Ecological Indicators 114 (2020) 106282

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Evaluating ecological health in the middle-lower reaches of the Hanjiang T

River with cascade reservoirs using the Planktonic index of biotic integrity
(P-IBI)
Yingying Zhanga,b,c, Xuan Bana,c,d, , Enhua Lia,c,d, , Zhi Wanga,c,d, Fei Xiaoa,c,d
⁎ ⁎

a
Institute of Geodesy and Geophysics, Chinese Academy of Sciences, No.340 Xudong Rd., Wuhan 430077, China
b
University of Chinese Academy of Sciences, No. 19A Yuquan Rd., Beijing 100049, China
c
Key Laboratory of Monitoring and Estimate for Environment and Disaster of Hubei Province, Wuhan 430077, China
d
Honghu Lake Station for Wetland Ecosystem Research, Chinese Academy of Sciences, Honghu 433200, China

ARTICLE INFO ABSTRACT

Keywords: Operation of the middle route of the South-to-North Water Diversion Project in the Hanjiang River, China, has
Planktonic Index of Biotic Integrity (P-IBI) made the environmental health downstream of the Danjiangkou Reservoir an important issue for people living
Riverine ecological health along the river. This study used the Planktonic Index of Biotic Integrity (P-IBI) including phytoplankton and
Cascade reservoirs zooplankton to evaluate riverine ecological health in an area with cascade reservoirs. Plankton and water
Hanjiang River
samples from 19 sampling sites were collected along the middle-lower reaches of the Hanjiang River in Nov.
2017 and July 2018. To further verify the reliability of the P-IBI results, they were compared with the Saprobic
Index (SI) and Comprehensive Water Quality Identification Index (CWQII). Redundancy analysis (RDA) was used
to evaluate correlations and variability between P-IBI, SI, CWQII, candidate metrics, and primary environmental
factors in the dry and wet seasons. The results showed that the ecological health of the aquatic ecosystem was
‘fair’ in status, oligotrophic, and class II (wet season)-class III (dry season) as evaluated by the IBI, SI, and CWQII,
respectively. The ecosystem during the wet season was in better health than that in the dry season: based on
CWQII, water quality at 63% of sites was in class III during the dry season, while 79% of sites were in class II in
the wet season; and 11% more sites had IBI-A values (the mean values of Phyto-IBI and Z-IBI) less than 3 IBI
scores (indicating “fair” status) in the dry season compared to the wet season. Ecological conditions were also
poorer in the reservoir backwater area. The main driving forces impacting aquatic ecosystem in the study area
were pollutant emissions and dam impacts. This study demonstrated that the P-IBI is a potential tool for eval-
uating riverine ecological health in areas with cascade reservoirs.

1. Introduction producer in the biological chain and has the most sensitive response to
changes in the river environment (Jakhar, 2013). Zooplankton occupies
Inter-basin water transportation and dam construction can control an intermediate position in the food web and is a considerable nutrient
floods, increase power-generating capacity, improve water efficiency, resource for waterfowl and fish; it is also sensitive to environmental
and play an important role in irrigation and river navigation, thus changes and is an important bioindicator (Sládeček, 1983; Whitfield
providing various possibilities for regional development (Gupta and van and Elliott, 2005). Biotic integrity is a multi-level indicator that com-
der Zaag, 2008; Moran et al., 2018). At the same time, they also have bines many biological indicators to measure and communicate biolo-
significant impacts on water temperatures, hydrological regimes, water gical status, reflecting the ecological health status of rivers and basins
quality, environmental geology, aquatic life, terrestrial organisms, (Karr and Chu, 2000). Biological criteria are widely used in ecological
landscapes, and heritage (Wang et al., 2012). When river systems health assessments due to their ability to integrate the impacts of
change from pristine to dam-reservoir-river status, the composition and measured and unmeasured factors, providing a better evaluation of
abundance of phytoplankton assemblages appear to be sensitive in- environmental conditions than water chemistry alone. With the clear
dicators of ecosystem health due to the significant alterations of habitat management need for biological assessments (EC (European
and hydrological regimes (Li et al., 2013a, b). Phytoplankton acts as a Communities), 2000), Indices of Biotic Integrity (IBI) based on fish,

⁎
Corresponding authors at: Institute of Geodesy and Geophysics, Chinese Academy of Sciences, No.340 Xudong Rd., Wuhan 430077, Hubei, China.
E-mail addresses: banxuan@whigg.ac.cn (X. Ban), lieh@whigg.ac.cn (E. Li).

https://doi.org/10.1016/j.ecolind.2020.106282
Received 12 April 2019; Received in revised form 26 February 2020; Accepted 3 March 2020
Available online 14 March 2020
1470-160X/ © 2020 Elsevier Ltd. All rights reserved.
Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

benthic invertebrates, and diatoms have become the most widely used the Data Center for Resources and Environmental Sciences, Chinese
management tool for evaluating the health of aquatic systems (Gibson Academy of Sciences (RESDC) (http://www.resdc.cn). In this study, 19
et al., 2000; Maulood et al., 2011; Jungwirth et al., 2000; Wang et al., sampling sites were selected from the area downstream of the Dan-
2005). Recently, phytoplankton-based IBI (Phyto-IBI) and zooplankton- jiangkou Reservoir as shown in Fig. 1.
based IBI (Z-IBI) have been used to assess the health of relatively stable
lake and bay ecosystems (Carpenter et al., 2006; Lacouture et al., 2006; 2.2. Sampling and laboratory analysis
Kane et al., 2009; Maulood et al., 2011; Baek et al., 2014; Johnson and
Buchanan, 2014), but are less used for studying riverine ecosystems Plankton and water samples from 19 sampling sites (Fig. 1) were
(Teng et al., 2014; Ma, 2015). In addition, river health affected by dams collected along the middle-lower reaches of the Hanjiang River in Nov.
and reservoirs has rarely been evaluated by Phyto-IBI (Wu et al., 2012a; 2017 and July 2018. Referring to the standards for plankton collection
Li et al., 2013a, b), and studies of the impacts of the dams on riverine and analysis by the Ministries of Agriculture and Water Resources of the
zooplankton are limited (Zhou et al., 2008). It is therefore necessary to People’s Republic of China (MAPRC, 2007; MWRPRC, 2014) and the
develop a Planktonic Index of Biotic Integrity (P-IBI) that includes both relevant literatures (Wang et al., 1993; SEPA, 2002b; Hu and Wei,
phytoplankton and zooplankton to evaluate the ecological health of 2006), the procedures for plankton collection were as follows: (1)
dam-reservoir-river systems (Pomari et al., 2018; Pomari et al., 2019). plankton nets of 64 um mesh size and 112 um mesh size were dragged
The Hanjiang River is the largest tributary of Yangtze River in China slowly in an ‘∞’ shape from the water surface to a depth of 0.5 m and
(Deng et al., 2015). Seven consecutive dams will be built along middle- then the filtrates from different mesh were placed into 50 mL plastic
lower reaches of the Hanjiang River, with the exception of a 40 km long bottles and covered for qualitative analysis; (2) two parallel water
river section between the Nianpanshan and Xinglong hubs (Li et al., samples with a 20 L bucket were collected from the water surface to a
2013a, b). When all seven dams are completed, the natural riverine depth of 0.5 m and mixed thoroughly at each site; (3) a plankton net of
habitats will be replaced by reservoir-lacustrine environments. Several 64 um mesh size was used to filter one mixed 20 L water sample and
studies have been conducted to assess the effects of the Danjiangkou 0.5 mL Lugol’s iodine solution was added to fix the filtered fluid in a
Dam and cascade reservoirs on hydrological regimes (Wang et al., 2015, 50 mL vial for determination of cladocera and copepods; (4) one liter of
Lu et al., 2018a, Song et al., 2018), the evolution of mid-channel bars another mixed sample was removed and preserved with 1.5% Lugol’s
(Xu, 1997a, b), changes in water quality (Liu and Yu, 1992; Wang et al., iodine solution, which was then concentrated to 50 mL for phyto-
2016), algal blooms (Yang et al., 2012; Li et al., 2013a, b), and mi- plankton, Protozoa, and rotifer samples after being settled for 48 h
gration processes and relationships between water and sediment (Xu, based on the concentrated water sample method.
1997a, b; Zhang et al., 2017; Lu et al., 2018b). Moreover, algal blooms Samples for zooplankton (primarily crustaceans) analysis were
occurred more than 11 times from 1992 to 2018, and the maximum studied under a compound microscope and specimens were identified
algal density showed an increasing trend from 1992 to 2000 (Cheng at the species level when possible (Jiang and Du, 1979; Shen, 1979).
et al., 2019). However, none of these studies have systematically Zooplankton quantity was expressed as the number of organisms per
documented the impacts of cascade dam construction on the composi- cubic meter. The concentrated phytoplankton samples were taken to
tion and abundance of plankton assemblages; those that have been the laboratory for identification and microscopic analysis (magnifica-
conducted were limited to some river sections and the Danjiangkou tion 400×). Phytoplankton, protozoa and rotifers were identified at the
Reservoir (Yin et al., 2011). In addition, no study has been conducted species and genus levels following the methods recommended by re-
with the aim of developing a P-IBI to assess aquatic ecosystem health in ference books (Hu and Wei, 2006; Wen and Xu, 2010; Wang, 1961;
the heavily dammed middle-lower reaches of the Hanjiang River. The Shen et al., 1990). A 0.1 mL plankton counting chamber was used to
goals of this study are as follows: (1) to investigate differences in the count the abundance of phytoplankton, which was expressed as cell/L
composition and abundance of hydropower dam-affected and un- (Wu et al., 2012b; Niu et al., 2015). Each sample from each section was
affected plankton assemblages; (2) to develop a feasible Planktonic counted twice and the mean value of the two numbers was selected as
Index of Biotic Integrity and assess the health of aquatic ecosystems in the result.
the dry and wet seasons; (3) to assess the feasibility of the P-IBI; (4) to Water samples were collected in sulfuric acid-washed (pH < 2)
analyze driving factors behind aquatic health in different sections of the plastic bottles for water quality analysis, and were immersed at least
river. 20 cm below the water surface (if the depth allowed) to eliminate the
air. There were three water bottles for each site. One was preserved by
2. Materials and methods adding sulfuric acid (analytical grade) at pH < 2, and all of them were
stored at 4 °C (to minimize deterioration prior to chemical analysis) for
2.1. Study area and sampling sites analysis of physicochemical concentrations. Concurrently, instream
parameters including pH, optically dissolved oxygen (ODO), con-
As the largest tributary of the Yangtze River, the Hanjiang River has ductivity (COND), oxide reduction potential (ORP), and water tem-
a length of 1570 km, an average annual temperature of 15–17 °C, and perature (WT) were measured in situ by EXO sonde (EXO2) (YSI
an annual precipitation ranges from approximately 700 mm to Incorporated, a Xylem brand, USA). For each water sample, quality
1,200 mm (Wang et al., 2015; Wang et al., 2016). The Danjiangkou parameters such as total nitrogen (TN), ammoniacal nitrogen (NH3-N),
Reservoir is located in Xichuan County (Henan Province) and Dan- nitrate-nitrogen (NO3-N), nitrite-nitrogen (NO2-N), total phosphorus
jiangkou City (Hubei Province). The middle reaches of the Hanjiang (TP), chemical oxygen demand (COD), five-day biochemical oxygen
River span from Danjiangkou Dam to Huangzhuang Gauge in Zhong- demand (BOD5), chlorophyll a (Chl-a), and total organic carbon (TOC)
xiang City, and below the Huangzhuang is the downstream area; the were analyzed. All analyses were carried out according to the standard
total area of the middle-lower reaches of the Hanjiang River Basin is methods (SEPA, 2002b), and the hydrochemical concentrations of
approximately 63,800 km2 (Song et al., 2018). The Danjiangkou Re- samplings are shown in Table 2.
servoir was completed in 1974 and the middle route of South-to-North
Water Diversion Project commenced water transfer in December 2014. 2.3. Site classification
Six cascade reservoirs (Wangfuzhou, Xinji, Cuijiaying, Yakou, Nian-
panshan, and Xinglong) are downstream of the Danjiangkou Reservoir. The reference conditions standards were based on the identification
The Wangfuzhou, Cuijiaying, and Xinglong Reservoirs are currently of minimally disturbed land use sites that represented the best physical,
operating and other reservoirs are under construction (Table 1). Land chemical, and biological conditions (Qadir and Malik, 2009; Li et al.,
use and land cover data from 2015 for the study area were provided by 2010; Li et al., 2018; Arman et al., 2019). First, we considered sites as

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Table 1
Information on the cascade reservoirs in the middle-lower reaches of the Hanjiang River.
Reservoir Normal water level (m) Distance from Danjiangkou (km) Regulation ability Normal capacity (million m3) Year constructed

Danjiangkou 157.0 0 Year 17,450 1973

Danjiangkou 170.0 0 Multiyear 29,050 2013
Wangfuzhou 86.2 30.0 Danjiangkou reservoir reverse regulation 149.5 2000
Xinji 76.2 89.7 Day 301.2 Under construction
Cuijiaying 62.7 134.0 Day 245.0 2010
Yakou 55.2 201.0 Day 608.0 Under construction
Nianpanshan 49.2 263.0 – 877.0 Under construction
Xinglong 36.2 378.0 – 273.0 2013

Fig. 1. Sampling sites (sites 1–11 are in the middle reach; sites 12–19 are in the lower reach), reservoirs (A, Danjiangkou; B, Wangfuzhou; C, Xinji; D, Cuijiaying; E,
Yakou; F, Nianpanshan; G, Xinglong) in the middle-lower reaches of the Hanjiang River, and land use and land cover for the basin.

“reference quality” where the rivers had good riparian vegetation, there water quality grade was lower than class III and located in an area with
were no towns or human communities along the river bank, no gravel- high human disturbance was selected as an impaired site.
mining activity or hydrologic modification in the watershed, and no
wastewater treatment discharge (Morley and Karr, 2002). Second, to 2.4. P-IBI development
select reference sites with better water quality (Buchanan et al., 2005),
the surface water quality was divided into five grades according to the Based on the literatures (Nygaard, 1949; Shannon and Weaver,
“Environment Quality Standards for Surface Water (GB3838-2002)” of 1949; Margalef, 1958; Palmer, 1969; Pielou, 1975; Gannon and
China (SEPA, 2002a) (Table A1). According to the study area conditions Stemberger, 1978; Sládeček, 1983; Pace, 1986; Ludwig and Reynolds,
and research by Zhou et al. (Zhou et al., 2013), we selected the sites 1988; Zhang and He, 1991; Lampitt et al., 1993; Havens, 1998; Wu,
with higher vegetation cover, lower human activities, and better water 1999; Hu and Wei, 2006; Kane et al., 2009; Tan et al., 2017), a large
quality as the final reference sites. A site where the seasonally averaged pool of attributes (Table A2) were selected as candidate metrics for

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Table 2 protection targets for each grade of CWQII are shown in Table A4.
The concentration of hydrochemical parameters at reference and impaired sites Trend analyses for IBI-A, CWQII, and SI values from upstream to
in the middle-lower reaches of the Hanjiang River (the mean ± standard de- downstream in the Hanjiang River were obtained using the ggplot2
viation value of different classfied sampling sites (the more information about package of R version 3.6.1.
impaired and reference sites can find in “2.3” and “3.2” section)).
Procedure reports for the dry and wet seasons indicated that the
Impaired sites Reference sites response data were compositional and had gradient lengths less than 3
SD (standard deviation) units long, so a liner redundancy analysis
Indicators Nov. 2017 July 2018 Nov. 2017 July 2018
(RDA) method was recommended for this type of study (Petr Šmilauer,
(mg/L)
2014). RDA as a multivariate ordination technique for direct gradient
TN 2.14 ± 0.87 2.52 ± 0.86 1.49 ± 0.07 1.82 ± 0.03 analysis, and was chosen to evaluate correlations and variability among
TP 0.18 ± 0.07 0.08 ± 0.05 0.09 ± 0.00 0.03 ± 0.00 P-IBI, SI, CWQII, and other selected metrics for IBI (Table A5) with
NH3-N 0.14 ± 0.05 0.19 ± 0.07 0.17 ± 0.01 0.11 ± 0.07
primary environmental factors in the dry and wet seasons. RDA was
NO3-N 1.89 ± 0.75 0.92 ± 0.26 1.24 ± 0.01 0.74 ± 0.03
NO2-N 0.04 ± 0.04 0.29 ± 0.34 0.01 ± 0.00 0.13 ± 0.11
conducted using Canoco 5.0. Log transformation Y = log (y + 1) was
COD 18.7 ± 11.15 10.88 ± 5.36 11.95 ± 6.85 9.65 ± 3.55 performed during the analysis. P-IBI and its metrics were set as passive
BOD5 2.17 ± 1.07 3.33 ± 3.30 1.50 ± 0.50 3.00 ± 0.00 variables to explore their relationships with environmental variables
Chl-a 5.24 ± 2.88 32.98 ± 35.99 1.39 ± 0.37 27.3 ± 0.00 and phytoplankton assemblages.
TOC 3.88 ± 0.73 4.86 ± 1.35 3.25 ± 0.05 3.5 ± 0.47

3. Results
Phyto-IBI, along with 15 metrics (Table A3) for Z-IBI that were relevant
to assessing anthropogenic impacts on plankton communities. All can- 3.1. Plankton composition and abundance
didate metrics were classified into four categories: biomass, abundance,
diversity, and trophic status. Selected metrics for the development of The diatom species made up the largest proportion (40% in the dry
the P-IBI were chosen by the following step-wise screening procedures: season, 38.34% in the wet season), followed by chlorophyta (33.08% in
(1) Discrimination power test: the metric with a lower separation power the dry season, 37.15% in the wet season), and chrysophyta (14.62% in
between the reference and impaired groups (interquartile ranges the dry season, 13.83% in the wet season). A total of 291 species of
overlapped the degree between boxes (IQ), IQ < 2) was eliminated phytoplankton belonging to 118 genera and seven phyla were identified
(Barbour et al., 1996; Wu et al., 2012a). (2) Redundancy test: Pearson with abundances ranging from 3.2 × 104 to 8.48 × 107 cell/L, and
correlation coefficients (|r| ≤ 0.9) for the selected metrics were re- Shannon-Wiener diversity index values ranging from 0.07 to 2.95. The
tained to avoid redundancy. (3) Variability analysis: metrics with lower zooplankton community was represented by four groups: protozoa,
coefficients of variation (CV) were retained due to high deviations of rotifer, cladocera, and copepod. Rotifer made up the largest proportion
metrics with CV > 1 (Wang et al., 2005). (42.61% in the dry season, 53.24% in the wet season) and protozoa
The IBI scores, which were calculated as the mean values of selected were next (28.7% in the dry season, 23.74% in the wet season). A total
metrics, were used to classify aquatic ecosystem health into five levels: of 170 species of zooplankton belonging to 100 genera were identified
0–1 (bad), 1–2 (poor), 2–3 (fair), 3–4 (good), and 4–5 (excellent). When with abundances ranging from 20.3 to 1.63 × 104 cell/L and Shannon-
the correlation between candidate metric and the pristine aquatic en- Wiener diversity index values ranging from 0.39 to 2.75. Variability in
vironment was positive (Tables A2 and A3), the assigned scores were 1, plankton abundance for each section in the dry and wet seasons is
2, 3, 4, and 5 for the < 25th, 25–50th, 50–75th, 75–90th, > 90th per- shown in Fig. 2.
centiles, respectively. Otherwise, the scores were in reverse order (EC In general, average phytoplankton abundance in the dry season was
(European Communities), 2000; Wu et al., 2012b; Li et al., 2013a, b). lower than in the wet season, and the average zooplankton abundance
Therefore, the final IBI scores (Phyto-IBI, Z-IBI) were calculated for the in the dry season was higher than in the wet season. However, total
19 sampling sites based on quantitative assessments of variability in the phytoplankton and zooplankton abundance had essentially the same
aquatic system upstream and downstream of the cascade reservoirs. The trends. Plankton had consistently high values in the wet and dry sea-
IBI-A value was the mean of Phyto-IBI and Z-IBI by season, and re- sons at sites 7 and 13 (Site 7 was at the Tangbai River tributary of the
presented the overall P-IBI for different seasons. Hanjiang River, about 1.5 km from the Tangbai River estuary; site 13
was located at the artificial main canal of the Hanjiang River water
supply project where water was diverted from the Yangtze River, about
2.5. Data analysis 4 km from the Hanjiang River). Plankton abundance was also greater
closer to the lower reaches of the Hanjiang River, especially for
The Shannon-Wiener diversity index, Margalef richness index, and
Pielou evenness index for phytoplankton and zooplankton were calcu-
lated using a free trial version PRIMER v7. To test the performance of
the proposed P-IBI, the results were compared with the Saprobic Index
(SI) and the Comprehensive Water Quality Identification Index
(CWQII). The Saprobic Index (SI) method proposed by Pantle and
Harald (1955) includes both zooplankton and phytoplankton (Pantle
and Harald, 1955), and classified pollution into four levels (Eduardo
et al., 2016): 1.0–1.5 (oligotrophic, negligible pollution), 1.5–2.5 (β-
mesotrophic, moderate pollution), 2.5–3.5 (α-mesotrophic, high pol-
lution), and 3.5–4.0 (eutrophic, excessive pollution). The CWQII
method proposed by Xu (Xu, 2005) was also combined with the na-
tional standard (SEPA, 2002a), and the corresponding water quality
classes for CWQII were as follows: (1.0–2.0, class Ⅰ), (2.0–3.0, class II),
(3.0–4.0, class III), (4.0–5.0, class Ⅳ), (5.0–6.0, class Ⅴ), (6.0+, Worse
than class Ⅴ). CWQII values were calculated based on indicators of TN,
TP, NH3-N, BOD5 and COD in this paper (Miao et al., 2009; Ban et al., Fig. 2. Plankton abundance at each site in the dry and wet seasons (P.A.,
2014), and the detailed environmental functions of surface water and abundance of phytoplankton; Z.A., abundance of zooplankton).

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Fig. 3. Box-plots of 15 candidate metrics between the reference and impaired sites in the dry season (M1, total phytoplankton biomass, M2, total phytoplankton
abundance, M4, chlorophyta abundance, M6, % total abundance composed of cyanophyta, M8, % total abundance composed of bacillariophyte, M9, % total
abundance composed of dominant species, M10, % total abundance composed of cyanophyta and chlorophyta, M11, % total abundance composed of bacillariophyte
and chlorophyta, M12, phytoplankton species number, M13, bacillariophyte species number, M14, Margalef index, M15, Shannon-Wiener index, M16, Simpson’s
diversity (1-λ), M18, diatom quotient, M20, generic diatom index).

zooplankton during the dry season, while plankton at site 3 was af- positively correlated with characteristics of a pristine aquatic environ-
fected by backwater from the Wangfuzhou hydropower station and had ment in the dry season, so the assigned scores were 1, 2, 3, 4, and 5
high values during the wet season (Fig. 2). according to the < 25th, 25–50th, 50–75th, 75–90th, > 90th percen-
tiles of weighted mean values, respectively. On the contrary, the more
negative with aquatic environment becomes, the higher value of the
3.2. Establishment of P-IBI and multimeric index validation
selected metrics (M9, M20) is, so score assignments were 5, 4, 3, 2, and
1. The final Phyto-IBI score in the dry season was the mean of all eight
As shown in Fig. 1, sites 1–6 were in high vegetation coverage areas,
selected metrics (Table 3). Qualifying Z-IBI metrics were kept in the dry
and sites of 1, 3, 8, and 12 were in the backwaters of Danjiangkou,
season following the same screening procedures (Table A5), and the Z-
Wangfuzhou, Cuijiaying, and Xinglong Reservoirs, respectively. Only
IBI was the average score of the selected metrics. Phyto-IBI and Z-IBI
sites 2, 4, 5 and 6 had higher vegetation cover of the selected reference
scores in the wet season were calculated in the same way.
sites. In addition, sampling sites 4 and 5 were in the tributary estuaries.
The IBI-A value was the average of Phyto-IBI and Z-IBI per season,
Sites 1, 7, 8, 12, 14, and 18 were in areas with high human disturbance
and represented the overall P-IBI in different seasons. The metrics se-
and low vegetation coverage, with poor water quality. Therefore,
lected for final IBI represented different aspects of plankton assem-
sampling sites 2 and 6 were selected as reference sites and sites 1, 7, 8,
blages and were significantly correlated with several environmental
12, 14, and 18 were impaired sites. Table 2 shows that the selected
variables. All candidate metrics were highly correlated with environ-
reference and impaired sites were reasonable, with higher water quality
mental variables in the dry season, except for M12 (Phytoplankton
in reference sites and lower water quality in impaired sites.
species number) and M_z7 (% total abundance composed of rotifer)
Taking the Phyto-IBI metrics for Nov. 2017 as an example, the
(Table A6); in the wet season, all candidate metrics except from M_z7
screening process for each step was as follows. First, 15 metrics were
and M_z8 (% total abundance composed of cladocera and copepod)
selected from 20 candidate metrics (Fig. 3), of which five (M3, M5, M7,
were highly correlated with environmental variables (Table A7).
M17, and M19) were eliminated because of their lower separation
power (IQ < 2) between the reference and impaired sites. Next, M2,
M10, M16, and M18 were rejected because they were highly redundant 3.3. Results for the study area
(|r| ≥ 0.90). Then, we eliminated M1, M4, and M6 with higher
variability (CV > 1). Final Phyto-IBI scores were calculated by the 3.3.1. Temporal and spatial variability of P-IBI
eight metrics (M8, M11, M12, M13, M14, M15) whose values were Spatially, we found that the scores for sampling sites 2, 3, 4, 6, 9, 17,

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Table 3
Eight component metrics for Phyto-IBI with corresponding scores.
Abbreviation Selected multi-metrics Assigned scores

5 (best) 4 3 2 1 (worst)

M8 % total abundance composed of bacillariophyte > 0.94 0.81–0.94 0.72–0.81 0.63–0.72 < 0.63
M9 % total abundance composed of dominant species < 0.29 0.29–0.52 0.52–0.69 0.69–0.86 > 0.86
M11 % total abundance of bacillariophyte and chlorophyta > 0.97 0.94–0.97 0.87–0.94 0.78–0.87 < 0.78
M12 Phytoplankton species number > 48.6 43–48.6 36–43 29.5–36 < 29.5
M13 Bacillariophyte species number > 25.4 22.5–25.4 18–22.5 15.5–18 < 15.5
M14 Margalef index > 8.43 6.52–8.43 5.95–6.52 4.26–5.95 < 4.26
M15 Shannon-Wiener index > 2.58 2.29–2.58 2.29–2.17 1.82–2.17 < 1.82
M20 Palmer algal genus pollution index < 10.5 10.5–16 16–18.5 18.5–24 > 24

18, and 19 were greater than 3 in the dry season. In the wet season, wet season were less than 3. Based on Z-IBI (Fig. 4), 53% of sites in the
scores for sites 4, 5, 9, 16, 17, 18, and 19 were greater than 3, and sites dry season and 47% of sites in the wet season were less than 3, so
6 and 8 were greater than 4 (Fig. 4(a)). This implied that the aquatic aquatic ecosystem health in the middle-lower reaches of the Hanjiang
ecosystem for 42% of sites were in ‘good’ status in the dry season and River was ‘fair’ overall. In addition, a slightly higher percentage of ‘fair’
more than 37% of sites in wet season were in ‘good’ status according to sites in the dry season showed that the state of the aquatic ecosystem in
the Phyto-IBI. In Fig. 4(b), Z-IBI scores for sites 1, 3, 6, 7, 8, 9, 11, 12, the wet season was better than in the dry season. We also observe from
and 17 were greater than 3 in the dry season. In the wet season, sites 3, Fig. 4(a) that aquatic health in the middle reaches was better than the
6, 8, 11, 12, 13, 16, 17, and 18 were greater than 3, and site 2 was 4. lower reaches. Mean site scores in both the middle and lower reaches
This showed that the aquatic ecosystem for 47% of sites were in ‘good’ based on Phyto-IBI in the wet season were better than in the dry season.
status in the dry season and more than 47% of sites in the wet season However, the mean score in the middle reaches in the wet season was
were in ‘good’ status. lower than the dry season score. In addition, mean Phyto-IBI scores at
The scores for 58% of sites in the dry season and 53% of sites in the all sampling sites in the wet season were higher than in the dry season,
reflecting a healthier aquatic ecosystem in the wet season, but mean
scores of Z-IBI in the wet season were lower than in the dry season.
Therefore, simply comparing Phyto-IBI and Z-IBI scores across different
hydrological periods could not identify which season had healthier
aquatic ecosystems. Using the mean values of Phyto-IBI and Z-IBI (IBI-
A) better displayed this change trend.
As can be seen in the graph (Fig. 5), the linear fit of IBI-A decreased
slightly in Nov. with no significant spatial change (P = 0.24), while the
linear fit increased non-significantly (P = 0.82) in July. Lower IBI-A
values downstream reflected a poorer aquatic ecosystem in the dry
season. We also observed that the aquatic ecosystem in the wet season
was healthier than in the dry season for 47% of sampling sites (2, 4, 6,
8, 9, 16, 17, 18 and 19) had IBI-A values greater than 3 in July, only
37% of sampling sites (2, 3, 6, 7, 8, 9, 17) were in ‘good’ condition in
the dry season. The longitudinal spatial distribution of ecological health
status (Fig. 6) showed that 74% of sites had mean IBI-A scores in the dry
and wet seasons between 2 and 3, implying that the aquatic ecosystem
overall was ‘fair’ in the middle-lower reaches of the Hanjiang River.

3.3.2. Comparison with SI and CWQII

It can be seen that water quality was better in the wet season than in
the dry season (Fig. 7), as 63% of sites (6, 7, 8, 9, 10, 12, 13, 14, 15, 16,
18, and 19) had CWQII values greater than 3 in the dry season (refer-
ring to class III water quality from Table A4), but only 21% (7, 12, 14,
and 19) of sites were greater than 3 in the wet season and 79% were
lower; and tended to deteriorate from upstream to downstream, as the
CWQII linear fit gently increased (slope = 0.03, P = 0.03 < 0.05;
slope = 0.05, P = 0.01 < 0.05) in the dry and wet seasons, respec-
tively. Obviously, the fact that the water quality in the dry season was
worse than in the wet season was similar to the IBI-A result where 11%
more sites scored less than three in the dry season than in the wet
season. SI was less than 1.5 at most sites in the dry and wet seasons,
which meant that the water was oligotrophic. Poorer water quality with
high CWQII values generally had high SI values (Fig. 7), and the SI
trend from upstream to downstream was not significant (P > 0.05).
Fig. 4. Phyto-IBI and Z-IBI scores along the middle-lower reaches of the Simply speaking, the ecological health of the aquatic ecosystem was in
Hanjiang River (M, the average of sites 1–11 in the middle reaches; L, the ‘fair’ status, oligotrophic, and class II (wet season)-class III (dry season)
average of sites 12–19 in the lower reaches; O, the average of all sampling sites; as evaluated by IBI, SI, and CWQII, respectively. Compared with
Reference sites 2 and 6 where IBI scores were relatively high). aquatic ecosystem state as indicated by CWQII and IBI, mean values of

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Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

SI were all below 1.5, which overestimated the oligotrophic status and
inaccurately reflected the overall health of this dammed aquatic en-
vironment.

3.4. Assessing the feasibility of the P-IBI

The 10 environmental variables used in the dry season explained

63.95% of the variability with the first four axes being significant
(P = 0.046 < 0.05, 999 Monte Carlo permutations). In terms of the
correlation of physicochemical variables, the variance of the first axis
was associated with NH3-N and Chl-a and represented 38.7% of the
variance of IBI, CWQII, SI, and other selected metrics. RDA axis 2 ex-
plained 12.1% of the variance indicated by TOC (Fig. 8). In the wet
season, seven environmental variables explained 63.47% with the first
four axes being significant (P = 0.03 < 0.05, 999 Monte Carlo per-
mutations). In terms of the physicochemical variable correlations, the
variance of the first axis was associated with ODO, pH, TN, NO3-N, and
represented 51.6% of the variance of IBI, CWQII, SI, and other selected
metrics. RDA axis 2 explained 8.6% of the variance indicated by WT,
Chl-a and TOC (Fig. 9). Generally, the final IBI scores and metrics were
indicative of ecological status, as indicated by the RDA results (Figs. 8
and 9).

4. Discussion

4.1. Development and evaluation of the P-IBI Fig. 6. Spatial distribution of aquatic ecosystem health based on IBI-A of season
mean (the average of Phyto-IBI and Z-IBI).
In the development of the IBI, the selection of reference sites was a
critical step. In this study, the middle-lower reaches of the Hanjiang The P-IBI we established was able to discriminate between impaired
River had a high level of water resources development in the Jianghan and reference site groups as Fig. 10 shows. The state of aquatic eco-
Plain area with large population density and abundant agriculture. system was evaluated using P-IBI in the middle and lower reaches of
Therefore, it was nearly impossible to select reference sites that were Hanjiang River. In addition, the state of aquatic ecosystem evaluated by
completely pristine and free from human disturbance. Instead, we se- CWQII was consistent with the IBI, reflecting better aquatic health
lected sites that had better water quality and were not affected by status in the wet season than in the dry season. Moreover, all candidate
backwater from the dam, with fewer surrounding urban areas and high metrics except for M12, M_z7, and M_z8 were highly correlated with
vegetation coverage. To retain as much plankton community informa- environmental variables (Tables A6 and A7). However, there were not
tion as possible, we constructed multiple candidate metrics that would significant correlations between the IBI and most of the physicochem-
reflect the biotic and ecological conditions throughout the Hanjiang ical indices. In the dry season, Z-IBI was negatively correlated with pH
River.

Fig. 5. IBI-A scores (the average of Phyto-IBI and Z-IBI) in the dry and wet seasons (the grey range is the 95% confidence interval).

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Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

Fig. 7. CWQII and SI values in the dry and wet seasons (the grey range is the 95% confidence interval).

Fig. 8. Redundancy analysis of the relationships between environmental

parameters, the component metrics, and IBI scores in the dry season (Phyto-IBI
(Phytoplankton-Index of Biotic Integrity), Z-IBI (Zooplankton-Index of Biotic
Integrity), IBI-A (Mean values of Phyto-IBI and Z-IBI), CWQII (Comprehensive
Water Quality Identification Index, SI (Saprobic Index); M8, % total abundance
composed of bacillariophyte, M9, % total abundance composed of dominant Fig. 9. Redundancy analysis of the relationships between environmental
species, M11, % total abundance composed of bacillariophyte and chlorophyta, parameters, the component metrics, and IBI scores in the wet season (Phyto-IBI
M12, Phytoplankton species number, M13, Bacillariophyte species number, (Phytoplankton-Index of Biotic Integrity), Z-IBI (Zooplankton-Index of Biotic
M14, Phytoplankton Margalef index, M15, Phytoplankton Shannon-Wiener Integrity), IBI-A (Mean values of Phyto-IBI and Z-IBI), CWQII (Comprehensive
index, M20, Palmer algal genus pollution index; M_z7, % total abundance Water Quality Identification Index, SI (Saprobic Index); M10, % total abun-
composed of rotifer, M_z8, % total abundance composed of cladocera and co- dance composed of cyanophyta and chlorophyta, M11, % total abundance
pepod, M_z9, Zooplankton species number, M_z12, Zooplankton Shannon- composed of bacillariophyte and chlorohyta, M13, Bacillariophyte species
Wiener index, M_z13, Zooplankton Simpson’s diversity (1-λ); total nitrogen number, M15, Shannon-Wiener index, M20, Palmer algal genus pollution index;
(TN), ammoniacal nitrogen (NH3-N), nitrate-nitrogen (NO3-N), nitrite-nitrogen M_z6, Copepod abundance, M_z7, % total abundance composed of rotifer, M_z8,
(NO2-N), total phosphorus (TP), chemical oxygen demand (COD), five-day % total abundance composed of cladocera and copepod, M_z11,
biochemical oxygen demand (BOD5), chlorophyll a (Chl-a), and total organic ZooplanktonMargalef index; total nitrogen (TN), nitrate-nitrogen (NO3-N),
carbon (TOC)). chlorophyll a (Chl-a), and total organic carbon (TOC), optically dissolved
oxygen (ODO), and water temperature (WT)).

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Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

indicators (Wang, 2007). Therefore, the multimeric P-IBI system was

selected over the univariate SI assessment. Overall, more than 50% of
IBI-A values in each season were less than 3, indicating a ‘fair’ state of
the aquatic ecosystem in the middle and lower reaches of Hanjiang
River. This was consistent with seasonal water quality variability,
which was poorer in the dry season: more ‘fair’ sites were indicated by
both Phyto-IBI and the Z-IBI in the dry season. The reasons for the poor
health in the lower reaches during the dry season may be inseparable
from the large increase in pollution along both sides of the river (Jing
et al., 2019). In addition, if the Yangtze River water level is high during
the dry season, it slows the flow rate of the Hanchuan reaches in the
lower part of Hanjiang River (Wu et al., 2005, Qu et al., 2014), which is
conducive to the growth and reproduction of phytoplankton and the
formation of blooms. The health of the middle reaches was worse than
that the lower reaches during the flood season due to the reservoir
backwater influence. In addition, the Danjiangkou Reservoir was in a
Fig. 10. IBI scores of reference sites and impaired sites. sluicing period during sampling and the lower reaches were only af-
fected by Xinglong Reservoir backwater, not altered with the water
(r = −0.52, P < 0.05), and the final Phyto-IBI was strongly negatively level changes in the Yangtze River.
correlated with pH (r = 0. 64, P < 0.01) and WT (r = −0.54, In the long-term, water quality in the middle-lower reaches of the
P < 0.05) in the wet season (Tables A6 and A7). This may have been Hanjiang River deteriorated annually. From the perspective of seasonal
related to the range of phytoplankton activities, growth cycles, and so variability, point source pollution is a problem during the dry season,
on. The monitoring results only represented sampling sites over a short and non-point source pollution is a problem during the flood season.
time and did not reflect long-term aquatic ecosystems health. Our study Spatially, the water quality was poor in the Xiantao and Wuhan sections
in July 2018 coincided with the discharge of water from the Dan- of the lower reaches. It was better at Danjiangkou Reservoir and in the
jiangkou Reservoir. Water was initially released on June 13, 2018 for a main stream of the middle reaches, but was also seriously polluted in
total of five days to maintain the river flow rate, flush the riverbed, and most tributaries, and most severely polluted in the Tangbai River, a
maintain human water use requirements. On July 4, 2018, the Dan- tributary of the Hanjiang River (Zeng, 2005; Li et al., 2013a, b, Jing
jiangkou Reservoir discharged water again (http://www.10yan.com/ et al., 2019). This was consistent with the results of our study of phy-
2018/0613/552031.shtml). This led to unstable plankton levels and a toplankton abundance and spatial distribution (Fig. 2), and the mean
lag in plankton response to the aquatic environment. The feeding be- Phyto-IBI scores for sites in the middle reaches (M) were higher than in
havior and habits of zooplankton were different, and zooplankton likely the lower reaches (O) in both seasons (Fig. 4(a)). However, mean Z-IBI
migrated vertically. The factors affecting zooplankton communities scores in the lower reaches (O) were slightly higher than in the middle
were not only influenced by river physiochemical factors, bottom-up reaches (M) in the wet season, and some sites scored greater than 3
effects (phytoplankton), and top-down effects (predation of fish), but using Z-IBI, but were greater than 3 using Phyto-IBI in the same season
also by seasonal changes (Guglielmo et al., 2011). Although the P-IBI (Fig. 4). There was not sufficient information to determine whether
was imperfect, it was necessary to attempt to adopt a plankton-based Phyto-IBI was better than Z-IBI. Survey frequency and sample size
evaluation system for different seasons, considering the algal blooms in should be increased to accurately compare the effectiveness of Phyto-
Hanjiang River. The first large-scale outbreak of algal blooms occurred IBI and Z-IBI in future research. The following discussion considers the
in spring of 1992 and continued to occur every few years, with serious driving forces of water quality and P-IBI spatiotemporal variability in
impacts on the environment along the river (Wang et al., 2018). The the Hanjiang River.
frequency of algal blooms increased after 2010 with an expanding
spatial scale that seriously threatens the regional ecology and presents 4.3. Driving forces of water quality and P-IBI spatiotemporal variability
new challenges (Yang et al., 2012). In the process of creating the IBI, a
causal relationship was assumed between aquatic community quality Phytoplankton and zooplankton assemblages associated with river
and ecosystem health, but the actual situation may not be entirely damming varied greatly depending on geographical location (Matthew
consistent with this hypothesis and it may not be possible to accurately et al., 1999, Truffer et al., 2003, Zhou et al., 2008). In this study, four
detect the impacts of all human activities. To reduce the impacts of water conservancy projects (Danjiangkou, Wangfuzhou, Cuijiaying,
seasonal changes in plankton on P-IBI, the number of surveys should Xinglong) were in operation, two were under construction (Yakou,
also be increased. Nianpanshan), and Xinji was preparation for construction in the
middle-lower reaches of the Hanjinag River. Sampling sites 1, 3, 8, and
12 were in backwater area of the Danjiangkou Dam project, the
4.2. Assessment results from the study area Wangfuzhou Hydropower Station project, the Cuijiaying Navigation
and Power Hub project, and the Xinglong Water Conservancy project,
The P-IBI developed in this study synthesized the abundance, respectively. High water levels, deep water, and slow flow speed in
composition, diversity index, and trophic characteristics of plankton backwater areas for water control projects reduce the speed of pollutant
assemblages along the river’s longitudinal gradient. Our results in- diffusion and river capacity to self-purify. The Cuijiaying Dam mainly
dicated that the ecological status of most samples in the study area was exists for shipping, power generation, and navigation maintenance. The
‘fair’ (Fig. 7), which was consistent with previous studies on plankton construction of Cuijiaying Dam altered the hydrology of the Xiangyang
pollution (Li et al., 2006; Pan et al., 2014). However, most sampling section of the Hanjiang River. The average annual water level in the
sites were oligo-saprobic as indicated by SI. The SI method evaluated reservoir area increased from 2.96 m to 5.70 m, and the average annual
the pollution status of the water body according to specific pollution flow rate decreased from 0.83 m/s to 0.33 m/s (Sun and Wu, 2013).
indicator species in each pollution zone and the existing indicator The reduced flow rate in the area was not conducive to pollutant dif-
species in water samples. There were limitations to this method, be- fusion, so pollutant concentrations in local waters near the sewage
cause the same pollution indicator species can appear in different pol- outlets in the hub and backwater areas increased, creating a serious
lution zones, and SI must be evaluated comprehensively with other aquatic ecological problem (Lin, 2011).

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Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

Abundant plankton was introduced from the Danjiangkou quality at 63% of sites was in class III during the dry season, while 79%
Reservoir. Phytoplankton abundance and major nutrient concentrations of sites were in class II during the wet season. Based on IBI-A, 11% more
around Danjiangkou Dam were much higher than those of previous sites had values less than 3 IBI score in the dry season than that in the
studies (Li et al., 2006, Yin et al., 2011, Pan et al., 2014). In addition, wet season. Environmental conditions were also poorer in the reservoir
due to water transfer, the water flow volume and water environmental backwater area. The main driving force impacting aquatic ecosystems
capacity in the middle-lower reaches of the Hanjiang River were re- in the study area could not be separated from pollutant emissions and
duced, leading to new problems for water quality and the environment. dam impacts. Although the spatial and seasonal distributions of aquatic
This caused a decrease in the population and quantity of aquatic or- health indicated by P-IBI agreed with CWQII, the correlation was not
ganisms in the Hanjiang River (Zhang et al., 2000, Hu and Zhang, ideal. Therefore, further testing and assessments of the applicability of
2008). Furthermore, the percentage of diatom species declined while P-IBI are still needed, although the metrics selected would likely be
green and blue-green algae species increased (Yin et al., 2011). Possible useful in other rivers impacted by dams. Further research is also needed
reasons for the relatively lower ecological status were severe human on other aquatic organisms (e.g. fish, macroinvertebrates, and macro-
interference, including point source emissions, diffuse sources (mainly phytes) to explore the negative impacts of cascade reservoirs, which
agricultural practices such as fertilizer and pesticides utilization), and would help develop a more comprehensive IBI based on all potential
artificial drainage systems. In addition, the main stream channels of the metrics worldwide.
middle and lower reaches of the Hanjiang River flow through seven
major cities, such as Xiangyang, Jingmen, Xiantao, and Xiaogan with CRediT authorship contribution statement
dense pollution sources. According to statistics, the total amount of
rural non-point source wastewater and domestic sewage discharge in Yingying Zhang: Conceptualization, Methodology, Software,
the middle-lower reaches of the Hanjiang River in 2015 were Formal analysis, Writing - original draft. Xuan Ban: Data curation,
26.3 × 104 and 4.7 × 104 t, respectively (Jing et al., 2019). These Methodology, Investigation, Writing - review & editing. Enhua Li:
pollutants were concentrated in Jingmen and Xiangyang. Industrial Supervision, Visualization, Investigation, Writing - review & editing.
wastewater discharge was mainly concentrated in Xiangyang, Jingmen, Zhi Wang: Visualization, Writing - review & editing. Fei Xiao:
and Xiaogan and the total amount of discharge was about 1.4 × 104 t Investigation, Resources.
(Jing et al., 2019). As a tributary of the Hanjiang River, the Tangbai
River is composed of two branches of the Tang River and the Bai River.
It flows through the important agricultural production areas of the Declaration of Competing Interest
Nanyang Basin, and receives a huge amount of industrial and domestic
wastewater, as well as agricultural run-off. The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
5. Conclusions ence the work reported in this paper.

In this study, the P-IBI effectively reflected the environmental Acknowledgements

conditions of flow regulation in the middle-lower reaches of Hanjiang
River in China and can be used in future studies to measure the long- This research paper supported by the Strategic Priority Research
term status of riverine ecosystems affected by cascade dams. Generally, Program of the Chinese Academy of Sciences, Grant No. XDA23040402,
the health of the aquatic ecosystem was in ‘fair’ status, oligotrophic, and the National Natural Science Foundation of China (Grant No.
and class II (wet season)-class III (dry season) as evaluated by IBI, SI, 41671512 and 51479186). The authors thank the editors and anon-
and CWQII, respectively. The ecosystem during the wet season was in ymous referees for their valuable comments and suggestions, which
better health than in the dry season. Based on CWQII method, water helped improve the manuscript.

Appendix A

Table A1
Standard value of basic quality items for environmental quality standards for surface water in China (mg/L) (GB3838-2002).
Indicators Grade of water quality

Class I Class II Class III Class IV Class V

CODMn ≤ 2 4 6 10 15
COD ≤ 15 15 20 30 40
BOD5 ≤ 3 3 4 6 10
NH3-N ≤ 0.15 0.5 1 1.5 2
TP ≤ 0.02 0.1 0.2 0.3 0.4
(lake, (lake, (lake, (lake, (lake,
reservoir reservoir reservoir reservoir reservoir
0.01) 0.025) 0.05) 0.1) 0.2)
TN ≤ 0.2 0.5 1 1.5 2

Notes: Permanganate index (CODMn), chemical oxygen demand (COD), five-day biochemical oxygen demand (BOD5), ammonia nitrogen (NH3-N), total phosphorus
(TP), total nitrogen (TN); http://openstd.samr.gov.cn/bzgk/gb/newGbInfo?hcno = 0DB5914A2BE0CB5D4F459544EDC0E09E (full version of GB3838-2002 in this
website).

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Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

Table A2
Candidate metrics of phytoplankton index of biotic integrity (Phyto-IBI).
Category Candidate multi-metrics Description Abbreviation Correlation Reference

Biomass Total biomass Phytoplankton biomass M1 − Zhang and He, 1991

Abundance Total abundance Phytoplankton abundance M2 −
Cyanophyta Abundance in cyanophyta M3 − Hu and Wei, 2006, Wang et al., 1993
Chlorophyta Abundance in chlorophyta M4 −
Bacillariophyte Abundance in bacillariophyte M5 +
% cyanophyta % total abundance composed of cyanophyta M6 −
% chlorophyta % total abundance composed of chlorophyta M7 −
% bacillariophyte % total abundance composed of bacillariophyte M8 +
% dominant species % total abundance composed of dominant species M9 − Lampitt et al., 1993
% total abundance composed of cyanophyta and chlorophyta M10 −
% total abundance composed of bacillariophyte and chlorophyta M11 + Tan et al., 2017
Diversify index Phytoplankton number Phytoplankton species number M12 +
Bacillariophyte number Bacillariophyte species number M13 +
Margalef index D = (S − 1)/ln N M14 + Margalef, 1958
Shannon-Wiener index H′ = −Σ(ni/N) ln(ni/N) M15 + Shannon and Weaver, 1949
Simpson’s diversity (1-λ) 1-λ = 1 − Sum((Ni * (Ni − 1))/(N * (N − 1))) M16 + Ludwig and Reynolds, 1988
Pielou’s evenness J′ = H′/log(S) M17 + Pielou, 1975
Trophic statues Diatom quotient Centrales abundance/pennales abundance M18 − Nygaard, 1949, Kane et al., 2009
Generic Diatom Index Abundances of M19 + Wu, 1999
(achnanthes + cocconeis + cyclotella)/abundances of
(cymbella + melosira + nitzschia)
Palmer algal genus pollution index M20 − Palmer, 1969

Note: Correlation indicators a correlation between candidate and pristine aquatic environment state; +, indicates a positive correlation; −, indicates a negative
correlation.

Table A3
Candidate metrics of zooplankton index of biotic integrity (Z-IBI).
Category Candidate multi-metrics Description Abbreviation Correlation Reference

Biomass Total biomass Zooplankton biomass M_z1 − Pace, 1986

Biomass of zooplankton/biomass of Lower during blooms of nuisance/inedible/toxic M_z2 + Havens, 1998
phytoplankton alga
Abundance Total abundance Zooplankton abundance M_z3 −
Rotifer Rotifer abundance M_z4 −
Cladocera Cladocera abundance M_z5 +
Copepod Copepod abundance M_z6 +
% rotifer % total abundance composed of rotifer M_z7 −
% total abundance composed of cladocera and M_z8 +
copepod
Diversify index Zooplankton number Zooplankton species number M_z9 +
Rotifer number Rotifer species number M_z10 −
Margalef index D = (S − 1)/ln N M_z11 + Margalef, 1958
Shannon-Wiener index H′ = −Σ(ni/N) ln(ni/N) M_z12 + Shannon and Weaver,
1949
Simpson’s diversity (1-λ) 1-λ = 1 − Sum((Ni * (Ni − 1))/(N * (N − 1))) M_z13 + Ludwig and Reynolds,
1988
Pielou’s evenness J′ = H′/log(S) M_z14 + Pielou, 1975
Trophic statues B/T Brachionus abundance/trichocera abundance M_z15 − Sládeček, 1983

Note: Correlation indicators a correlation between candidate and pristine aquatic environment state; +, indicates a positive correlation; −, indicates a negative
correlation.

Table A4
The comprehensive surface water environmental function grade evaluated by CWQII.
Water quality identification index Level of comprehensive water Environmental functions of surface water and targets for its protection for each grade

1.0 ≤ X1. X2 ≤ 2.0 Class Ⅰ Mainly for source of water and national nature protection areas
2.0 < X1. X2 ≤ 3.0 Class II Mainly for class I protection areas for centralize potable water sources, protection areas for rare fishes,
spawning ground for fishes and shrimps and other aquatic animals
3.0 < X1. X2 ≤ 4.0 Class III Mainly for Class II protection areas for centralized potable water sources, protection areas for general fishes,
and swimming areas
4.0 < X1. X2 ≤ 5.0 Class Ⅳ Mainly for general industrial water areas and entertainment water areas with no direct body contact
5.0 < X1. X2 ≤ 6.0 Class Ⅴ Mainly for farmland water areas and water areas for general landscape requirements
6.0 < X1. X2 Worse than Class Ⅴ

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Table A5
Selected metrics for P-IBI in dry and wet seasons.
Nov. July Nov. July

Abbreviation Metrics Abbreviation metrics Abbreviation Metrics Abbreviation metrics

Phyto-IBI M8 % bacillariophyte M10 % total abundance Z-IBI M_z7 % rotifer M_z6 Copepod abundance
metrics composed of metrics
cyanophyta and
chlorophyta
M9 % dominant species M11 % total abundance M_z8 % total abundance M_z7 % rotifer
composed of composed of
bacillariophyte and cladocera and
chlorophyta copepod
M11 % total abundance M13 Bacillariophyte M_z9 Zooplankton M_z8 % cladocera and
composed of number number copepod
bacillariophyte and
chlorophyta
M12 Phytoplankton M15 Shannon-Wiener M_z12 Shannon-Wiener M_z11 Margalef index
number index index
M13 Bacillariophyte M20 Palmer algal genus M_z13 Simpson’s diversity
number pollution index (1-λ)
M14 Margalef index M_z15 Brachionus
abundance/
trichocera
abundance
M15 Shannon-Wiener
index
M20 Palmer algal genus
pollution index

Table A6
Pearson correlation of Candidate metrics and P-IBI score with physicochemical variables in dry season (* Significant correlation at 0.05 level (bilateral); **
Significant correlation at 0.01 level (bilateral)).
Abbreviation TN TP NH3-N NO3-N NO2-N TOC Chl-a pH

Phyto-IBI −0.057 −0.222 0.448 −0.123 −0.141 −0.095 −0.304 0.125

Z-IBI −0.095 −0.155 0.023 −0.104 0.057 −0.197 −0.014 −0.523*
M8 % bacillariophyte 0.377 0.32 −0.053 0.379 0.393 0.634** 0.510* −0.096
M9 % dominant phytoplankton species 0.484* 0.480* −0.402 0.543* 0.445 0.752** 0.541* −0.233
M11 % bacillariophyte and chlorophyta 0.472* 0.572* −0.284 0.511* 0.372 0.649** 0.429 −0.115
M12 Phytoplankton species number −0.011 −0.224 0.364 −0.04 −0.02 0.035 −0.254 −0.121
M13 Bacillariophyte species number −0.189 −0.347 0.384 −0.236 −0.243 −0.346 −0.549* 0.013
M14 Phytoplankton Margalef index −0.295 −0.401 0.427 −0.331 −0.309 −0.354 −0.531* −0.031
M15 Phytoplankton Shannon-Wiener index −0.255 −0.141 0.15 −0.257 −0.347 −0.685** −0.787** −0.113
M20 Palmer algal genus pollution index −0.085 −0.303 0.672** −0.176 −0.017 −0.16 −0.203 0.084
M_z7 % rotifera 0.299 0.239 0.074 0.284 0.138 0.285 0.027 0.287
M_z8 % cladocera and copepoda −0.349 −0.395 0.495* −0.399 −0.246 −0.34 −0.204 0.18
M_z9 Zooplankton species number 0.409 0.235 0.124 0.38 0.434 0.502* −0.011 −0.278
M_z12 Zooplankton Shannon-Wiener index 0.680** 0.792** −0.493* 0.751** 0.494* 0.646** 0.358 −0.364
M_z13 Zooplankton Simpson’s diversity (1-λ) 0.523* 0.615** −0.447 0.575* 0.312 0.389 0.138 −0.179
M_z15 Brachionus/trichocera 0.426 0.546* −0.269 0.449 0.322 0.319 0.068 −0.172

Table A7
Pearson correlation of Candidate metrics and P-IBI score with physicochemical variables in wet season (* Significant correlation at 0.05 level (bilateral); **
Significant correlation at 0.01 level (bilateral)).
Abbreviation TN TP NH3-N NO3-N NO2-N TOC WT ODO pH

Phyto-IBI −0.18 −0.311 −0.337 0.024 −0.321 −0.417 −0.538* −0.443 −0.636**
Z-IBI 0.016 −0.056 −0.059 −0.075 −0.08 0.05 −0.341 0.051 0.021
M10 % cyanophyta and chlorophyta −0.225 −0.008 0.147 −0.414 0.088 −0.015 0.221 0.530* 0.749**
M11 % bacillariophyte and chlorophyta −0.107 −0.293 −0.354 0.128 −0.352 −0.472* −0.557* −0.517* −0.607**
M13 Bacillariophyte number 0.1 −0.134 0.043 0.298 −0.207 0.047 −0.734** −0.294 −0.418
M15 Phytoplankton Shannon-Wiener index 0.085 0.036 −0.035 0.261 −0.184 −0.066 −0.315 −0.644** −0.679**
M20 Palmer algal genus pollution index 0.528* 0.328 0.276 0.623** 0.063 0.415 −0.163 −0.494* −0.517*
M_z6 Copepoda abundance −0.296 −0.081 −0.178 −0.41 −0.12 −0.069 0.32 0.748** 0.535*
M_z7 % rotifera −0.103 0.029 −0.161 −0.111 −0.148 0.036 0.3 0.196 0.138
M_z8 % cladocera and Copepoda −0.191 −0.182 −0.058 −0.138 −0.279 −0.3 −0.348 0.039 −0.003
M_z11 Zooplankton Margalef index 0.42 0.034 −0.181 0.578** −0.086 0.256 −0.276 −0.266 −0.624**

12
Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

Appendix B. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ecolind.2020.106282.

References Lampitt, R.S., Wishner, K.F., Turley, C.M., Angel, M.V., 1993. Marine snow studies in the
Northeast Atlantic Ocean: distribution, composition and role as a food source for
migrating plankton. Mar. Biol. 116, 689–702. https://doi.org/10.1007/BF00355486.
Arman, N.Z., Salmiati, S., Said, M.I.M., Aris, A., 2019. Development of macroinvertebrate- Li, B.S., Zhou, P.J., Wang, X.Y., Zhu, L.D., 2013a. Opportunities and eco-environmental
based multimetric index and establishment of biocriteria for river health assessment influence of cascade hydropower development and water diversion projects in
in Malaysia. Ecol. Ind. 104, 449–458. Hanjiang river basin. J. Geol. Soc. India 82, 692–700. https://doi.org/10.1007/
Baek, S.H., Son, M., Kim, D., Choi, H.W., Kim, Y.O., 2014. Assessing the ecosystem health s12594-013-0207-3.
status of Korea Gwangyang and Jinhae bays based on a planktonic index of biotic Li, F.Q., Cai, Q.H., Ye, L., 2010. Developing a Benthic Index of Biological Integrity and
integrity (P-IBI). Ocean Sci. J. 49, 291–311. https://doi.org/10.1007/s12601-014- some relationships to environmental factors in the subtropical Xiangxi River, China.
0029-2. Int. Rev. Hydrobiol. 95, 171–189. https://doi.org/10.1002/iroh.200911212.
Ban, X., Wu, Q.Z., Pan, B.Z., Du, Y., Feng, Q., 2014. Application of composite water Li, J.P., Dong, S.K., Liu, S.L., Yang, Z.F., Peng, M.C., Zhao, C., 2013b. Effects of cascade
quality identification index on the water quality evaluation in spatial and temporal hydropower dams on the composition, biomass and biological integrity of phyto-
variations: a case study in Honghu Lake, China. Environ. Monitor. Assessment. 186, plankton assemblages in the middle Lancang-Mekong River. Ecol. Eng. 60, 316–324.
4237–4247. https://doi.org/10.1007/s10661-014-3694-9. https://doi.org/10.1016/j.ecoleng.2013.07.029.
Barbour, M.T., Gerritsen, J., Griffith, G.E., Frydenborg, R., McCarron, E., White, J.S., Li, X.F., Huang, D.M., Xie, W.X., 2006. Preliminary study on zooplankton in autumn in the
Bastian, M.L., 1996. A framework for biological criteria for florida streams using middle reaches of Hanjiang River. Water Fishery (in Chinese) 26, 56–59. https://doi.
benthic macroinvertebrates. J. North Am. Bentholog. Soc. 15, 185–211. https://doi. org/10.15928/j.1674-3075.2006.02.029.
org/10.2307/1467948. Li, Y., Yang, N., Qian, B., Yang, Z., Liu, D., Niu, L., Zhang, W., 2018. Development of a
Buchanan, C., Lacouture, R.V., Marshall, H.G., Olson, M., Johnson, J.M., 2005. bacteria-based index of biotic integrity (Ba-IBI) for assessing ecological health of the
Phytoplankton reference communities for Chesapeake Bay and its tidal tributaries. Three Gorges Reservoir in different operation periods. Sci. Total Environ. 640–641,
Estuaries 28, 138–159. https://doi.org/10.1007/BF02732760. 255–263.
Carpenter, K.E., Johnson, J.M., Buchanan, C., 2006. An index of biotic integrity based on Lin, Q.C., 2011. Influence of dams on river ecosystem and its countermeasures. J. Water
the summer polyhaline zooplankton community of the Chesapeake Bay. Marine Resour. Prot. 3, 7. https://doi.org/10.4236/jwarp.2011.31007.
Environ. Res. 62, 165–180. https://doi.org/10.1016/j.marenvres.2006.03.009. Liu, J.K., Yu, Z.T., 1992. Water quality changes and effects on fish populations in the
Cheng, B., Xia, R., Zhang, Y., Yang, Z., Hu, S., Guo, F., Ma, S., 2019. Characterization and hanjiang river, China, following hydroelectric dam construction. Regulated Rivers,
causes analysis for algae blooms in large river system. Sustainable Cities Soc. 51, Res. Manag. 7, 359–368. https://doi.org/10.1002/rrr.3450070406.
101707. https://doi.org/10.1016/j.scs.2019.101707. Lu, X.R., Wang, X.L., Yang, C., Liu, X., Yang, Q., 2018a. Changes and driving forces of the
Deng, Z.M., Zhang, X., Li, D., Pan, G.Y., 2015. Simulation of land use/land cover change water-sediment relationship in the Middle Reaches of the Hanjiang River. Water 10,
and its effects on the hydrological characteristics of the upper reaches of the Hanjiang 16. https://doi.org/10.3390/w10070887.
Basin. Environ. Earth Sci. 73, 1119–1132. https://doi.org/10.1007/s12665-014- Lu, X.R., Zhuang, Y.H., Wang, X.L., Yang, Q., 2018b. Assessment of streamflow change in
3465-5. middle-lower reaches of the Hanjiang River. J. Hydrol. Eng. 23, 12. https://doi.org/
EC (European Communities), 2000. Directive 2000/60/EC of the European Parliament 10.1061/(ASCE)HE.1943-5584.0001727.
and of the Council of 23 October 2000 Establishing a framework for community Ludwig, J.A., Reynolds, J.F., 1988. Statistical Ecology: A primer in Methods and
action in the field of water policy. Off. J. Eur. Commun. 22 (L327), 1–72. https://doi. Computing. John Wiley and Sons, New York.
org/10.1017/cbo9780511610851.056. Ma, Q., 2015. Assessment of ecosystem health of Upper Yangtze River in Yibin to Jiangjin
Eduardo, A.L., Carla, H., Marilia, S., Carlos, W., Luc, E., 2016. Diatoms as bioindicators in using plankton-index of Biotic Integrity. Southwest University, Chongqing, P.R.
rivers. In: River Algae (chapter11), pp. 245–271. Doi: 10.1007/978-3-319-31984- China.
1_11. MAPRC, 2007. The Specification for Ecological Environment Monitoring of
Gannon, J.E., Stemberger, R.S., 1978. Zooplankton (Especially Crustaceans and Rotifers) Fisheries—Part 3: Freshwater. SC/T 9102.3-2007. Ministry of Agriculture of the
as indicators of water quality. Trans. Am. Microscop. Soc. 97, 16–35. https://doi.org/ People’s Republic of China.
10.2307/3225681. Margalef, R., 1958. Information theory in ecology. General Syst. 3, 36–71.
Gibson, G.R., Bowman, A.B., Gerritsen, J., Snyder, B.D., 2000. Estuarine and coastal Matthew, M.P., Sullivan, C.A., Acreman, M.C., 1999. Ecosystem impacts of large dams.
marine waters: bioassessment and biocriteria technical guidance. Environmental Centre for Ecology & Hydrology.
Protection Agency (EPA) Office of Water. Maulood, B.K., Alobaidy, A.H.M.J., Alsaboonchi, A., Abid, H.S., Alobaidy, G.S., 2011.
Guglielmo, L., Minutoli, R., Bergamasco, A., Granata, A., Zagami, G., Antezana, T., 2011. Phytoplankton Index of Biological Integrity (P-IBI) in Several Marshes, Southern
Short-term changes in zooplankton community in Paso Ancho basin (Strait of IRAQ. J. Environ. Protect. 2, 387–394. https://doi.org/10.4236/jep.2011.24043.
Magellan): functional trophic structure and diel vertical migration. Polar Biol. 34, Miao, Q., Ying, G., Liu, Z.Q., Tan, X.H., 2009. Application of comprehensive water quality
1301–1317. https://doi.org/10.1007/s00300-011-1031-0. identification index in water quality assessment of river. Congress Intell. Syst.
Gupta, J., van der Zaag, P., 2008. Interbasin water transfers and integrated water re- https://doi.org/10.1109/GCIS.2009.166.
sources management, where engineering, science and politics interlock. Phys. Chem. Moran, E.F., Lopez, M.C., Moore, N., Müller, N., Hyndman, D.W., 2018. Sustainable hy-
Earth, Parts A/B/C 33, 28–40. https://doi.org/10.1016/j.pce.2007.04.003. dropower in the 21st century. Proc. Natl. Acad. Sci. 115, 11891. https://doi.org/10.
Havens, K.E., 1998. Size structure and energetics in a plankton food web. Oikos 81, 1073/pnas.1809426115.
346–358. https://doi.org/10.2307/3547055. Morley, S.A., Karr, J.R., 2002. Assessing and restoring the health of urban streams in the
Hu, H.J., Wei, Y.X., 2006. The freshwater algae of China, systematics, taxonomy and Puget Sound basin. Conservation Biol. 16, 1498–1509. https://doi.org/10.1046/j.
ecology. Beijing (in Chinese). Science Press, Beijing. 1523-1739.2002.01067.x.
Hu, Z.F., Zhang, L.P., 2008. Effect of median-line south-to-north water transfer project on MWRPRC, 2014. Standards for the investigation of reservoir fishery resources. SL
water environment in middle and lower reaches of Hanjiang River. J. Water Resour. 167–2017. Ministry of Water Resources of the People’s Republic of China.
Arch. Eng. (in Chinese) 6, 15–17. Niu, H., Chen, C., Han, B.P., 2015. Quality and reliability of quantifying phytoplankton
Jakhar, P., 2013. Role of phytoplankton and zooplankton as health indicators of aquatic abundance and biomass data based upon the concerntrated water sample method. J.
ecosystem: a review. Ijirs Com 2, 489–500. Lake Sci. 5, 22–28.
Jiang, X.Z., Du, N.S., 1979. Fauna Sinica, Crustacea, Freshwater Cladocera. Beijing (in Nygaard, G., 1949. Hydrobiological studies on some Danish ponds and lakes. Part II. The
Chinese). Science Press, Beijing. quotient hypothesis and some new or little known phytoplankton organisms. Det
Jing, Z.X., Xia, J., Zhang, X., Wang, Q., 2019. Spatial and temporal distribution and Kongelige Danske Videnskabernes Selskab, Biologiske Shrifter. 7, 1–293.
variation of water quality in the middle and down stream of Hanjiang River. Res. Pace, M.L., 1986. An empirical analysis of zooplankton community size structure across
Environ. Sci. 32, 104–115. https://doi.org/10.13198/j.issn.1001-6929.2018.07.25. lake trophic gradients. Limnol. Oceanogr. 31, 45–55. https://doi.org/10.4319/lo.
Johnson, J.M., Buchanan, C., 2014. Revisiting the chesapeake bay phytoplankton index of 1986.31.1.0045.
biotic integrity. Environ. Monit. Assess. 186, 1431–1451. https://doi.org/10.1007/ Palmer, C.M., 1969. A composite rating of algae tolerating organic pollution. J. Phycol. 5,
s10661-013-3465-z. 78–82. https://doi.org/10.1111/j.1529-8817.1969.tb02581.x.
Jungwirth, M., Muhar, S., Schmutz, S., 2000. Assessing the ecological integrity of running Pomari, J., Kane, D.D., Nogueira, M.G., 2018. Application of multiple-use indices to assess
waters. Doi: 10.1023/A:1017045527233. reservoirs water quality and the use of plankton community data for biomonitoring
Kane, D.D., Gordon, S.I., Munawar, M., Charlton, M.N., Culver, D.A., 2009. The purposes. Int. J. Hydro. 2, 168–179. https://doi.org/10.15406/ijh.2018.02.00065.
Planktonic Index of Biotic Integrity (P-IBI), an approach for assessing lake ecosystem Pomari, J., Kane, D.D., Ferreira, R.A.R., Nogueira, M.G., 2019. A new tool to assess
health. Ecol. Ind. 9, 1234–1247. https://doi.org/10.1016/j.ecolind.2009.03.014. ecosystem health in large subtropical reservoirs: development and validation of a
Karr, J.R., Chu, E.W., 2000. Introduction: sustaining living rivers. In: Assessing the Planktonic Index of Biotic Integrity. Aquatic Ecosyst. Health Manag. 22, 15–29.
Ecological Integrity of Running Waters. Springer, Netherlands, pp. 1–14. https://doi. https://doi.org/10.1080/14634988.2019.1562837.
org/10.1007/978-94-011-4164-2_1. Pan, X.J., Zhu, A.M., Zheng, Z.W., Qiao, Y., 2014. Structural characteristics and influ-
Lacouture, R.V., Johnson, J.M., Buchanan, C., Marshall, H.G., 2006. Phytoplankton index encing factors of phytoplankton community in the middle and lower reaches of
of biotic integrity for Chesapeake Bay and its tidal tributaries. Estuaries Coasts 29, HanjiangRiver during spring season. Chinese J. Ecol. 33, 33–40. https://doi.org/10.
598–616. https://doi.org/10.2307/3809726. 13292/j.1000-4890.20131220.0012.

13
Y. Zhang, et al. Ecological Indicators 114 (2020) 106282

Pantle, R., Harald, B., 1955. Die biologische Überwachung der Gewässer und die North Am. Bentholog. Soc. 24, 990–1008. https://doi.org/10.1899/03-028.1.
Darstellung ihrer Ergebnisse. GWF 96. Jg. Heft 18, S.604. Wang, Y.K., Wang, D., Wu, J.C., 2015. Assessing the impact of Danjiangkou reservoir on
Petr Šmilauer, J.L., 2014. Multivariate Analysis of Ecological Data using Canoco 5, second ecohydrological conditions in Hanjiang river, China. Ecol. Eng. 81, 41–52. https://
ed. Cambridge University Press, Cambridge. doi.org/10.1016/j.ecoleng.2015.04.006.
Pielou, E.C., 1975. Ecological Diversity. Wiley-InterScience, New York. Wen, J.Z., Xu, H.X., 2010. Atlas of Freshwater Phytoplankton in China Beijing (in
Qadir, A., Malik, R.N., 2009. Assessment of an index of biological integrity (IBI) to Chinese). Science Press, Beijing.
quantify the quality of two tributaries of river Chenab, Sialkot, Pakistan. Whitfield, A., Elliott, M., 2005. Fishes as indicators of environmental and ecological
Hydrobiologia 621, 127–153. https://doi.org/10.1007/s10750-008-9637-0. changes within estuaries, a review of progress and some suggestions for the future. J.
Qu, Y.P., Huang, Y., He, Z.G., 2014. Influence of backwater support of the Yangtze river Fish Biol. 61 (supplement A), 229–250. https://doi.org/10.1006/jfbi.2002.2079.
on the water-sand process from xinglong of the han river to hanchuan. China Water Wu, H.J., Yu, Q.M., Shen, Y.F., 2005. A structure characteristics of exosystem along the
Transport 62–64. https://doi.org/10.13646/j.cnki.42-1395/u.2014.11.027. middle and lower reaches of Hanjiang river in spring. J. Huazhong Univ. Sci. Tech.
SEPA, 2002a. Environmental Quality Standard for Surface Water (EQSSW), GB (Nat. Sci. Ed.) 33, 99–101.
3838–2002. State Environment Protection Administration. Wu, J.T., 1999. A generic index of diatom assemblages as bioindicator of pollution in the
SEPA, 2002b. Monitoring and Analysis Methods of Water and Wastewater, fourth ed. Keelung River of Taiwan. Hydrobiologia 397, 79–87. https://doi.org/10.1023/
China Environmental Science Press, Beijing. a:1003694414751.
Shannon, C.E., Weaver, W., 1949. The Mathematical Theory of Communication. The Wu, N.C., Cai, Q.H., Fohrer, N., 2012a. Development and evaluation of a diatom-based
University of Illinois press, Urbana. index of biotic integrity (D-IBI) for rivers impacted by run-of-river dams. Ecol. Ind.
Shen, J.R., 1979. Fauna Sinica, Crustacea, Freshwater Copepoda. Science Press, Beijing. 18, 108–117. https://doi.org/10.1016/j.ecolind.2011.10.013.
Shen, Y.F., Gu, M.R., Gong, X.J., Shi, Z.X., Wei, Y.X., Zheng, Y., 1990. New Technology of Wu, N.C., Schmalz, B., Fohrer, N., 2012b. Development and testing of a phytoplankton
Micro-Biological Monitoring. China Architecture & Building Press, Beijing. index of biotic integrity (P-IBI) for a German lowland river. Ecol. Ind. 13, 158–167.
Sládeček, V., 1983. Rotifers as indicators of water quality. Hydrobiologia 100, 169–201. https://doi.org/10.1016/j.ecolind.2011.05.022.
Song, X.X., Zhuang, Y.H., Wang, X.L., Li, E.H., 2018. Combined effect of Danjiangkou Xu, J.X., 1997a. Evolution of mid-channel bars in a braided river and complex response to
reservoir and cascade reservoirs on hydrologic regime downstream. J. Hydrol. Eng. reservoir construction: an example from the middle Hanjiang River, China. Earth
23, 12. https://doi.org/10.1061/(ASCE)HE.1943-5584.0001660. Surf. Process. Landforms 22, 953–965. https://doi.org/10.1002/(SICI)1096-
Sun, C., Wu, H.J., 2013. Effect of water diversion and cascade development on water 9837(199710)22:10<953::AID-ESP789>3.0.CO;2-S.
environmental capacity of the Hanjiang River in Xiangyang. Environ. Protec. Sci. (in Xu, J.X., 1997b. Study of sedimentation zones in a large sand-bed braided river, an ex-
Chinese) 39, 9–12. https://doi.org/10.16803/j.cnki.issn.1004-6216.2013.02.003. ample from the Hanjiang River of China. Geomorphology 21, 153–165. https://doi.
Tan, Q., Ma, Q.Q., Li, B.B., 2017. Ecological health assessment of the upper reaches of the org/10.1016/s0169-555x(97)00039-1.
Yangtze River, based on biotic integrity index of phytoplankton. Freshwater Fisheries Xu, Z.X., 2005. Comprehensive water quality identification index for environmental
(in Chinese) 47, 97–104. https://doi.org/10.13721/j.cnki.dsyy.2017.03.015. quality assessment of surface water. J. Tongji Univ. (Nat. Sci.) 33, 482–488. https://
Teng, L.H., Zhang, B., Liu, X.J., Bai, C.J., Zhang, J., Tan, D.P., Huang, P.S., 2014. doi.org/10.1360/biodiv.050058.
Development and use of a Phytoplankton-Index of Biotic Integrity to assess Yongjiang Yang, Q., Xie, P., Shen, H., Xu, J., Wang, P.L., Zhang, B., 2012. A novel flushing strategy
River ecosystem health. Polish J. Environ. Stud. 23, 901–908. for diatom bloom prevention in the lower-middle Hanjiang River. Water Res. 46,
Truffer, B., Bratrich, C., Markard, J., Peter, A., Wüest, A., Wehrli, B., 2003. Green hy- 2525–2534. https://doi.org/10.1016/j.watres.2012.01.051.
dropower, the contribution of aquatic science research to the promotion of sustain- Yin, D.C., Zheng, L.L., Song, L.R., 2011. Spatio-temporal distribution of phytoplankton in
able electricity. Aquat. Sci. 65, 99–110. https://doi.org/10.1007/s00027-003- the Danjiangkou Reservoir, a water source area for the Southto-North Water
0643-z. Diversion Project (Middle Route), China. Chin. J. Oceanol. Limnol. 29, 531–540.
Wang, F.J., 2007. Evaluation of Water Quality and the Type of Nourishment in the East- Zeng, Q., 2005. A Study of the Water Environment and the Sustainable Development at
Half of Lake Chaohu by Means of Plankton. Anhui Agricultural University. the Middle and Lower Reaches of the Hanjiang River. Eastern China Normal
Wang, J., Wang, J.C., Xu, Q., 2018. Causes analysis of water bloom in middle and lower University, Shanghai.
reaches of Hanjiang River in 2018 and its countermeasures. Yangtze River (in Zhang, J.H., Sun, M.K., Deng, Z.M., Lu, J., Wang, D.W., Chen, L., Liu, X.Y., 2017. Runoff
Chinese) 49, 7–11. https://doi.org/10.16232/j.cnki.1001-4179.2018.17.002. and sediment response to cascade hydropower exploitation in the middle and lower
Wang, J.J., 1961. Flora of Freshwater Rotifers in China Beijing (in Chinese). Science Han River, China. Math. Prob. Eng. 1–15. https://doi.org/10.1155/2017/8785236.
Press, Beijing. Zhang, J.M., He, Z.H., 1991. Manual of Investigation for Fisheries Resources in Inland
Wang, M.D., Wang, M.X., Luo, S.Y., 1993. The Handbook of Aquatic Organism Waters. Beijing (in Chinese). Agriculture Press, Beijing.
Monitoring. Southeast University Press, Nanjing. Zhang, J.Y., Luo, L., Li, C.S., 2000. Study on the impact of the Middle Route Project of
Wang, Q.G., Du, Y.H., Su, Y., Chen, K.Q., 2012. Environmental impact post-assessment of South-to-North Water Transfer on the ecological environment of the middle and
dam and reservoir projects, a review. Procedia Environ. Sci. 13, 1439–1443. https:// lower reaches of the Hanjiang River. Environ. Sci. Technol. (in Chinese) (supple-
doi.org/10.1016/j.proenv.2012.01.135. ment), 1–32. https://doi.org/10.19672/j.cnki.1003-6504.2000.s1.001.
Wang, Y.G., Zhang, W.S., Zhao, Y.X., Peng, H., Shi, Y.Y., 2016. Modelling water quality Zhou, S.C., Tang, T., Wu, N.C., Fu, X.C., Cai, Q.H., 2008. Impacts of a small dam onri-
and quantity with the influence of inter-basin water diversion projects and cascade verine zooplankton. Int. Rev. Hydrobiol. 93, 297–311. https://doi.org/10.1002/iroh.
reservoirs in the Middle-lower Hanjiang River. J. Hydrol. 541, 1348–1362. https:// 200711038.
doi.org/10.1016/j.jhydrol.2016.08.039. Zhou, Y., Qu, X.D., Zhao, R., Ma, S.Q., Zhang, Y., Yin, Q.W., 2013. Standardized methods
Wang, Y.K., Stevenson, R.J., Metzmeier, L., 2005. Development and evaluation of a for selecting reference and impaired sites to evaluate river health. Res. Environ. Sci.
diatom-based Index of Biotic Integrity for the Interior Plateau Ecoregion, USA. J. 26, 410–417. https://doi.org/10.13198/j.res.2013.04.73.zhouy.013.

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