidal creek. page 5 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan Fig. 3. The proportions (Y axis on left) and the abundances (Y axis on right) of the dominant rotifers in different sampling sites in Shantou. The lines represent the total abundances and the column represent the rotifer composition. Abbreviations used in the figures: HD, Han River downstream; RE, reservoir; TC, tidal creek. Table 1. The list of rotifer species observed in the three water bodies investigated in Shantou Species Names Abbreviation used in CCA Water Bodies RE (Reservoir) HD (Han Downstream) TC (Tidal creek) Brachionus calyciflorus f. monstruosus De Ridder, 1987 Bra_cal + B. urceolaris Müller, 1773 Bra_urc + B. angularis Gosse, 1851 Bra_ang + + B. plicatilis Müller, 1786 Bra_pli + B. caudatus Barrois & Daday, 1894 Bra_cau + + B. falcatus Zacharias, 1898 Bra_fal + B. quadridentatus Hermann, 1783 Bra_qua + B. donneri Brehm, 1951 Bra_don + B. diversicornis Daday, 1883 Bra_div + B. forficula Wierzejski, 1891 Bra_for + Anuraeopsis fissa Gosse, 1851 Anu_fis +++ Polyarthra dolichoptera Idelson, 1925 Pol_dol + + page 6 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan Species Names Abbreviation used in CCA Water Bodies RE (Reservoir) HD (Han Downstream) TC (Tidal creek) P. vulgaris Carlin, 1943 Pol_vul +++ P. euryptera Wierzejski, 1891 Pol_eur + P. indica Segers & Babu, 1999 Pol_ind + P. remata Skorikov, 1896 Pol_rem + Filinia longiseta Ehrenberg, 1834 Fil_lon + F. opoliensis Zacharias, 1898 Fil_opo + F. cornuta Weisse, 1848 Fil_cor + F. novaezealandiae Shiel & Sanoamuang, 1993 Fil_nov + Asplanchna priodonta Gosse, 1850 Asp_pro + + A. brightwellii Gosse, 1850 Asp_bri + + Keratella cochlearis Gosse, 1851 Ker_coc ++ + + K. tecta Gosse, 1851 Ker_tec + + K. tropica Apstein, 1907 Ker_tro + + Lecane bulla Gosse, 1851 Lec_bul + + L. closterocerca Schmarda, 1859 Lec_clo + L. papuana Murray, 1913 Lec_pap + L. stichaea Harring, 1913 Lec_sti + L. ungulata Gosse, 1887 Lec_ung + + L. stenroosi Meissner, 1908 Lec_ste + L. hamata Stokes, 1896 Lec_ham + L. luna Müller, 1776 Lec_lun + + Proalides subtilis Rodewald, 1940 Pro_sub + Hexarthra mira Hudson, 1871 Hex_mir + Collotheca sp. Collotheca + + Trichocerca pusilla Jennings, 1903 Tri_pus + + T. similis Wierzejski, 1893 Tri_sim + + T. stylata Gosse, 1851 Tri_sty + + T. cylindrica Imhof, 1891 Tri_cyl +++ T. insignis Herrick, 1885 Tri_ins + T. rousseleti Voigt, 1902 Tri_rou + T. capucina Wierzejski & Zacharias, 1893 Tri_cap + Trichotria tetractis Ehrenberg, 1830 Tri_tet + Wolga spinifera Western, 1894 Wol_spi + Mytilina ventralis Ehrenberg, 1830 Myt_ven + Testudinella patina Hermann, 1783 Tes_pat + + Gastropus hyptopus Ehrenberg, 1838 Gas_hyp + Ascomorpha ovalis Bergendal, 1892 Asc_ova + + A. saltans Bartsch, 1870 Asc_sal + + Synchaeta stylata Wierzejski, 1893 Syn_sty + S. oblonga Ehrenberg, 1832 Syn_obl + + S. tremula Müller, 1786 Syn_tre + S. pectinata Ehrenberg, 1832 Syn_pec + Colurella adriatica Ehrenberg, 1831 Col_adr + Ploesoma truncatum Levander, 1894 Plo_tru + Cephalodella sp. Cephalodella + + Cephalodella gibba Ehrenberg, 1830 Cep_gib + Conochilus unicornis Rousselet, 1892 Con_uni + Encentrum sp. Encentrum + + Bdelloidea spp. Bdelloidea + + + “+” represents the presence of the item; blank represents the absence of the item. HD, Han River downstream; RE, reservoir; TC, tidal creek. Table 1. (Continued) page 7 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan contribution to the variation in different communities (10.43%). In addition, A. fissa, P. vulgaris, H. mira and B. angularis also played an important role in their differentiation. On the other hand, the mean abundance of P. vulgaris and H. mira in RE were significantly higher than that in HD, while the abundance of A. fissa and B. angularis in HD were higher than in RE (Table 2). The abundances of these species were responsible for the differentiation between RE and HD. Rotifer community indices Rotifer abundance in TC (7 ± 3) was significantly lower than that in HD (127 ± 251) and RE (235 ± 193) (P < 0.05) (Fig. 5A). The highest TSIROT was recorded in RE (51 ± 2; P < 0.05), followed by HD (48 ± 3), and lowest (46 ± 5) in TC (Fig. 5B). However, both of the BT and KIN indices were in the order: HD (1.2; 0.22) > RE (0.7; 0.06) > TC (0; 0) (Fig. 5C). The highest diversity index of both Simpson’s in HD and Shannon-Weiner (0.72 ± 0.11; 2.13 ± 0.62) were significantly higher than that in RE (0.56 ± 0.15; 1.72 ± 0.48) and TC (0.35 ± 0.30; 0.82 ± 0.75) (P < 0.01; P < 0.05). The higher proportion of dominant species in RE resulted in a decrease of the value of Pielou’s evenness (0.62 ± 0.16), which was significantly lower than that in HD (0.89 ± 0.08; P < 0.01). The Margalef and Brillouin diversities were higher in HD (1.30 ± 0.59; 1.28 ± 0.43), but not significant (P > 0.05) (Fig. 5D). The diversity and evenness levels suggested that Fig. 4. The non-metric multidimensional scaling (NMDS) plots of rotifer community in Shantou. Abbreviations used in the figures: HD, Han River downstream; RE, reservoir; TC, tidal creek. Table 2. Dominant species and their contribution rate to differences between RE and HD in Shantou Species Average Abundance (Log) Contribution (%) RE (Reservoir) HD (Han Downstream) Keratella cochlearis 94.54 4.79 10.43 Anuraeopsis fissa 6.83 26.63 8.41 Polyarthra vulgaris 58.58 42.50 8.23 Brachionus angularis 6.88 11.42 7.51 Hexarthra mira 25.96 04.80 Ascomorpha saltans 1.67 2.42 4.54 Synchaeta stylata 02.33 3.92 K. tecta 3.17 1.17 3.79 S. oblonga 0.75 1.83 3.67 Trichocerca pusilla 2.79 10.54 3.50 T. similis 3.67 0.92 3.19 T. cylindrica 4.29 0.75 2.64 page 8 of 14Zoological Studies 58: 23 (2019) © 2019 Academia Sinica, Taiwan the species composition of HD water bodies was more even, compared to RE and TC water bodies. Relationships between community composition and environment variables Rotifer abundance showed a significantly positive correlation with chlorophyll-a concentration (R = 0.52, P < 0.001). However, there was no significant correlation between rotifer abundance and other environment factors such as SD, TN, TP, temperature, or salinity (P > 0.05). The multivariate regression analysis was conducted with the rotifer abundance as response variables and environment factors as dependent variables including chlorophyll-a, SD, TN, TP, temperature (Temp), salinity (Sal), pH and DO. After eliminating the non-significant independent variables, multivariate regression analysis suggested that the total abundance of rotifers was only significantly related to chlorophyll-a, SD and temperature (Table 3). The Shannon-Weiner index was correlated with salinity. Simpson and Pielou’s index were associated with salinity, TN, DO, and temperature, and Margalef was related to DO only. The CCA summarized the relationships between the rotifer species composition and environmental variables (Fig. 6) (Pseudo-F = 1.628, P < 0.001). After forward selection with Monte Carlo permutation tests, chlorophyll-a, TP, TN, SD and temperature were significant contributors to the model (Table 4). The first two ordination axes explained 43.6% of species– environment variability in the ordination of physical and chemical factors (Table 5). From the perspective of species with high contribution rate of community difference, Polyarthra vulgaris stands in the middle of the figure, indicating Fig. 5. Rotifer community indices among three water bodies. (A) Rotifer total abundance; (B) Ejsmont-Karabin’s rotifer trophic state index; (C) Sladecek’s B/T quotient and Keratella-index (KIN) values; (D) α biodiversity indices. Letters indicate sample means that are similar (same letter) or significantly different (different letter) among different water bodies; blank represents no significant difference. Abbreviations used in the figures: HD, Han River downstream; RE, reservoir; TC, tidal creek. (A) (C) (B) (D) page 9 of 14Zoological Studies 58: 23 (2019)