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Seasonal shift in zooplankton communities in two sub-tropical urban wetlands, Southern China
Acta Ecologica Sinica 36 (2016) 236–245
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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Seasonal shift in zooplankton communities in two sub-tropical urban wetlands, Southern China Songlu Liu a, Xinlu Shi a,⁎, Henglong Xu b,⁎, Guijie Liu a, Cuicui Hou a, Xiaowen Zhu a a b
Hangzhou Key Laboratory for Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou 310036, China Laboratory of Microbial Ecology, College of Marine Life Science, Ocean University of China, Qingdao 266003, China
a r t i c l e
i n f o
Article history: Received 5 July 2015 Received in revised form 1 February 2016 Accepted 4 March 2016 Keywords: Urban landscape Zooplankton Bioindicator Species diversity Sub-tropical wetland Environmental stress
a b s t r a c t The seasonal shift in the community pattern of zooplankton was studied in two typical urban landscape wetland systems (West Lake and Xixi Wetland) during four. seasons (June 2013 to May 2014). Samples were monthly collected at six sampling stations within a gradient of environmental stress in West Lake and Xixi Wetland, respectively. A total of 119 zooplankton species were identified, comprising 75 rotifers, 23 cladocerans and 21 copepods. Multivariate analysis revealed that: (1) the species compositions represented significant differences between two biotopes, with Rotifera assemblage as the primary contributor to the difference; (2) the community structures showed dissimilar seasonal variation in both wetlands, and 14 rotifer species were the main contributors to this dissimilarity; (3) the temporal variations in zooplankton community structures were significantly correlation with the environmental variables in both systems, especially NO2-N and NO3-N in West Lake, pH, DO, T, COD in Xixi Wetland; (4) the species diversity indices (Margalef, Pielou and Shannon-Wiener) showed higher values in Xixi Wetland than that in West Lake. Based on the above results, we suggest that zooplankton community structures are significantly shaped by environmental drivers, and thus may be used as potential bioindicators of water quality in sub-tropical urban landscape wetland ecosystems. © 2015 Published by Elsevier B.V. on behalf of Ecological Society of China.
Contents 1. 2.
Introduction . . . . . . . . . . . . . . . . Materials and methods . . . . . . . . . . . 2.1. Study area and sampling sites . . . . . 2.2. Sampling and data collection . . . . . 2.3. Data analyses . . . . . . . . . . . . 3. Results . . . . . . . . . . . . . . . . . . . 3.1. Environmental variables. . . . . . . . 3.2. Species composition and typical species. 3.3. Spatiotemporal variations in abundance 3.4. Relationships between biota and abiota . 4. Disscussion . . . . . . . . . . . . . . . . . 5. Conclusions. . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . .
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1. Introduction
⁎ Corresponding authors. E-mail addresses: [email protected] (X. Shi), [email protected] (H. Xu).
http://dx.doi.org/10.1016/j.chnaes.2016.03.006 1872-2032/© 2015 Published by Elsevier B.V. on behalf of Ecological Society of China.
Zooplankton plays a significant role as the primary link in the local trophic food chain, transferring the energy from bacteria/phytoplankton to other invertebrates and fish in aquatic ecosystems [28,33]. Because of short life cycle and quick response to the environment changes, their
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Fig. 1. Map showing the sampling stations in West Lake and Xixi Wetland, Hangzhou, China.
changes in abundance, species diversity and community composition may provide important indications of environmental change or disturbance [6,31]. Compared with single species-based indicator, the community-based bioassessment has proved to be the more reliable [19]. In previous decades, many studies on freshwater zooplankton communities have been carried out in different bodies like rivers, streams, lakes and smaller aquatic habitats (e.g., [3,11,20,23]). However, as regards the differences in zooplankton community patterns and their relationships to water conditions between lake and wetland systems, little information is known [18,21,32,41]. West Lake, located near Hangzhou city, southern China, is one of the world cultural heritages, with an area of 6.5 km2 and a mean depth of 2.7 m. In 1999, after the water diversion from Qiantang River and dredge project was finished, the water eutrophication of the lake had been improved [22,42]. Xixi Wetland, located in the same city, is the Table 1 The location and character of the twelve sampling sites. Sites
Location
Character
1 2 3 4 5 6 A B C D E F
N30°15′23.61″, E120°08′27.04″ N30°15′41.07″, E120°08′53.03″ N30°15′28.23″, E120°09′08.71″ N30°14′57.04″, E120°09′20.63″ N30°13′56.41″, E120°08′20.92″ N30°14′04.34″, E120°08′16.09″ N30°15′33.16″, E120°03′26.81″ N30°15′58.53″, E120°03′33.19″ N30°16′16.59″, E120°03′19.60″ N30°16′20.15″, E120°03′20.15″ N30°16′29.49″, E120°03′47.39″ N30°16′29.14″, E120°03′55.06″
Water diversion corner, lotus, fish Spacious, much more tourists Near water outlet, restaurant Located in outer lake Near water inlet Ornamental fish pond Near water inlet, wharf Farming, fishing River intersection, market place Natural riverway Ornamental riverway, Near water outlet Ornamental pond
representative national wetland park with urban, farming and culture in China, and its water network belongs to the canal water system. It covers an area of 5.29 km2, which was studded with network river and scaly pond with a mean depth of 2.13 m [16,17,27]. With the rapid development of social and economical conditions, both wetland systems as the urban landscape have been more vulnerable to suffer pollution from human activities [35]. In this study, the zooplankton community features and their relationship to changes of environmental conditions were comparatively studied in both wetland systems during a 1-year period (June 2013 to May 2014). The aims of this study were: (1) to document the zooplankton community composition and species diversity between the two different water bodies, (2) to show the difference in zooplankton community structures in response to environment variables between the two biotopes, and (3) to assess the environmental quality status of both urban landscapes based on zooplankton community. 2. Materials and methods 2.1. Study area and sampling sites A total of twelve sampling stations (1–6, A–F) were selected in Xixi Wetland and West Lake (Fig. 1). Their characteristics were presented in Table 1. 2.2. Sampling and data collection Samples were monthly collected from June 2013 to May 2014. At each sampling site, samples were taken from upper-mid-bottom layers mixed of the water using an organic glass hydrophore (2.5 l) [25]. The
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Table 2 The monthly mean values and standard deviation of physicochemical parameters at two water bodies during the four seasons. Parameters
W-su
W-au
W-wi
W-sp
X-su
X-au
X-wi
X-sp
pH Temp (°C) DO (mg/L) COD (mg/L) TP (mg/L) TN (mg/L) NH4-N (mg/L) NO2-N (mg/L) NO3-N (mg/L)
8.5 ± 0.67 31.5 ± 1.76 7.46 ± 1.07 18.1 ± 8.80 0.11 ± 0.06 1.53 ± 0.37 0.09 ± 0.08 0.03 ± 0.02 0.60 ± 0.53
7.29 ± 1.19 21.5 ± 5.93 7.87 ± 1.27 15.7 ± 6.07 0.09 ± 0.03 1.03 ± 1.87 0.06 ± 0.27 0.02 ± 0.07 1.09 ± 1.12
7.34 ± 0.79 9.16 ± 2.40 10.4 ± 0.91 9.44 ± 3.24 0.06 ± 0.03 3.12 ± 0.88 0.28 ± 0.33 0.04 ± 0.02 2.30 ± 0.50
8.07 ± 0.59 20.1 ± 5.24 8.42 ± 2.02 5.0 ± 6.19 0.07 ± 0.03 2.96 ± 0.75 0.14 ± 0.07 0.04 ± 0.04 2.22 ± 0.65
6.71 ± 0.57 29.0 ± 3.88 4.62 ± 1.30 15.9 ± 7.61 0.15 ± 0.01 1.32 ± 1.10 0.60 ± 1.25 0.03 ± 0.03 0.57 ± 0.89
6.86 ± 0.61 20.2 ± 6.22 4.98 ± 1.47 11.1 ± 5.35 0.14 ± 0.08 1.87 ± 1.21 0.27 ± 0.40 0.07 ± 0.07 1.12 ± 0.77
7.50 ± 0.30 9.44 ± 1.51 8.83 ± 1.60 8.06 ± 3.44 0.10 ± 0.07 2.80 ± 1.41 0.32 ± 0.27 0.04 ± 0.03 1.80 ± 1.17
7.45 ± 0.24 22.2 ± 3.82 6.71 ± 1.56 14.7 ± 7.70 0.15 ± 0.07 2.07 ± 1.37 0.26 ± 0.27 0.07 ± 0.05 1.37 ± 1.00
W = West Lake, X = Xixi Wetland, su = Summer, au = Autumn, wi = Winter, sp. = Spring; DO = Dissolved oxygen, COD = Chemical oxygen demand, BOD5 = Biological oxygen demand, TN = Total nitrogen, TP = Total phosphorus, NH4-N = Ammonium nitrogen, NO3-N = Nitrate nitrogen, NO2-N = Nitrite nitrogen.
quantitative samples of microcrustacean were gathered approximately 50 ml, which filtered 20 l the mixed water through #25 plankton net and fixed with 4% Formaldehyde immediately. All samples were observed and counted under dissecting microscope. Rotifera samples were gathered in 1000 ml organic glass hydrophore and fixed with Lugol's iodine solution (1.5% final concentration, v/v), precipitated for 36 h and the final volume set to 50 ml of concentrated sediments, a 1 ml subsample of this final concentrated sample was placed to observe and count under light microscope. The physicochemical parameters were measured within 12 h from 1000 ml water samples. Zooplankton samples were identified according to the keys of Shen [24], Jiang and Du [13], Wang [36], Zhou and Chen [43] in Chinese under compound microscope (Leica DM6000B) and dissecting microscope (Leica M205A). Water temperature (T), pH and dissolved oxygen (DO) were measured in situ with an OHAUS ST20 and HACH HQ30d. The determination of chemical oxygen demand (COD), total nitrogen (TN), and total phosphorus (TP), ammonium nitrogen (NH4-N), nitrate nitrogen (NO3-N), nitrite nitrogen (NO2-N) was performed following standard methods of American Public Health Association [1]. 2.3. Data analyses A univariable analysis involving mean values and standard deviation (SD) values was applied to assess the abiotic variables in sites and seasons. Species diversity (Shannon-Wiener H′), evenness (Pielou J′) and richness (Margalef d) indices are commonly employed in communitylevel investigations and are suitable for simple statistical analyses [12]. The three indices were computed following the equations: H0 ¼ −
S X
P i ð ln P i Þ
i¼1
J0 ¼ H0= ln S d ¼ ðS−1Þ= ln N where H′ = observed diversity index; Pi = proportion of the total count arising from the ith species; S = total number of species; and N = total number of individuals. Dominance index (Y) of species in each sample was calculated using the following formula: Y¼
ni f N i
where ni is the number of individuals of species i, fi is the frequency of species i that occurred in a sample, and N is the total number of species(Y N 0.02). Multivariate analysis of biotic and abiotic data among sites and seasons were analyzed with PRIMER 5.0 [4]. Clustering analysis and MDS ordination were conducted based on standardized Euclidean distances
from log-transformed physicochemical variables and on Bray-Curtis similarity matrix from fourth-foot transformed biotic communities [2, 26,30]. An analysis of similarity (ANOSIM) was run to determine the significant discrepancies between different groups of physicochemical data and biotic abundance [5]. The R value of ANOSIM close to 1 indicating that the groups are entirely separate and 0 value indicating that there is no difference between groups [5]. A similarity percentage-species contribution (SIMPER) analysis was used to identify the typical species that contributed to group similarity [30,39]. The spatial environmental status of the twelve sampling sites was summarized using the principle component analysis (PCA) based on Euclidean distance matrices from log-transformed abiotic data [40]. The submodule BIOENV was used to analyze potential relationships between biotic variables and abiotic data [37,38]. 3. Results 3.1. Environmental variables The fluctuations in the mean values and the range of various physicochemical parameters at two water bodies during study period were summarized in Table 2. Average water temperature followed an annual pattern (e.g. summer N autumn = spring N winter), and presented no differences between the two areas. The pH values in West Lake were general higher than Xixi Wetland, except in summer. Values of DO had a negative relationship with temperature in both areas, and usually they were lower in Xixi Wetland than in West Lake and this was also the fact for COD, TN and NO3-N values during the entire sampling period. On the contrary, TP, NH4-N, NO2-N values were higher in Xixi Wetland than in West Lake. The hierarchical clustering of Euclidean distance of physicochemical variables among sites and seasons is presented in Fig. 3. The cluster analysis revealed two groups at a 0.7 distance. The first group included summer at both sites and autumn in Xixi Wetland (W-su, X-su, X-au), the second group comprised spring and winter at both sites and autumn in Xixi Wetland (W-sp, X-sp, W-wi, X-wi). The result showed the significant difference of total environment data about two stations only expressed in autumn. ANOSIM was able to detected significant differences among the sites and seasons in physicochemical parameters at global R = 0.792, P = 0.018. 3.2. Species composition and typical species A total of 119 zooplankton species were identified, comprising 75 rotifers, 23 cladocerans, 21 copepods. The abundance, occurrence and dominant species were summarized in Table 3. In West Lake, the zooplankton was composed of 39 rotifers, 16 cladocerans, 19 copepods, while in Xixi Wetland, 57 rotifers, 19 cladocerans and 16 copepods were recorded. The dominant species of Rotifera in Xixi Wetland were Anuraeopsis fissa, Keratella cochlearis and Polyarthra trigla, while on this basis it also included Asplanchna priodonta, Euchlanis dilatata and Polyarthra dolichoptera in West Lake. The dominant crustacean species
Table 3 The abundance, occurrence and dominant species of zooplankton in West Lake (W) and Xixi Wetland (X) during June 2013 to May 2014. W Abundance
Occurrence (%)
Dominance
Abundance
Occurrence (%)
+++ +++ − − +++ +++ − − − +++ +++ ++ − +++ +++ +++ − +++ +++ − +++ − +++ − − − − +++ +++ ++ +++ − ++ ++ − ++ +++ +++ +++ − − +++ − − +++ − − − − − +++
50 8 0 0 1 36 0 0 0 13 1 6 0 1 6 15 0 3 6 0 1 0 1 0 0 0 0 4 3 22 26 0 3 38 0 1 6 3 1 0 0 1 0 0 1 0 0 0 0 0 10
*
+++ +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ − − − +++ − ++ ++ − ++ − +++ +++ +++ +++ − +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ +++ − +++ +++ − +++ +++ +++ +++ ++ −
11 7 18 14 1 40 1 1 3 25 0 26 1 0 0 0 8 0 3 1 0 1 0 17 8 10 1 0 11 24 1 8 10 53 6 1 1 0 4 1 1 0 6 1 0 13 10 3 3 4 0
*
*
*
Dominance
*
S. Liu et al. / Acta Ecologica Sinica 36 (2016) 236–245
Rotifera Asplanchna priodonta Asplanchna girodi Asplanchna brightwelli Ascomorpha ecaudis Ascomorpha saltans Anuraeopsis fissa Asplanchnopus multiceps Brachionus quadridentatus Brachionus urceus Brachionus calyciflorus Brachionus leydigi Brachionus angularis Brachionus caudatus Brachionus budapestiensis Brachionus forficula Brachionus diversicornis Chromogaster ovalis Colurella uncinata Colurella adriatica Colurella uncinata forma bicuspidata Cephalodella exigna Cephalodella incila Diplois daviesiae Diurella rousseleti Diurella dixon-nuttalli Dissotrocha aculeata Dicranophorus forcipatus Euchlanis lyra Epiphanes senta Eosphora najas Euchlanis dilatata Filinia longiseta Keratella valga Keratella cochlearis Keratella quadrata Lecane luna Lecane ungulata Lecane inermis Lecane glypta Lecane leontina Lecane sympoda Lepadella ovalis Lepadella patella Lindia truncata Monostyla pyriformis Monostyla unguitata Monostyla lunaris Monostyla bulla Monostyla elachis Monostyla closterocerca Notholca labis
X
*
239
(continued on next page)
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Table 3 (continued) W
X Occurrence (%)
Notholca squamula Pompholyx complanta Pompholyx sulcata Polyarthra trigla Polyarthra dolichoptera Polyarthra minor Platyias militaris Platyias quadricornis Proales daphnicola Resticula melandocus Rhinoglena frontalis Synchaeta oblonga Synchaeta tremula Synchaeta stylata Synchaeta pectinata Schizocerca diversicornis Scaridium longicaudum Trichocerca longiseta Trichocerca similis Trichocerca elongata Trichocerca gracilis Trichocerca weberi Trichocerca rousseleti Trichocerca porcellus Testudinella patina
+++ +++ +++ +++ +++ − − − − − − +++ +++ − − − − +++ ++ +++ +++ +++ +++ − −
3 28 6 33 24 0 0 0 0 0 21 1 0 0 0 0 1 3 3 1 1 4 0 0
Cladocera Alona rectangula Bosmina longirostris Bosminopsis deitersi Ceriodaphnia cornuta Ceriodaphnia quadrangula Chydorus sphaericus Daphnia hyalina Daphnia pulex Diaphanosoma brachyurum Diaphanosoma leuchtenbergianum Diaphanosoma sarsi Moina brachiata Moina macrocopa Moina micrura Moina affinis Moina rectirostris Moin odaphnia macleayi Pleuroxus aduncus Rhynchotalona falcata Simocephalus vetulus Simocephalus vetuloides Scapholeberis kingi Scapholeberis mucronata
+ + + + − + + − + + − + + + + − + + − + − − +
11 31 7 1 0 6 11 0 6 8 0 1 1 17 3 0 3 1 0 1 0 0 7
Copepoda Nauplius larva Cyclops vicinus vicinus Eucyclops serrulatus
++ ++ −
90 14 0
Dominance
* *
*
*
Abundance
Occurrence (%)
− +++ +++ +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ +++ +++ − +++ − +++ − − +++ +++
0 3 14 57 17 14 1 1 11 1 1 8 0 7 4 7 1 0 24 0 6 0 0 1 6
+ + + − + + + + ++ + + + − + − + − + + + + + +
6 18 33 0 4 1 13 1 19 7 1 1 0 24 0 3 0 1 1 3 3 3 1
++ + +
83 10 4
Dominance
*
*
*
*
S. Liu et al. / Acta Ecologica Sinica 36 (2016) 236–245
Abundance
*
*
*
241
such as Thermocyclops sp., Sinocalanus sp. and Moina micrura were presented in both areas. The SIMPER analysis revealed that Rotifera was the primary contributor to the similarity in each group and dissimilarity between groups, the within-group average similarity was 53.11% in West Lake and 49.23% in Xixi Wetland, and between-group average dissimilarity was 69.51%. The typical species that contributed to the dissimilarity between two biotopes were summarized in Table 4. Of 14 rotifer species, Eosphora najas was the most primary contributor to the dissimilarity; P. dolichoptera was the common/dominant species in both wetland systems, while Asplanchna brightwelli and Monostyla unguitata were occurred in Xixi Wetland but absent from West Lake. Schizocerca diversicornis was present in West Lake but not in Xixi Wetland.
0 3 49 1 11 7 0 0 40 17 6 0 63 28 13 18 43 8
*
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3.3. Spatiotemporal variations in abundance
* *
*
*
*
− + ++ + + + − − + + + − ++ + + + + +
The spatiotemporal variations in abundance of the three zooplankton groups are showed in Fig. 2. The West Lake group included Fig. a-c and the Xixi Wetland group comprised Fig. d-f. It should be noted that these groups occurred in specific spatiotemporal distribution patterns. For example, Cladocera was the dominant zooplankton group at site 2 of West Lake in August (Fig. 2b), while it was leading in June at site B of Xixi Wetland (Fig. 2e). Copepoda mainly dominated at sites 1 and 2 of West Lake in September (Fig. 2c), this situation occurred in February at site C of Xixi Wetland (Fig. 2f). By contrast, the abundance of Rotifera presented many peaks, which indicates that this group was the highest contributor in abundance. The dendrogram showed that the zooplankton community patterns were discriminated into two groups, primarily by season, at a 90% similarity (Fig. 4). The first group included summer and autumn at all stations (W-su, X-su, W-au, X-au) and the second group comprised spring and winter at all stations (W-wi, X-wi, W-sp, X-sp). A significant difference between the groups was confirmed by ANOSIM at global R = 0.865, P = 0.029.
“*” Dominant species, “+” Abundance (ind.l−1), “−” Absent, “+” 1, “++” 1–10, “+++” 10–100.
Limnoithona tetraspina Limnoithona sinensis Mesocyclops leuckarti Neodiaptomus schmackeri Onychocamptus mohammed Paracyclops fimbriatus Paracyclopina nana Sinocalanus tenellus Sinocalanus dorrii Sinocalanus sinensis Schmackeria poplesia Schmackeria forbesi Thermocyclops taihokuensis Thermocyclops hyalinus Thermocyclops kawamurai Thermocyclops dybowskii Thermocyclops mongolicus Thermocyclops brevifurcatus
+ − + + + + + + + + + + + + + + + +
8 0 29 3 11 6 8 4 54 1 2 4 36 13 25 33 24 7
3.4. Relationships between biota and abiota The relationships between zooplankton and environmental variables in the six sampling stations were investigated using cluster and MDS/PCA ordination (Fig. 5a, b). There was a clear discrimination between the two water bodies as both the zooplankton and environmental variables are concerned. Thus, all stations in West Lake were separated from all sites of Xixi Wetland. It is indicated that, the zooplankton communities has the significant difference between the two water areas (Fig. 5a). The results of principal component analysis (PCA), with vectors for physicochemical variables at each site are shown in Fig. 5b. Two principal components accounted for 76.6% of the total spatial environment variables (PC1 = 50.1%; PC2 = 26.5%). The first axis represented nutrients (eg. TN, TP, and NO3-N) were mainly distributed in the left part, thus separating the eutrophic sites (A, B, C, E and 6) from other sites. It should be noted that the NO3-N, NO2-N, NH4-N and TP were strongly correlated with the PC1, which was the primary contributor to the environmental patterns (50.1%). The second axis separated all sites in Xixi Wetland located in above and almost all sites in West Lake distributed at bottom, which meaning West Lake and Xixi Wetland had significant variance, and, this spatial distribution pattern of environmental variables was consistent with those of zooplankton communities showed in Fig. 5a. Meanwhile, the DO, COD, pH and TP distributed at bottom of Fig 5b, thus separating the high organic pollutant sites (1, 2, 3, 4, 5 and 6) from the water body of Xixi Wetland (26.5%) and two less polluted sites D and F from other sites. The BIOENV analyses present the matching degree between environmental factors and zooplankton communities. The result revealed that NO2-N and NO3-N was the best match to explain the temporal
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Table 4 The SIMPER analysis showing the average abundance (ind/l) of the most important species and between-group dissimilarity (%) summed across those species contribution ≥2% of West Lake (W) and Xixi Wetland (X) during Jun. 2013 to May 2014. Species
W
X
Dissimilarity (%)
Ascomorpha saltans Asplanchna girodi Asplanchna brightwelli Eosphora najas Euchlanis dilatata Epiphanes senta Keratella valga Monostyla unguitata Polyarthra dolichoptera Proales daphnicola Polyarthra trigla Pompholyx complanata Schizocerca diversicornis Trichocerca similis
2.5 24.33 0 73.31 38.22 4.83 3.33 0 57.35 0 37.14 23.91 18.96 2.67
31.81 20.29 18.87 19.61 2.5 41.03 24.17 18.19 23.67 28.98 29.53 5.25 0 27.69
2.64 2.29 1.5 4.59 3.06 2.86 1.92 1.39 2.74 2.15 1.77 1.69 1.6 1.88
variation in zooplankton communities in West Lake, and pH, DO, T and COD was the best match in Xixi Wetland (Table 5). Diversity indices can serve as a useful indicator of the overall pollution of water, the lower in the values of diversity index shows the rise in the level of the pollution [32]. Comparing the average data on the species diversity indices of the two stations, it has been observed in 1 year circle that the higher values of d, J′ and H′ indexes were recorded in Xixi Wetland (d = 8.07, J′ = 0.84, H′ = 3.33) compare to West Lake (d = 6.56, J′ = 0.75, H′ = 2.79). It is indicating that the condition of water quality in Xixi Wetland was slightly better than West Lake, and was also fit with the consequence of Fig. 5. 4. Disscussion In order to compare the difference in zooplankton communities in response to water quality between the two urban landscapes in Hangzhou City, we apply the powerful multivariate analyses [25]. At present, there were very few studies comparing the freshwater in urban landscape areas. In this study, the freshwater analyzed in present study are shallow systems. Abiotic variables, such as primary nutrients, can be easily and repeatedly measured, which is useful in monitoring programs [29]. The values of TP, NH4-N, NO2-N in Xixi Wetland were almost higher than in West Lake during the whole year, that is probably due to more domestic sewage be discharged in Xixi Wetland and the influence of
fishery production. For the value of Chemical oxygen demand (COD), West Lake was higher than Xixi Wetland during the research period, indicating a more serious organic pollution or excessive organic matter decomposition. As the abiotic indices are sensitive to short-term changes in water quality, the seasonal pattern showed in Fig. 3 indicating rainy season may influence water physicochemical factors more or less. Relative to abiotic indices, biotic indices can tell more about longerterm conditions. Because of species assemblages exhibit the cumulative impacts of stressors on a habitat over time, biological data are preferred by investigators to use in monitoring water environment [29]. Similar domination of rotifers was observed in both collect stations (Fig. 2), and 14 rotifer species were the main contributors to between-group dissimilarity (Table 4). It has been suggested that the apparent dominance of rotifers maybe due to their relatively short generation times and rare to be preyed by fish which compared with the larger crustacean zooplankton [20,34]. The cluster analysis demonstrated that zooplankton communities distribution have significant seasonal variability (Fig. 4), the total Rotifer species number and abundance during four seasons in Xixi Wetland were higher than that in West Lake, while the diversity of microcrustacean didn't have significant difference in two survey areas, so Rotifer communities might have been the primary contributor leading to the difference between West Lake and Xixi Wetland. The dominant species, e.g., A. priodonta, P. trigla, Bosmina longirostris, Diaphanosoma brachyurum, Mesocyclops leuckarti as the indicators of the eutrophic status of water bodies were recorded both in the two
Fig. 2. The spatial-temporal variations in species abundance of three zooplankton groups in West Lake (a–c) and Xixi Wetland (d–e) during the study period.
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Table 5 Summary of bio-environment (BIOENV) analysis showing the 10 best matches of environmental variables with temporal variations in zooplankton abundances in West Lake (W) and Xixi Wetland (X) in Hangzhou China during Jun. 2013 to May 2014. Rank
W
Chemical variable
X
P values 1 2 3 4 5 6 7 8 9 10
0.433 0.433 0.411 0.403 0.402 0.396 0.388 0.385 0.378 0.374
Chemical variable
P values NO3-N NO2-N, NO3-N TN, NO2-N, NO3-N TP, NO2-N, NO3-N TN, NO3-N TP, NO3-N NH4-N, NO2-N, NO3-N TP, TN, NO3-N TP, TN, NO2-N, NO3-N TN, NH4-N, NO2-N, NO3-N
0.587 0.587 0.585 0.582 0.581 0.574 0.571 0.567 0.566 0.562
pH, DO, T, COD pH, DO, T, COD, TP DO, T, COD DO, T, COD, TP pH, DO, T, COD, TN DO, T, COD, TP pH, DO, T, COD, NO2-N DO, T, COD, TP, TN DO, T, COD, TP, NO2-N DO, T, COD, NO2-N
P value = Spearman correlation coefficient; T = Water temperature, DO = Dissolved oxygen, COD = Chemical oxygen demand, TN = Total nitrogen, TP = Total phosphorus, NH4-N = Ammonium nitrogen, NO3-N = Nitrate nitrogen, NO2-N = Nitrite nitrogen.
areas [7,9,15]. Other indicator species, such as Brachionus angularis, K. cochlearis, and Filinia longiseta were more abundant in Xixi Wetland [10], Ferdous and Muktadir [8] concluded the Cladocera species of Ceriodaphnia quadrangula as indicators of the eutrophic status of water bodies, in our study, it was found to be present in Xixi Wetland but absent in West Lake. It is clear that although there was little difference between these two research areas about dominance species, but the zooplankton communities structure also had a significant difference.
dominant community, and 14 rotifer species were the main contributors to this dissimilarity. 3. All these results indicates that changes of conditions affecting the faunistic composition of the plankton occurred, so plankton should be preferred over others for early signals due to their low cost, less time consumption and ease of handling. 4. Comparative studies about urban landscape freshwater system in Hangzhou city will keep long-term research to provide reliable information for water quality monitoring.
5. Conclusions Acknowledgements 1. The physicochemical and zooplankton composition of the two water areas reveals that the water quality of Xixi wetland is better than Westlake, although it is also polluted by human activities. 2. A significant difference was found in zooplankton community structure between both wetland systems, and Rotifera assemblage as the
This work was supported by the Natural Science Foundation of China (project numbers: 31272262, 31071880 and 41076089). Zhejiang Key Scientific & Technological Innovation Team Project (2010R50039-20), and the Hangzhou Key Laboratory for Animal Adaptation and Evolution (20100333T05). I wish to thank Yong Jiang, Zhe Chen, Ping Zhang for
Fig. 3. Cluster analysis of physicochemical variable in the both areas during June 2013 to May 2014. (W, West Lake; X, Xixi Wetland; su, summer; au, autumn; wi, winter; sp, spring).
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Fig. 4. Cluster analysis of zooplankton community in the both areas during June 2013 to May 2014 (W, West Lake; X, Xixi Wetland; su, summer; au, autumn; wi, winter; sp., spring).
Fig. 5. Multidimensional scaling (MDS) ordination with cluster analysis for spatial patterns of zooplankton communities (a) and Principal component analysis (PCA) plot based on the annual average data of log-transformed abiotic and forth foot-transformed biotic in the twelve stations.
improving the manuscript and thank Cuicui Hou, Xiaowen Zhu for helping in sampling collection.
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Contents lists available at ScienceDirect
Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Seasonal shift in zooplankton communities in two sub-tropical urban wetlands, Southern China Songlu Liu a, Xinlu Shi a,⁎, Henglong Xu b,⁎, Guijie Liu a, Cuicui Hou a, Xiaowen Zhu a a b
Hangzhou Key Laboratory for Animal Adaptation and Evolution, Hangzhou Normal University, Hangzhou 310036, China Laboratory of Microbial Ecology, College of Marine Life Science, Ocean University of China, Qingdao 266003, China
a r t i c l e
i n f o
Article history: Received 5 July 2015 Received in revised form 1 February 2016 Accepted 4 March 2016 Keywords: Urban landscape Zooplankton Bioindicator Species diversity Sub-tropical wetland Environmental stress
a b s t r a c t The seasonal shift in the community pattern of zooplankton was studied in two typical urban landscape wetland systems (West Lake and Xixi Wetland) during four. seasons (June 2013 to May 2014). Samples were monthly collected at six sampling stations within a gradient of environmental stress in West Lake and Xixi Wetland, respectively. A total of 119 zooplankton species were identified, comprising 75 rotifers, 23 cladocerans and 21 copepods. Multivariate analysis revealed that: (1) the species compositions represented significant differences between two biotopes, with Rotifera assemblage as the primary contributor to the difference; (2) the community structures showed dissimilar seasonal variation in both wetlands, and 14 rotifer species were the main contributors to this dissimilarity; (3) the temporal variations in zooplankton community structures were significantly correlation with the environmental variables in both systems, especially NO2-N and NO3-N in West Lake, pH, DO, T, COD in Xixi Wetland; (4) the species diversity indices (Margalef, Pielou and Shannon-Wiener) showed higher values in Xixi Wetland than that in West Lake. Based on the above results, we suggest that zooplankton community structures are significantly shaped by environmental drivers, and thus may be used as potential bioindicators of water quality in sub-tropical urban landscape wetland ecosystems. © 2015 Published by Elsevier B.V. on behalf of Ecological Society of China.
Contents 1. 2.
Introduction . . . . . . . . . . . . . . . . Materials and methods . . . . . . . . . . . 2.1. Study area and sampling sites . . . . . 2.2. Sampling and data collection . . . . . 2.3. Data analyses . . . . . . . . . . . . 3. Results . . . . . . . . . . . . . . . . . . . 3.1. Environmental variables. . . . . . . . 3.2. Species composition and typical species. 3.3. Spatiotemporal variations in abundance 3.4. Relationships between biota and abiota . 4. Disscussion . . . . . . . . . . . . . . . . . 5. Conclusions. . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . .
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1. Introduction
⁎ Corresponding authors. E-mail addresses: [email protected] (X. Shi), [email protected] (H. Xu).
http://dx.doi.org/10.1016/j.chnaes.2016.03.006 1872-2032/© 2015 Published by Elsevier B.V. on behalf of Ecological Society of China.
Zooplankton plays a significant role as the primary link in the local trophic food chain, transferring the energy from bacteria/phytoplankton to other invertebrates and fish in aquatic ecosystems [28,33]. Because of short life cycle and quick response to the environment changes, their
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Fig. 1. Map showing the sampling stations in West Lake and Xixi Wetland, Hangzhou, China.
changes in abundance, species diversity and community composition may provide important indications of environmental change or disturbance [6,31]. Compared with single species-based indicator, the community-based bioassessment has proved to be the more reliable [19]. In previous decades, many studies on freshwater zooplankton communities have been carried out in different bodies like rivers, streams, lakes and smaller aquatic habitats (e.g., [3,11,20,23]). However, as regards the differences in zooplankton community patterns and their relationships to water conditions between lake and wetland systems, little information is known [18,21,32,41]. West Lake, located near Hangzhou city, southern China, is one of the world cultural heritages, with an area of 6.5 km2 and a mean depth of 2.7 m. In 1999, after the water diversion from Qiantang River and dredge project was finished, the water eutrophication of the lake had been improved [22,42]. Xixi Wetland, located in the same city, is the Table 1 The location and character of the twelve sampling sites. Sites
Location
Character
1 2 3 4 5 6 A B C D E F
N30°15′23.61″, E120°08′27.04″ N30°15′41.07″, E120°08′53.03″ N30°15′28.23″, E120°09′08.71″ N30°14′57.04″, E120°09′20.63″ N30°13′56.41″, E120°08′20.92″ N30°14′04.34″, E120°08′16.09″ N30°15′33.16″, E120°03′26.81″ N30°15′58.53″, E120°03′33.19″ N30°16′16.59″, E120°03′19.60″ N30°16′20.15″, E120°03′20.15″ N30°16′29.49″, E120°03′47.39″ N30°16′29.14″, E120°03′55.06″
Water diversion corner, lotus, fish Spacious, much more tourists Near water outlet, restaurant Located in outer lake Near water inlet Ornamental fish pond Near water inlet, wharf Farming, fishing River intersection, market place Natural riverway Ornamental riverway, Near water outlet Ornamental pond
representative national wetland park with urban, farming and culture in China, and its water network belongs to the canal water system. It covers an area of 5.29 km2, which was studded with network river and scaly pond with a mean depth of 2.13 m [16,17,27]. With the rapid development of social and economical conditions, both wetland systems as the urban landscape have been more vulnerable to suffer pollution from human activities [35]. In this study, the zooplankton community features and their relationship to changes of environmental conditions were comparatively studied in both wetland systems during a 1-year period (June 2013 to May 2014). The aims of this study were: (1) to document the zooplankton community composition and species diversity between the two different water bodies, (2) to show the difference in zooplankton community structures in response to environment variables between the two biotopes, and (3) to assess the environmental quality status of both urban landscapes based on zooplankton community. 2. Materials and methods 2.1. Study area and sampling sites A total of twelve sampling stations (1–6, A–F) were selected in Xixi Wetland and West Lake (Fig. 1). Their characteristics were presented in Table 1. 2.2. Sampling and data collection Samples were monthly collected from June 2013 to May 2014. At each sampling site, samples were taken from upper-mid-bottom layers mixed of the water using an organic glass hydrophore (2.5 l) [25]. The
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Table 2 The monthly mean values and standard deviation of physicochemical parameters at two water bodies during the four seasons. Parameters
W-su
W-au
W-wi
W-sp
X-su
X-au
X-wi
X-sp
pH Temp (°C) DO (mg/L) COD (mg/L) TP (mg/L) TN (mg/L) NH4-N (mg/L) NO2-N (mg/L) NO3-N (mg/L)
8.5 ± 0.67 31.5 ± 1.76 7.46 ± 1.07 18.1 ± 8.80 0.11 ± 0.06 1.53 ± 0.37 0.09 ± 0.08 0.03 ± 0.02 0.60 ± 0.53
7.29 ± 1.19 21.5 ± 5.93 7.87 ± 1.27 15.7 ± 6.07 0.09 ± 0.03 1.03 ± 1.87 0.06 ± 0.27 0.02 ± 0.07 1.09 ± 1.12
7.34 ± 0.79 9.16 ± 2.40 10.4 ± 0.91 9.44 ± 3.24 0.06 ± 0.03 3.12 ± 0.88 0.28 ± 0.33 0.04 ± 0.02 2.30 ± 0.50
8.07 ± 0.59 20.1 ± 5.24 8.42 ± 2.02 5.0 ± 6.19 0.07 ± 0.03 2.96 ± 0.75 0.14 ± 0.07 0.04 ± 0.04 2.22 ± 0.65
6.71 ± 0.57 29.0 ± 3.88 4.62 ± 1.30 15.9 ± 7.61 0.15 ± 0.01 1.32 ± 1.10 0.60 ± 1.25 0.03 ± 0.03 0.57 ± 0.89
6.86 ± 0.61 20.2 ± 6.22 4.98 ± 1.47 11.1 ± 5.35 0.14 ± 0.08 1.87 ± 1.21 0.27 ± 0.40 0.07 ± 0.07 1.12 ± 0.77
7.50 ± 0.30 9.44 ± 1.51 8.83 ± 1.60 8.06 ± 3.44 0.10 ± 0.07 2.80 ± 1.41 0.32 ± 0.27 0.04 ± 0.03 1.80 ± 1.17
7.45 ± 0.24 22.2 ± 3.82 6.71 ± 1.56 14.7 ± 7.70 0.15 ± 0.07 2.07 ± 1.37 0.26 ± 0.27 0.07 ± 0.05 1.37 ± 1.00
W = West Lake, X = Xixi Wetland, su = Summer, au = Autumn, wi = Winter, sp. = Spring; DO = Dissolved oxygen, COD = Chemical oxygen demand, BOD5 = Biological oxygen demand, TN = Total nitrogen, TP = Total phosphorus, NH4-N = Ammonium nitrogen, NO3-N = Nitrate nitrogen, NO2-N = Nitrite nitrogen.
quantitative samples of microcrustacean were gathered approximately 50 ml, which filtered 20 l the mixed water through #25 plankton net and fixed with 4% Formaldehyde immediately. All samples were observed and counted under dissecting microscope. Rotifera samples were gathered in 1000 ml organic glass hydrophore and fixed with Lugol's iodine solution (1.5% final concentration, v/v), precipitated for 36 h and the final volume set to 50 ml of concentrated sediments, a 1 ml subsample of this final concentrated sample was placed to observe and count under light microscope. The physicochemical parameters were measured within 12 h from 1000 ml water samples. Zooplankton samples were identified according to the keys of Shen [24], Jiang and Du [13], Wang [36], Zhou and Chen [43] in Chinese under compound microscope (Leica DM6000B) and dissecting microscope (Leica M205A). Water temperature (T), pH and dissolved oxygen (DO) were measured in situ with an OHAUS ST20 and HACH HQ30d. The determination of chemical oxygen demand (COD), total nitrogen (TN), and total phosphorus (TP), ammonium nitrogen (NH4-N), nitrate nitrogen (NO3-N), nitrite nitrogen (NO2-N) was performed following standard methods of American Public Health Association [1]. 2.3. Data analyses A univariable analysis involving mean values and standard deviation (SD) values was applied to assess the abiotic variables in sites and seasons. Species diversity (Shannon-Wiener H′), evenness (Pielou J′) and richness (Margalef d) indices are commonly employed in communitylevel investigations and are suitable for simple statistical analyses [12]. The three indices were computed following the equations: H0 ¼ −
S X
P i ð ln P i Þ
i¼1
J0 ¼ H0= ln S d ¼ ðS−1Þ= ln N where H′ = observed diversity index; Pi = proportion of the total count arising from the ith species; S = total number of species; and N = total number of individuals. Dominance index (Y) of species in each sample was calculated using the following formula: Y¼
ni f N i
where ni is the number of individuals of species i, fi is the frequency of species i that occurred in a sample, and N is the total number of species(Y N 0.02). Multivariate analysis of biotic and abiotic data among sites and seasons were analyzed with PRIMER 5.0 [4]. Clustering analysis and MDS ordination were conducted based on standardized Euclidean distances
from log-transformed physicochemical variables and on Bray-Curtis similarity matrix from fourth-foot transformed biotic communities [2, 26,30]. An analysis of similarity (ANOSIM) was run to determine the significant discrepancies between different groups of physicochemical data and biotic abundance [5]. The R value of ANOSIM close to 1 indicating that the groups are entirely separate and 0 value indicating that there is no difference between groups [5]. A similarity percentage-species contribution (SIMPER) analysis was used to identify the typical species that contributed to group similarity [30,39]. The spatial environmental status of the twelve sampling sites was summarized using the principle component analysis (PCA) based on Euclidean distance matrices from log-transformed abiotic data [40]. The submodule BIOENV was used to analyze potential relationships between biotic variables and abiotic data [37,38]. 3. Results 3.1. Environmental variables The fluctuations in the mean values and the range of various physicochemical parameters at two water bodies during study period were summarized in Table 2. Average water temperature followed an annual pattern (e.g. summer N autumn = spring N winter), and presented no differences between the two areas. The pH values in West Lake were general higher than Xixi Wetland, except in summer. Values of DO had a negative relationship with temperature in both areas, and usually they were lower in Xixi Wetland than in West Lake and this was also the fact for COD, TN and NO3-N values during the entire sampling period. On the contrary, TP, NH4-N, NO2-N values were higher in Xixi Wetland than in West Lake. The hierarchical clustering of Euclidean distance of physicochemical variables among sites and seasons is presented in Fig. 3. The cluster analysis revealed two groups at a 0.7 distance. The first group included summer at both sites and autumn in Xixi Wetland (W-su, X-su, X-au), the second group comprised spring and winter at both sites and autumn in Xixi Wetland (W-sp, X-sp, W-wi, X-wi). The result showed the significant difference of total environment data about two stations only expressed in autumn. ANOSIM was able to detected significant differences among the sites and seasons in physicochemical parameters at global R = 0.792, P = 0.018. 3.2. Species composition and typical species A total of 119 zooplankton species were identified, comprising 75 rotifers, 23 cladocerans, 21 copepods. The abundance, occurrence and dominant species were summarized in Table 3. In West Lake, the zooplankton was composed of 39 rotifers, 16 cladocerans, 19 copepods, while in Xixi Wetland, 57 rotifers, 19 cladocerans and 16 copepods were recorded. The dominant species of Rotifera in Xixi Wetland were Anuraeopsis fissa, Keratella cochlearis and Polyarthra trigla, while on this basis it also included Asplanchna priodonta, Euchlanis dilatata and Polyarthra dolichoptera in West Lake. The dominant crustacean species
Table 3 The abundance, occurrence and dominant species of zooplankton in West Lake (W) and Xixi Wetland (X) during June 2013 to May 2014. W Abundance
Occurrence (%)
Dominance
Abundance
Occurrence (%)
+++ +++ − − +++ +++ − − − +++ +++ ++ − +++ +++ +++ − +++ +++ − +++ − +++ − − − − +++ +++ ++ +++ − ++ ++ − ++ +++ +++ +++ − − +++ − − +++ − − − − − +++
50 8 0 0 1 36 0 0 0 13 1 6 0 1 6 15 0 3 6 0 1 0 1 0 0 0 0 4 3 22 26 0 3 38 0 1 6 3 1 0 0 1 0 0 1 0 0 0 0 0 10
*
+++ +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ − − − +++ − ++ ++ − ++ − +++ +++ +++ +++ − +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ +++ − +++ +++ − +++ +++ +++ +++ ++ −
11 7 18 14 1 40 1 1 3 25 0 26 1 0 0 0 8 0 3 1 0 1 0 17 8 10 1 0 11 24 1 8 10 53 6 1 1 0 4 1 1 0 6 1 0 13 10 3 3 4 0
*
*
*
Dominance
*
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Rotifera Asplanchna priodonta Asplanchna girodi Asplanchna brightwelli Ascomorpha ecaudis Ascomorpha saltans Anuraeopsis fissa Asplanchnopus multiceps Brachionus quadridentatus Brachionus urceus Brachionus calyciflorus Brachionus leydigi Brachionus angularis Brachionus caudatus Brachionus budapestiensis Brachionus forficula Brachionus diversicornis Chromogaster ovalis Colurella uncinata Colurella adriatica Colurella uncinata forma bicuspidata Cephalodella exigna Cephalodella incila Diplois daviesiae Diurella rousseleti Diurella dixon-nuttalli Dissotrocha aculeata Dicranophorus forcipatus Euchlanis lyra Epiphanes senta Eosphora najas Euchlanis dilatata Filinia longiseta Keratella valga Keratella cochlearis Keratella quadrata Lecane luna Lecane ungulata Lecane inermis Lecane glypta Lecane leontina Lecane sympoda Lepadella ovalis Lepadella patella Lindia truncata Monostyla pyriformis Monostyla unguitata Monostyla lunaris Monostyla bulla Monostyla elachis Monostyla closterocerca Notholca labis
X
*
239
(continued on next page)
240
Table 3 (continued) W
X Occurrence (%)
Notholca squamula Pompholyx complanta Pompholyx sulcata Polyarthra trigla Polyarthra dolichoptera Polyarthra minor Platyias militaris Platyias quadricornis Proales daphnicola Resticula melandocus Rhinoglena frontalis Synchaeta oblonga Synchaeta tremula Synchaeta stylata Synchaeta pectinata Schizocerca diversicornis Scaridium longicaudum Trichocerca longiseta Trichocerca similis Trichocerca elongata Trichocerca gracilis Trichocerca weberi Trichocerca rousseleti Trichocerca porcellus Testudinella patina
+++ +++ +++ +++ +++ − − − − − − +++ +++ − − − − +++ ++ +++ +++ +++ +++ − −
3 28 6 33 24 0 0 0 0 0 21 1 0 0 0 0 1 3 3 1 1 4 0 0
Cladocera Alona rectangula Bosmina longirostris Bosminopsis deitersi Ceriodaphnia cornuta Ceriodaphnia quadrangula Chydorus sphaericus Daphnia hyalina Daphnia pulex Diaphanosoma brachyurum Diaphanosoma leuchtenbergianum Diaphanosoma sarsi Moina brachiata Moina macrocopa Moina micrura Moina affinis Moina rectirostris Moin odaphnia macleayi Pleuroxus aduncus Rhynchotalona falcata Simocephalus vetulus Simocephalus vetuloides Scapholeberis kingi Scapholeberis mucronata
+ + + + − + + − + + − + + + + − + + − + − − +
11 31 7 1 0 6 11 0 6 8 0 1 1 17 3 0 3 1 0 1 0 0 7
Copepoda Nauplius larva Cyclops vicinus vicinus Eucyclops serrulatus
++ ++ −
90 14 0
Dominance
* *
*
*
Abundance
Occurrence (%)
− +++ +++ +++ +++ +++ +++ +++ +++ +++ +++ +++ − +++ +++ +++ +++ − +++ − +++ − − +++ +++
0 3 14 57 17 14 1 1 11 1 1 8 0 7 4 7 1 0 24 0 6 0 0 1 6
+ + + − + + + + ++ + + + − + − + − + + + + + +
6 18 33 0 4 1 13 1 19 7 1 1 0 24 0 3 0 1 1 3 3 3 1
++ + +
83 10 4
Dominance
*
*
*
*
S. Liu et al. / Acta Ecologica Sinica 36 (2016) 236–245
Abundance
*
*
*
241
such as Thermocyclops sp., Sinocalanus sp. and Moina micrura were presented in both areas. The SIMPER analysis revealed that Rotifera was the primary contributor to the similarity in each group and dissimilarity between groups, the within-group average similarity was 53.11% in West Lake and 49.23% in Xixi Wetland, and between-group average dissimilarity was 69.51%. The typical species that contributed to the dissimilarity between two biotopes were summarized in Table 4. Of 14 rotifer species, Eosphora najas was the most primary contributor to the dissimilarity; P. dolichoptera was the common/dominant species in both wetland systems, while Asplanchna brightwelli and Monostyla unguitata were occurred in Xixi Wetland but absent from West Lake. Schizocerca diversicornis was present in West Lake but not in Xixi Wetland.
0 3 49 1 11 7 0 0 40 17 6 0 63 28 13 18 43 8
*
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3.3. Spatiotemporal variations in abundance
* *
*
*
*
− + ++ + + + − − + + + − ++ + + + + +
The spatiotemporal variations in abundance of the three zooplankton groups are showed in Fig. 2. The West Lake group included Fig. a-c and the Xixi Wetland group comprised Fig. d-f. It should be noted that these groups occurred in specific spatiotemporal distribution patterns. For example, Cladocera was the dominant zooplankton group at site 2 of West Lake in August (Fig. 2b), while it was leading in June at site B of Xixi Wetland (Fig. 2e). Copepoda mainly dominated at sites 1 and 2 of West Lake in September (Fig. 2c), this situation occurred in February at site C of Xixi Wetland (Fig. 2f). By contrast, the abundance of Rotifera presented many peaks, which indicates that this group was the highest contributor in abundance. The dendrogram showed that the zooplankton community patterns were discriminated into two groups, primarily by season, at a 90% similarity (Fig. 4). The first group included summer and autumn at all stations (W-su, X-su, W-au, X-au) and the second group comprised spring and winter at all stations (W-wi, X-wi, W-sp, X-sp). A significant difference between the groups was confirmed by ANOSIM at global R = 0.865, P = 0.029.
“*” Dominant species, “+” Abundance (ind.l−1), “−” Absent, “+” 1, “++” 1–10, “+++” 10–100.
Limnoithona tetraspina Limnoithona sinensis Mesocyclops leuckarti Neodiaptomus schmackeri Onychocamptus mohammed Paracyclops fimbriatus Paracyclopina nana Sinocalanus tenellus Sinocalanus dorrii Sinocalanus sinensis Schmackeria poplesia Schmackeria forbesi Thermocyclops taihokuensis Thermocyclops hyalinus Thermocyclops kawamurai Thermocyclops dybowskii Thermocyclops mongolicus Thermocyclops brevifurcatus
+ − + + + + + + + + + + + + + + + +
8 0 29 3 11 6 8 4 54 1 2 4 36 13 25 33 24 7
3.4. Relationships between biota and abiota The relationships between zooplankton and environmental variables in the six sampling stations were investigated using cluster and MDS/PCA ordination (Fig. 5a, b). There was a clear discrimination between the two water bodies as both the zooplankton and environmental variables are concerned. Thus, all stations in West Lake were separated from all sites of Xixi Wetland. It is indicated that, the zooplankton communities has the significant difference between the two water areas (Fig. 5a). The results of principal component analysis (PCA), with vectors for physicochemical variables at each site are shown in Fig. 5b. Two principal components accounted for 76.6% of the total spatial environment variables (PC1 = 50.1%; PC2 = 26.5%). The first axis represented nutrients (eg. TN, TP, and NO3-N) were mainly distributed in the left part, thus separating the eutrophic sites (A, B, C, E and 6) from other sites. It should be noted that the NO3-N, NO2-N, NH4-N and TP were strongly correlated with the PC1, which was the primary contributor to the environmental patterns (50.1%). The second axis separated all sites in Xixi Wetland located in above and almost all sites in West Lake distributed at bottom, which meaning West Lake and Xixi Wetland had significant variance, and, this spatial distribution pattern of environmental variables was consistent with those of zooplankton communities showed in Fig. 5a. Meanwhile, the DO, COD, pH and TP distributed at bottom of Fig 5b, thus separating the high organic pollutant sites (1, 2, 3, 4, 5 and 6) from the water body of Xixi Wetland (26.5%) and two less polluted sites D and F from other sites. The BIOENV analyses present the matching degree between environmental factors and zooplankton communities. The result revealed that NO2-N and NO3-N was the best match to explain the temporal
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Table 4 The SIMPER analysis showing the average abundance (ind/l) of the most important species and between-group dissimilarity (%) summed across those species contribution ≥2% of West Lake (W) and Xixi Wetland (X) during Jun. 2013 to May 2014. Species
W
X
Dissimilarity (%)
Ascomorpha saltans Asplanchna girodi Asplanchna brightwelli Eosphora najas Euchlanis dilatata Epiphanes senta Keratella valga Monostyla unguitata Polyarthra dolichoptera Proales daphnicola Polyarthra trigla Pompholyx complanata Schizocerca diversicornis Trichocerca similis
2.5 24.33 0 73.31 38.22 4.83 3.33 0 57.35 0 37.14 23.91 18.96 2.67
31.81 20.29 18.87 19.61 2.5 41.03 24.17 18.19 23.67 28.98 29.53 5.25 0 27.69
2.64 2.29 1.5 4.59 3.06 2.86 1.92 1.39 2.74 2.15 1.77 1.69 1.6 1.88
variation in zooplankton communities in West Lake, and pH, DO, T and COD was the best match in Xixi Wetland (Table 5). Diversity indices can serve as a useful indicator of the overall pollution of water, the lower in the values of diversity index shows the rise in the level of the pollution [32]. Comparing the average data on the species diversity indices of the two stations, it has been observed in 1 year circle that the higher values of d, J′ and H′ indexes were recorded in Xixi Wetland (d = 8.07, J′ = 0.84, H′ = 3.33) compare to West Lake (d = 6.56, J′ = 0.75, H′ = 2.79). It is indicating that the condition of water quality in Xixi Wetland was slightly better than West Lake, and was also fit with the consequence of Fig. 5. 4. Disscussion In order to compare the difference in zooplankton communities in response to water quality between the two urban landscapes in Hangzhou City, we apply the powerful multivariate analyses [25]. At present, there were very few studies comparing the freshwater in urban landscape areas. In this study, the freshwater analyzed in present study are shallow systems. Abiotic variables, such as primary nutrients, can be easily and repeatedly measured, which is useful in monitoring programs [29]. The values of TP, NH4-N, NO2-N in Xixi Wetland were almost higher than in West Lake during the whole year, that is probably due to more domestic sewage be discharged in Xixi Wetland and the influence of
fishery production. For the value of Chemical oxygen demand (COD), West Lake was higher than Xixi Wetland during the research period, indicating a more serious organic pollution or excessive organic matter decomposition. As the abiotic indices are sensitive to short-term changes in water quality, the seasonal pattern showed in Fig. 3 indicating rainy season may influence water physicochemical factors more or less. Relative to abiotic indices, biotic indices can tell more about longerterm conditions. Because of species assemblages exhibit the cumulative impacts of stressors on a habitat over time, biological data are preferred by investigators to use in monitoring water environment [29]. Similar domination of rotifers was observed in both collect stations (Fig. 2), and 14 rotifer species were the main contributors to between-group dissimilarity (Table 4). It has been suggested that the apparent dominance of rotifers maybe due to their relatively short generation times and rare to be preyed by fish which compared with the larger crustacean zooplankton [20,34]. The cluster analysis demonstrated that zooplankton communities distribution have significant seasonal variability (Fig. 4), the total Rotifer species number and abundance during four seasons in Xixi Wetland were higher than that in West Lake, while the diversity of microcrustacean didn't have significant difference in two survey areas, so Rotifer communities might have been the primary contributor leading to the difference between West Lake and Xixi Wetland. The dominant species, e.g., A. priodonta, P. trigla, Bosmina longirostris, Diaphanosoma brachyurum, Mesocyclops leuckarti as the indicators of the eutrophic status of water bodies were recorded both in the two
Fig. 2. The spatial-temporal variations in species abundance of three zooplankton groups in West Lake (a–c) and Xixi Wetland (d–e) during the study period.
S. Liu et al. / Acta Ecologica Sinica 36 (2016) 236–245
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Table 5 Summary of bio-environment (BIOENV) analysis showing the 10 best matches of environmental variables with temporal variations in zooplankton abundances in West Lake (W) and Xixi Wetland (X) in Hangzhou China during Jun. 2013 to May 2014. Rank
W
Chemical variable
X
P values 1 2 3 4 5 6 7 8 9 10
0.433 0.433 0.411 0.403 0.402 0.396 0.388 0.385 0.378 0.374
Chemical variable
P values NO3-N NO2-N, NO3-N TN, NO2-N, NO3-N TP, NO2-N, NO3-N TN, NO3-N TP, NO3-N NH4-N, NO2-N, NO3-N TP, TN, NO3-N TP, TN, NO2-N, NO3-N TN, NH4-N, NO2-N, NO3-N
0.587 0.587 0.585 0.582 0.581 0.574 0.571 0.567 0.566 0.562
pH, DO, T, COD pH, DO, T, COD, TP DO, T, COD DO, T, COD, TP pH, DO, T, COD, TN DO, T, COD, TP pH, DO, T, COD, NO2-N DO, T, COD, TP, TN DO, T, COD, TP, NO2-N DO, T, COD, NO2-N
P value = Spearman correlation coefficient; T = Water temperature, DO = Dissolved oxygen, COD = Chemical oxygen demand, TN = Total nitrogen, TP = Total phosphorus, NH4-N = Ammonium nitrogen, NO3-N = Nitrate nitrogen, NO2-N = Nitrite nitrogen.
areas [7,9,15]. Other indicator species, such as Brachionus angularis, K. cochlearis, and Filinia longiseta were more abundant in Xixi Wetland [10], Ferdous and Muktadir [8] concluded the Cladocera species of Ceriodaphnia quadrangula as indicators of the eutrophic status of water bodies, in our study, it was found to be present in Xixi Wetland but absent in West Lake. It is clear that although there was little difference between these two research areas about dominance species, but the zooplankton communities structure also had a significant difference.
dominant community, and 14 rotifer species were the main contributors to this dissimilarity. 3. All these results indicates that changes of conditions affecting the faunistic composition of the plankton occurred, so plankton should be preferred over others for early signals due to their low cost, less time consumption and ease of handling. 4. Comparative studies about urban landscape freshwater system in Hangzhou city will keep long-term research to provide reliable information for water quality monitoring.
5. Conclusions Acknowledgements 1. The physicochemical and zooplankton composition of the two water areas reveals that the water quality of Xixi wetland is better than Westlake, although it is also polluted by human activities. 2. A significant difference was found in zooplankton community structure between both wetland systems, and Rotifera assemblage as the
This work was supported by the Natural Science Foundation of China (project numbers: 31272262, 31071880 and 41076089). Zhejiang Key Scientific & Technological Innovation Team Project (2010R50039-20), and the Hangzhou Key Laboratory for Animal Adaptation and Evolution (20100333T05). I wish to thank Yong Jiang, Zhe Chen, Ping Zhang for
Fig. 3. Cluster analysis of physicochemical variable in the both areas during June 2013 to May 2014. (W, West Lake; X, Xixi Wetland; su, summer; au, autumn; wi, winter; sp, spring).
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Fig. 4. Cluster analysis of zooplankton community in the both areas during June 2013 to May 2014 (W, West Lake; X, Xixi Wetland; su, summer; au, autumn; wi, winter; sp., spring).
Fig. 5. Multidimensional scaling (MDS) ordination with cluster analysis for spatial patterns of zooplankton communities (a) and Principal component analysis (PCA) plot based on the annual average data of log-transformed abiotic and forth foot-transformed biotic in the twelve stations.
improving the manuscript and thank Cuicui Hou, Xiaowen Zhu for helping in sampling collection.
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