Science of the Total Environment 541 (2016) 65–73
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Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
Site-specific water quality criteria for aquatic ecosystems: A case study of
pentachlorophenol for Tai Lake, China
Yi Chen a,b, Shuangying Yu c, Song Tang d, Yabing Li a, Hongling Liu a,⁎, Xiaohui Zhang a, Guanyong Su a, Bing Li b,
Hongxia Yu a, John P. Giesy a,e,f,g
a
State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, Jiangsu 210023, China
Jiangsu Provincial Academy of Environmental Sciences, Nanjing, Jiangsu 210036, China
Savannah River Ecology Laboratory, University of Georgia, Aiken, SC 29808, USA
d
School of Environment and Sustainability, University of Saskatchewan, Saskatoon, SK S7N 5B3, Canada
e
Toxicology Centre, University of Saskatchewan, Saskatoon, SK S7N 5B3, Canada
f
Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, SK S7N 5B3, Canada
g
School of Biological Sciences, University of Hong Kong, Hong Kong, SAR, China
b
c
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Acute toxicity tests of nine native
species were performed.
• Species compositions in the 1980s were
considered to restore the healthier
ecological community in Tai Lake.
• In situ toxicity tests were performed to
consider the bioavailability of PCP in
Tai Lake.
• Like criteria in some developed countries, criteria of PCP were expressed as
functions of pH.
a r t i c l e
i n f o
Article history:
Received 7 May 2015
Received in revised form 30 August 2015
Accepted 1 September 2015
Available online xxxx
Editor: D. Barcelo
a b s t r a c t
Given the widely varying types of aquatic ecosystems and bioavailability of chemicals, it is important to develop
site-specific water quality criteria (WQC) to ensure criteria are neither over- nor under-protective. In the study,
using pentachlorophenol (PCP) as an example, several approaches to derive site-specific WQC were investigated,
including the conventional species sensitivity distribution (SSD), weighted SSD based on the proportion of each
trophic level, and water effect ratio (WER) method. When corrected to a pH of 7.8, the conventional SSD
approach resulted in criteria maximum concentration (CMC) and criteria continuous concentration (CCC) of
18.11 and 1.74 μg/L, respectively. If SSD was weighted according to the current species composition in
Tai Lake, the CMC and CCC were 32.81 and 4.48 μg/L, respectively. However, available data suggest that many
Abbreviations: WQC, water quality criteria; PCP, pentachlorophenol; 2, 4-DCP, 2, 4-dichlorophenol; SSDs, species sensitivity distributions; CMC, criteria maximum concentration; CCC,
criteria continuous concentration; WER, water effect ratio; ACR, acute-chronic ratio; NOEC, no observed effect concentration; LOEC, lowest observed effect concentration; MATC, maximum acceptable toxicant concentration; EC50, 50% effective concentration; LC50, 50% lethal concentration; EC10, 10% effective concentration; WQS, water quality standard.
⁎ Corresponding author at: School of the Environment, Nanjing University, Nanjing, Jiangsu 210023, China.
E-mail address: hlliu@nju.edu.cn (H. Liu).
http://dx.doi.org/10.1016/j.scitotenv.2015.09.006
0048-9697/© 2015 Elsevier B.V. All rights reserved.
66
Keywords:
Site-specific criteria
Historic species composition
Criteria maximum concentration (CMC)
Criteria continuous concentration (CCC)
Water-effect ratio
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
sensitive species inhabiting Tai Lake during 1980s were disappeared. Considering the species composition of the
healthier ecosystem in 1980s, the CMC and CCC were 10.99 and 0.38 μg/L, respectively, which provide more
protective water quality standards. Water effect ratio (WER) was further used to correct for co-occurrence of
other toxicants and factors affecting bioavailability of PCP. A final WER of 4.72 was applied to adjust the criteria
derived by using the weighted SSD for the 1980s aquatic community, and the final CMC and CCC obtained were
51.87 and 1.79 μg/L, respectively, at a pH of 7.8. Water quality criteria derived using the 1980s species
composition and adjusted with WER were deemed the most appropriate WQC for water management and aquatic life protection. Merits of the various approaches for developing WQC for protection of aquatic species were
discussed.
© 2015 Elsevier B.V. All rights reserved.
1. Introduction
Aquatic ecosystems vary dramatically in their physicochemical
properties, which in turn affect bioavailability of some metal and organic chemical contaminants. In addition, species compositions and their
relative sensitivities to chemical contaminants vary widely among
ecosystems, which might lead the national criteria to be over- or
under-protective for specific basin. There are two basic uncertainties
that could be made when applying national WQC. First, the presence
of other contaminants might result in the WQC being underprotective. In addition, the bioavailable fraction or forms in which
contaminants can occur might affect relative potencies of contaminants
under various conditions. Therefore, it is of great significance for a range
of water quality criteria (WQC) that are adjusted for conditions among
ecoregions (USEPA, 2002, 2004, 2009). In general, due to adsorption
to particulates or coordination interaction of the organic or in-organic
ligands, chemical activities, the available fractions of contaminants are
generally less under field conditions than in tests conducted under
laboratory conditions where contaminants are normally nearly 100%
available. Therefore, hardness-adjusted WQC criteria have been developed for metals and more recently, the Biotic Ligand Model has been
applied to correct for the forms of metals present under varying geochemical conditions. Furthermore, for sediment acid volatile sulfides
(AVS) and organic carbon normalization have been used to modify
sediment quality criteria (SQC) based on site-specific conditions. In
addition, the U.S. EPA published guidelines for deriving numerical sitespecific WQC by considering the effects of physical and chemical parameters (e.g., pH, hardness, temperature, etc.) and proposed use of the
water effect ratio (WER) (Carlson, 1984).
Tai Lake (Ch: Taihu), one of the largest freshwater lakes in China, has
been contaminated with municipal, industrial and agricultural runoff
due to rapid economic growth and intensive industrialization in the
region. It is unique in its geological characteristics, assemblage of species
and pattern of contaminants (Wu et al., 2008). The current WQC used
for Tai Lake were developed based on national water quality standards
and therefore might not be appropriate for protecting the local aquatic
community.
Chlorophenols (CPs) are an important group of contaminants in
China and other parts of the world. As raw materials in production of
textile additives, pharmaceutical products, chemicals and pesticides,
large amounts of CPs have the potential to enter aquatic environments
and are frequently detected (Gao et al., 2008). Chlorophenols are especially problematic because of their resistance to degradation, toxicity to
aquatic life, and potential to bioaccumulate (Bello et al., 2013; Jin et al.,
2012a; Martí et al., 2011).
One of the more common CPs is pentachlorophenol (PCP), a priority
pollutant in China (Zhou et al., 1990). It has been widely detected in
environmental media including air, water, sediment, soil, and tissues
of wildlife, and humans (Hodin et al., 1991; Mari et al., 2007). Use of
PCP as a molluscicide in Dongting Lake resulted in concentrations
as great as 104 μg/L in water and 4.8 × 104 μg/kg dry mass (dm) in
sediment (Yin et al., 2008; Zheng et al., 2012). The maximum concentrations of PCP in water of two major river basins (Yellow and Yangtze)
were 29 and 0.59 μg/L, respectively (Gao et al., 2008). The median
concentrations of PCP in the Yangtze River and Tai Lake were 60 and
12 ng/L (Qu et al., 2004). Pentachlorophenol has also been found in
aquatic organisms (e.g., fish, shrimp, carp) at concentrations as great
as 6.3 × 102 μg/kg wet mass (wm) in grass carp (Ctenopharyngodon
idellus) (Zheng et al., 2000), posing potential risks to humans via consumption of fish.
Several studies demonstrated the toxic potency of PCP. Concentrations from 0.025 to 5 mg/L resulted in lesser hatchability and greater
mortality and deformities in embryos of zebrafish (Danio rerio)
(Zheng and Zhu, 2005). The 96-h median lethal concentration (LC50)
for the catfish (Ictalurus punctatus) was 68 μg/L (Luo et al., 2009). Fishes
were the most sensitive species, followed by invertebrates and aquatic
plants (Luo et al., 2009).
Several WQC have been developed for CPs in China, including 2, 4dichlorophenol (2,4-DCP) (Yin et al., 2002) and 2, 4, 6-trichlorophenol
(2,4,6-TCP) (Yin et al., 2003). The criteria maximum concentration
(CMC) and the criteria continuous concentration (CCC) for 2, 4-DCP
were 1.25 × 103 μg/L, and 2.12 × 102 μg/L, respectively (Yin et al.,
2002). For 2, 4, 6-TCP, the CMC and CCC were 1.01 × 103 μg/L and
2.3 × 102 μg/L, respectively (Yin et al., 2003). pH-dependent WQC for
2, 4-DCP, 2, 4, 6-TCP and PCP (CMC2,4-DCP = exp.(0.6274 × pH +
0.7630), CCC2,4-DCP = exp.(0.6274 × pH-2.1056); CMC2,4,6-TCP =
exp.(0.8937 × pH-1.1374), CCC2,4,6-TCP = exp.(0.8937 × pH-2.9706);
CMCPCP = exp.(0.7330 × pH-3.2847), CCCPCP = exp.(0.7330 × pH4.3564); μg/L) were derived by considering species compositions
among three trophic levels (Xing et al., 2012a).
Because of the unique regional characteristics and importance of the
resources provided by Tai Lake, it was deemed necessary to develop
site-specific WQC for this Lake that would be more certain to effectively
protect native biota more effectively by adjusting WQC to local
geochemical and ecological conditions as well as local water quality.
The objective of the present study was to develop site-specific WQC
for PCP in order to protect the aquatic community that inhabited Tai
Lake prior to its current more contaminated state half a decade ago.
Several WQC were generated based on (1) laboratory toxicity testing
of native aquatic biota; (2) species composition and structure of the
aquatic community specific to Tai Lake, and (3) geochemical characteristics of water in Tai Lake.
2. Materials and methods
2.1. Toxicity of PCP
2.1.1. Chemicals
Pentachlorophenol was purchased from Sigma-Aldrich (98%;
St. Louis, MO, USA) and was dissolved in dimethyl sulfoxide (DMSO)
to make a stock solution, which was stored at −20 °C. Concentrations
of DMSO in treatments did not exceed 0.05% (v/v).
2.1.2. Selection of test species
Test species were selected based on the following criteria: (1) native
species in China; (2) species found in Tai Lake; (3) ability to be raised
in the laboratory; and (4) sufficient numbers to repeat the experiment. The nine (9) species (Table S1) used in the present study
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
were from 4 phyla, including green algae (Scenedesmus obliquus), oligochaete (Limnodrilus hoffmeisteri), water flea (Daphnia magna),
shrimp (Neocaridina denticulate), tadpole of wood frog (Rana
chensinensis), yellow catfish (Pelteobagrus fulvidraco), silver carp
(Hypophthalmichthysmolitrix), bighead carp (Hypophthalmichthys
nobilis), and grass carp (C. idellus). S. obliquus and D. magna were cultured and maintained following previously published methods (Xing
et al., 2012a, 2012b). L. hoffmeisteri were collected from the field a
year prior to initiating toxicity tests. Water was changed every other
day and animals were fed with soybean powder and lettuce.
N. denticulate, R. chensinensis and fish were purchased from a local market in Nanjing, China. All individuals of the same species were from the
same collected location. N. denticulate was acclimated in the laboratory
for at least 14 days and was fed with D. magna. Mortalities for all test
animals during acclimation were less than 10%. Healthy young
N. denticulate of similar mass (approximately 0.16 g) and length (2–
3 cm) were selected for the experiment. R. chensinensis tadpoles
(20 days posthatching) were maintained at room temperature for
7 days. Tadpoles of wood frog were fed twice a day and water was
changed daily. Mortality was less than 10% during acclimation. Tadpoles
were not fed the day before exposure. Individuals with snout-to-vent
length of 1.2–1.4 cm were randomly assigned to treatments. Juvenile
fishes were also acclimated for at least 14 days and housing conditions
were similar to those for other species. Only health larvae (3–4 cm
length) were used in studies. Fish were not fed the day before initiating
exposure. For all organisms, tap water aerated for at least 3 days was
used. Dissolved oxygen (DO), pH, conductivity, alkalinity (CaCO3),
and hardness (CaCO3) were 6.07 ± 0.24 mg/L, 8.12 ± 0.11, 319 ±
9.10 μs/cm, 95.48 ± 4.64 mg/L, and 126 ± 4.95 mg/L, respectively.
2.1.3. Acute toxicity testing
For each species tested there was a control, a solvent control
(DMSO) and six concentrations of PCP. There were three replicates per
treatment and each replicated had ten organisms. Organisms were not
fed during the experiment and water was changed daily. Temperature
during the experiment was 24 ± 1 °C for D. magna and 20 ± 1 °C for
other species. The initial density of S. obliquus was approximately 105
cells/mL in 50 ml Erlenmeyer flasks containing 20 mL sterilized WC
medium. The exposure lasted for 24 h (Suter and Cormier, 2008).
Biomass was measured after 24 h and the average rate of growth was
calculated as described previously (Xing et al., 2012b). D. magna and
all fish were exposed to PCP for 48 h and 96 h, respectively.
2.1.4. Toxicity data collection and selection
Information on toxicity of PCP to aquatic organisms, published prior
to April 2014, was obtained from AQUIRE (http://www.epa.gov/
ecotox), CNKI China, Weipu database or other published literature.
Studies from previous literature were selected if the test species was
native to Tai Lake and if information on pH and exposure duration
was provided. Data were also selected according to criteria by Stephan
et al. (1985) with the duration of exposure was 96 h for fish, 48 h
for D. magna, and 24 h for algae. Endpoints for acute toxicity were
50% median lethal concentration (LC50) or 50% median effective concentration (EC50). To increase the number of species with toxicity data
available for the analysis, acute studies using other exposure durations,
such as 72 h for fish and 24 h for the water flea, were also included. For
chronic toxicity data, exposures of 96 h or 72 h were selected for algae
(due to rapid cell division rate of algae (CCME, 2007)), 21 d for
D. magna, and 14 days or longer for fish. Compared to the no observed
effect concentration (NOEC) and lowest observed effect concentration
(LOEC) values which largely depend on experimental designs and
statistical analyses, maximum acceptable toxicity concentration
(MATC, the geometric average of NOEC and LOEC) and 10% effective
concentration (EC10) derived from concentration effect curves are
more reliable and therefore were given priority in WQC derivation. If
the MATC or EC10 were not available, the NOEC or LOEC was used to
67
derive the chronic criteria (Xing et al., 2012a, 2012b). Chronic data for
D. magna were calculated from previous studies on multi-generational
toxicity data of PCP (Chen et al., 2014; Stephan et al., 1985). Toxicity
data that had no corresponding pH value reported were eliminated.
All the acute and chronic toxicity data screened are shown in Table S2
and S3.
2.2. Historical and current species compositions of Tai Lake
Information on historic and current aquatic species assemblage in
Tai Lake was obtained from the open literature, CNKI China and
Weipu. Databases, and survey reports published by Nanjing Institute
of Geography and Limnology, Chinese Academy of Sciences, Suzhou
Environmental Monitoring Station and Jiangsu Environmental Monitoring Center (Chen and Liu, 2003; Fan, 1996; Gu et al., 2005; Lei et al.,
2008; Ni and Zhu, 2005; Sun and Huang, 1993; Zheng et al., 2007).
Historical data on species from various ecological communities in
Tai Lake are summarized in the supporting information (Tables S4-8).
2.3. Tai Lake toxicity tests
To assess potential effects of physicochemical characteristics of Tai
Lake and presence of other toxicants in Tai Lake on toxicity of PCP,
acute toxicity tests with Tai Lake water were conducted with the 9
aquatic species used in the previous laboratory toxicity test. Samples
were collected during April to December 2013 from West Tai Lake, the
part of Tai Lake that was most polluted. Twenty-liter water samples
were collected from each of the four sites, including Huangnian,
Fenshui, Dapu, and Chendong (Fig. 1, Table S10). All samples were
collected at a depth of 0.5 m, transported at 4 °C in amber jars to the
Laboratory of Pollution Control and Resource Reuse at Nanjing University. An additional five hundred-milliliter water samples from each sampling site were also obtained for water chemistry analyses. Water
quality parameters including pH, temperature, and dissolved oxygen
were measured with YSI multiple water quality parameters (6600 V24, Ecosense, Ohio, USA) in situ. Average temperature was 16–17 °C
and pH was approximately 6.0–7.0. DO was 7.56 ± 2.15 mg/L. Water
samples from each site were homogenized by mixing, filtered
(0.45 μm) and stored in a refrigerator at 4 °C for further determination
of metal ions using inductively coupled plasma mass spectrometry,
ICP-MS (NexION™ 300X ICP-MS, PerkinElmer, USA).
After acute toxicities were determined for site waters, a water-effect
ratio (WER) was calculated for each site. The WER is defined as the ratio
of the toxic potency of PCP in Tai Lake water samples to that in laboratory water.
2.4. Data analysis
2.4.1. Acute toxicity and derivation of chronic data
The LC50, EC50 values with 95% confidence intervals were estimated
using Trimmed Spearman Karber method (TSK) Program Version 1.5.
The EC10 of intrinsic rate of population of growth was calculated with
Graphpad Prism (GraphPad Prism Development Core Team, http://
www.graphpad.com/scientific-software/prism/).
2.4.2. Data processing and WQC development
Toxicity of PCP is affected by pH (Bello et al., 2013; Kishino and
Kobayashi, 1995; Martí et al., 2011; Sinclair et al., 1999). Due to the
hydroxyl on the benzene ring PCP can exist as the ion or protonated
neutral form. The protonated neutral form is more likely to cross cell
membranes and accumulate in organisms, and as a result has greater
toxic potency. Toxicity and pH are related through the pKa, which determines the relative proportions of PCP that are in the ionic and neutral
forms. In order to consider effects of pH on toxic potency of PCP,
water quality criteria used by U.S. EPA have been expressed as functions
of pH (USEPA, 2009). In the present study, toxicity data were
68
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
Fig. 1. Map of Tai Lake in China and the four sites where water samples were collected for in situ toxicity testing.
standardized to the standard pH according to USEPA (http://water.epa.
gov/scitech/swguidance/standards/criteria/current/index.cfm#altable),
which is 7.8, by use of a previously developed relationship to predict
toxicity of PCP as a function of pH (R2 = 0.3310, P = 0.00020)
(Eq. (1)) (Xing et al., 2012b).
△lnEC50 =LC50 ¼ 0:7330 △pH
ð1Þ
After correction for pH (Tables S11 ~ 12), species sensitivity distributions (SSDs) were developed for acute and chronic toxicity. In order to
be protective of the healthier and more integrated ecological community in Tai Lake during the 1980s, in addition to the conventional SSD
method, a weighted SSD (WSSD) methodology was considered when
calculating a site-specific WQC for PCP (Shi et al., 2014; Xing et al.,
2012a). To obtain a large number of species for chronic SSD analysis,
the Acute-Chronic ratio (ACR) method was used for estimating chronic
toxicity. Since the ACRs for a majority of species were within a factor of
ten, the final ACR was calculated as the geometric mean of all the ACRs
available (Stephan et al., 1985). The SSD method uses all acute and
chronic toxicity data available to generate a cumulative probability
distribution of sensitivity using the log-normal model. Hazard concentrations that are protective of 95% species (HC5) were calculated. Due
to uncertainties in calculating the HC5, the final WQC was calculated
by dividing the HC5 values by a factor of 2 (Shi et al., 2014; Stephan
et al., 1985). For the SSD method, the cumulative probability was
calculated (Eq. (2)).
Pi ¼ Ri =ðN þ 1Þ
ð2Þ
Where: Pi was the cumulative probability of species, Ri was the rank
of specie i, N was the number of toxicity data screened.
In order to take the species composition into consideration, weighted SSDs were also developed (Eq. (3)).
8
Sp1
>
>
>
>
< Sp2
X ¼ Sp3
>
>
⋮
>
>
:
SPk
SI1 SV1
SI2 SV2
SI3 SV3
⋮
⋮
SIl SVm
9
>
>
>
>
=
>
>
>
>
;
ð3Þ
Where k, l and m were the number of toxicity data for plants, invertebrates and vertebrates representing the first, second and third trophic
levels, respectively (Forbes and Calow, 2002). Spi (i = 1,2,…,k) was the
sample of plants, SIi (i = 1,2,…,l) the sample of invertebrates, and SVi
(i = 1,2,…,m) the sample of vertebrates. The probability of one species
of plant, invertebrate and vertebrate was calculated by Eqs. (4), (5) and
(6), respectively.
PPi ¼ Np =ðN kÞ
ð4Þ
PIi ¼ NI =ðN lÞ
ð5Þ
PVi ¼ NV =ðN mÞ
ð6Þ
In which, PPi, PIi and PVi were probabilities of individual plants, invertebrates and vertebrates, respectively. Values for Np, NI and NV were the
number of plants, invertebrates and vertebrates in Tai Lake; N was the
number of total species. The resistant green algae and cyanobacteria
were included in the plant taxonomic level. The cumulative probability
was calculated by adding the probabilities of species for which the
toxicity data were ranked. Since the relative sensitivities of the species
that have disappeared from Tai Lake are unknown, a conservative estimation method was applied (Wang et al., 2014). This method has
been shown to be appropriate and that it delivers output specifically
for the ecosystems of interest. Briefly, p% Hazardous Concentration
(HCp) can be derived that relates to a probability of a fraction p(%) of
species that would exceed the threshold for a given degree of effect,
and p% depends on the number (N) of species in Tai Lake.
3. Results and discussion
3.1. Development of WQC based on current acute and chronic toxicity data
3.1.1. Acute and chronic toxicity data collection
Acute toxicities were determined for nine species native to Tai Lake,
China (Table 1). The LC50 for H. molitrix, P. fulvidraco, H. nobilis, and
C. idellus were less than 400 μg/L (22–368 μg/L), indicating PCP is extremely toxic to fish according to the toxicity classification standards
(Jin et al., 2012b; Zhang et al., 2007). The LC50 was 450.08 μg/L for
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
69
Table 1
Acute toxicity of pentachlorophenol to nine native aquatic species at Tai Lake, China, at pH = 8.10.
Species
Silver carp (Hypophthalmichthysmolitrix)
Yellow catfish (Pelteobagrus fulvidraco)
Shrimp (Neocaridina denticulate)
Bighead carp (Hypophthalmichthys nobilis)
Grass carp (Ctenopharynodon idellus)
Water flea (Daphnia magna)
Wood frog (Rana chensinensis)
Oligochaete (Limnodrilus hoffmeisteri)
Green algae (Scenedesmus obliquus)
Duration
Endpoint
4 days
4 days
4 days
4 days
4 days
2 days
4 days
4 days
1 days
LC50
LC50
LC50
LC50
LC50
EC50
LC50
LC50
EC50
D. magna, which is also relative sensitive to PCP. The EC50 and LC50 of
PCP for S. obliquus and L. hoffmeisteri were 1861.58 and 884.18 μg/L,
respectively, consistent with previously studies in which an EC50 of
930 μg/L (pH = 7.5) for S. obliquus and a LC50 of 500 μg/L (pH = 7.0)
for L. hoffmeisteri were reported (Chapman et al., 1982; Xing et al.,
2012b).
Chronic data for D. magna, an EC10 value of 4.79 μg/L, based on intrinsic growth rate of population (Chen et al., 2014), was calculated from
previous studies on multi-generational toxicity data of PCP.
There were 63 acute toxicity values for 30 aquatic species, and 19
chronic toxicity values for 16 species (Fig. 2). At pH = 7.80, acute toxicity ranged from 17.00 (H. smolitrix) to 29,622.83 μg/L (Chlorella kessleri)
with a median of 242.36 μg/L (n = 30), and chronic toxicity ranged from
3.79 (D. magna) to 7470.48 μg/L (C. kessleri) with a median of
124.45 μg/L (n = 16). The most acutely sensitive species were
H. smolitrix, P. fulvidraco, Carassius auratus, I. punctatus (Fig. 3a) while
the most chronically sensitive species were D. magna, Macrobrachium
superbum, Mylopharyngodon piceus, Plagiognathops microlepis (Fig. 3b).
The difference in numbers of relatively more sensitive species between
acute and chronic toxicity was due to a lack of chronic toxicity data and
the fact that there is usually a lack of chronic toxicity data for sensitive
species with acute toxicity data available. The ACR of each species
with chronic data was calculated and the final acute-chronic ratio
(FACR) was 3.75 (Table S12). For species with no chronic toxicity data,
toxicity data were generated using the FACR (Table S13). Based on
ACR method, the most chronically sensitive species were D. magna,
H. smolitrix, M. superbum and P. fulvidraco. As indicated above,
H. molitrix and P. fulvidraco were also the most acutely sensitive species
(Fig. 3a).
3.1.2. Development of WQC for PCP and comparison among methods for
deriving chronic WQC
Toxicity values adjusted for pH were used for the construction of
SSDs. Two SSDs were derived for chronic toxicity using screened
Fig. 2. Aquatic toxicity data of pentachlorophenol included for derivation of species sensitivity distributions. n is the number of data points and the line in the boxplot indicates the
median toxicity value. Geometric mean was used when there was more than one toxicity
value for a species.
Concentration (95% CI) (μg/L)
21.63 (18.64–26.63)
98.54 (85.22–111.85)
151.80 (135.82–173.11)
181.10 (165.12–197.08)
367.52 (351.54–386.16)
450.08 (412.80–476.71)
548.62 (503.34–599.22)
884.18 (761.68–1028.00)
1861.58 (1720.43–3542.06)
experimental data only (n = 16) or experimental data and ACRderived data combined (n = 30) (Fig. 3). The HC5 of the SSD for acute
and chronic toxicity were 36.22 and 3.48 μg/L, respectively. To protect
95% of species, the CMC was 18.11 μg/L and the CCC was 1.74 μg/L.
The chronic HC5 based on both screened and ACR predicted toxicity
values was 4.66 μg/L (n = 30), the corresponding CCC was 2.33 μg/L,
1.5-fold greater than the CCC derived with screened data only. The
CMC obtained in this study was similar to the CMC (19 μg/L, freshwater,
at pH = 7.8) used by the USEPA, while the CCC, derived in this study
was almost 8.6-fold less than the CCC (15 μg/L, freshwater, at pH =
7.8) used by the USEPA. This result suggests that the USEPA chronic
water criteria would be less protective than the more site-specific
WQC developed with endemic species for Tai Lake. However, this result
is likely due to variation that would be observed among empirical
results.
3.2. Development of WQC based on historical species composition
3.2.1. Historical changes in species composition
Numbers of species of phytoplankton, macrophytes, zooplankton,
benthic animals and fishes in the last century and the early 21st century
were collected and compared (Tables S4–S8). In the 1980s, there were
seven phyla of phytoplankton, three phyla of macrophytes, three
phyla of zooplankton, five phyla of benthic animals and fourteen orders
of fishes. In recent years, the number of phyla was eight, three and nine
for phytoplankton, benthic animals, and fish, respectively (Cai et al.,
2010; Chen and Liu, 2003; Gu et al., 2005). Numbers of species of phytoplankton have increased, with a majority increase in cyanobacteria. This
is likely due to increasing pollution from rapid human population
growth and industrial development around Tai Lake (Fan, 1996).
Proportions of plants, invertebrates and vertebrates were 38%, 40%
and 22%, respectively, in 1980s, and 67%, 21%, and 12%, respectively in
the early 21st (Fig. 4). The number of relatively more sensitive fish
decreased significantly from 107 to 60 (Fig. S1), such as Cynoglossus
purpureomaculatus, Fugu obscurus, Opsariichthys uncirostris bidens,
and Distoechodon tumirostris (Table S9). Lots of migratory fishes
(e.g., Acipenser sinensis, Tenualosa reevesii, Myxocyprinus asiaticus,
Ochetobibus elongates, Luciobrama macrocephalalus, Elopichthys
bambusa, Coreius heterokon, Rhinogobio typus Bleeker, Saurogobio
dumerili, Cobitis sinensis, Leiocssis longirostris, Pseudobagrus taeniatus,
etc.) almost disappeared.
Numbers of species of Chlorophyta, Aulacoseira and Cyanophyta
have increased greatly, especially for Chlorophyta, with an almost
four-fold increase than that in 1987. Cyanobacteria became the dominant taxa since 1998 (Qian et al., 2008). However, there were reductions
in numbers of species for invertebrates and fishes. Numbers of species
of Mollusca, Arthropoda and Cypriniformes have decreased by nearly
half. Invertebrates belonging to Aschelminthes, and some fish like
Mugiliformes have disappeared. Numbers of species of invertebrates
and fishes have decreased from 190 to 111, 107 to 60, respectively
(Fan, 1996). Which might due to the increasing development of agriculture and industries and urbanization that has resulted in pollution
of Tai Lake.
70
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
Fig. 3. Species sensitivity distributions (SSDs) for acute (a) and chronic toxicity (b and c) of pentachlorophenol. Chronic toxicity values in (b) are experimental data whereas values in
(c) include both experimentally and acute-chronic ratio (ACR) derived data. Values in red (a and b) are the data obtained in the present study, while those in red (c) are data calculated
by the ACR method.
3.2.2. Weighted SSD based on 1980s and current species composition in
Tai Lake
Considering species diversity, the aquatic ecological community in
the 1980s would be considered “healthier” than the current community.
The theoretical basis of SSD is that the data on sensitivities of individual
species to toxicants are distributed as a random sample from the entire
population of possible sensitivities and are used to estimate descriptive
parameters of the SSD. Generally, the SSD method has been found to be
useful to predict the response of the entire community to toxicants
(Maltby et al., 2005; Schroer et al., 2004), but there are still some issues
regarding the application of SSDs (Forbes and Calow, 2002). As mentioned previously, the screened toxicity data include acute values from
30 species and chronic values from 16 species. The most sensitive
species were L. hoffineisteri, fish, and crustaceans. The more sensitive
species included H. molitrix, P. fulvidraco, Carassius auratus, I. punctatus,
D. magna, M. superbum, M. piceus, and P. microlepis, which all belong to
invertebrates and fishes. Since 1980, the total numbers of species of
Fig. 4. Proportions of taxonomic groups (plants, invertebrates and vertebrates, in 1980s
and 21st century in Tai Lake, China.)
vertebrates and fishes decreased from 297 to 171, respectively
(Fig. S1) and several species including C. purpureomaculatus,
F. obscurus, O. uncirostris bidens, and D. tumirostris have disappeared
(Table S9). The elimination of these sensitive species had an impact on
the structure and function of the community. Since sensitive species
that have disappeared from Tai Lake were not available, the WQC
derived with toxicity data obtained in this study may not be adequate
to protect the healthier community of 1980s. To generate the most
appropriate criteria, HCp was calculated based on the concept that if
the threshold for effect was equal to the effect concentration for the
most sensitive species. The chance that a species would be affected
would be 1/N (number of species considered in targeted basin.). However, the probability of adversely affecting functioning of the ecosystem
would remain unknown (Wang et al., 2014). Since more tolerant plants
or algae account for a large proportions of the species present currently,
only the total number of invertebrates and vertebrates were considered
when deriving the HCp (P = 1/297 and 1/171). Water quality criteria
that would promote restoration of the more diverse community that
was present in the 1980s (297 species) compared to that for the current
community (171 species) are considered more protective.
By considering the species compositions present in the 1980s and
current the species compositions, weighted methods were used with
SSDs to estimate HC5 or HCp as the cutoff point (Table 2). For weighted
SSDs, HCp was used as the cutoff point, and the CMC and CCC for acute
and chronic toxicity were 10.99 and 0.38 μg/L, respectively, by considering the number of invertebrates and vertebrates in 1980s. While, the
CMC and CCC for acute and chronic toxicity were 32.81 and 4.48 μg/L,
respectively, when using the number of invertebrates and vertebrates
in the current community. The acute and the chronic values derived
by the weighted SSDs combined with HCp considering that species compositions of the 1980s were slightly more conservative than values obtained with the conventional SSD (HC5/2, 18.11 and 1.74 μg/L)
(Table 2, Fig. 5). The acute value generated by the weighted SSD was
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
71
Table 2
Comparison of water quality criteria derived in this study and current national standard.
Method
Cutoff point
Acute value with 95% CI
(μg/L)
Chronic value with 95% CI
(μg/L)
Current national standard
(μg/L)
0.05
0.05
P1
0.05
P2
36.22 (27.99–48.19)
48.64 (39.36–61.23)
10.99 (−)
104.23 (83.95–131.52)
32.81 (24.77–50.58)
3.48 (−)
4.72 (−)
0.38 (−)
21.38 (11.80–42.66)
4.48 (−)
9
Unweighted SSD
Weighted SSDa
Weighted SSDb
a
b
1
2
Weighted SSD based on species composition in 1980s.
Weighted SSD based on current species composition.
Cutoff point selected by considering the number of species in 1980s.
Cutoff point selected by considering the current number of species.
3-fold lower than the value obtained with the unweighted method,
while the chronic value was approximately 7-fold lower than that
obtained with unweighted method. Criteria considering number of species (sensitive invertebrates and vertebrates), with HCp as the cutoff
point resulted in the most conservative WQC (Table 2). As we know,
using models built for two species in the same taxonomic level, when
predicted toxicity values were compared with the actual values, even
for species in the same kingdom, differences were greater than 10-fold
for 29% of data points studied (Raimondo et al., 2010). In order to
decrease the uncertainty, further taxonomic level classification should
be performed to improve the values estimated by use of the SSD,
because for species in the same family, predicted values were with 5fold of actual value for 91% of data points for species in the same family
(Raimondo et al., 2010). Whereas, when community structure were
considered, uncertainty was reduced and the developed WQC are
more protective (Versteeg et al., 1999). Additionally, while taking into
account the relative proportions of species and their respective sensitivities, the weighted SSD method with cutoff point HCp is likely to be more
protective of the most sensitive species compared to the conventional
SSD with cutoff point HC5 (Wang et al., 2014).
From a conservation perspective, the weighted SSD method with
cutoff point HCp is deemed to be more appropriate to protect ecosystem
integrity since it would not be possible to determine if the most sensitive species are keystone species upon which ecosystem function
might be dependent.
3.3. Toxicity in water of Tai Lake
3.3.1. Water effect ratio (WER)
Water from the Dapu site was the most toxic to P. fulvidraco,
N. denticulate, H. nobilis, D. magna, R. chensinensis, L. hoffmeisteri, and
S. obliquus compared with the other three sites (Table S15). Because
toxicity of PCP is affected by pH, water effect ratios (WER) were calculated after correcting original toxicity data for pH (Table 3). The WER
was 4.72, 5.81, 5.98 and 7.21 for Dapu, Huangnian, Chendong, and
Fenshui, respectively. The range of WER values among locations was relatively small so the most conservative value of 4.72 observed at Dapu
was chosen to be protective. Based on surveys conducted in July 2013
and December 2013, four physicochemical parameters (Temperature,
pH, turbidity and Chl a) (Table S16) and concentrations of 13 elements
(Cr, Pb, V, and Zn et al) (Table S17) of the water samples from all sampling sites were summarized, respectively. Concentrations of Cr, Pb, V,
and Zn (Table S16) were the greatest at Dapu (Table S17), which
might result into a relatively small WER value at Dapu. Therefore, in
order to derive the WQC conservatively, the WER of Dapu (4.72) was
applied to derive site-specific WQC considering real water effect. The
fact that the WER was greater than 1.0 suggests that there were factors
in water from Tai Lake that reduced the exposure (i.e., bioavailability)
and/or toxicity of PCP to test organisms. This is not uncommon since
standard laboratory testing procedures is likely to generate more
conservative toxicity estimates due to procedures such as continuous
exposure and use of clean water in which there lacks ligands that can
bind to toxicants to reduce bioavailability.
3.3.2. Development of Tai Lake site-specific WQC
Using a WER of 4.72, when pH = 7.8, to restore the aquatic species composition in 1980s, the CMC and CCC values were 51.87 and
1.79 μg/L, respectively. Considering the relationship between LC50/
EC50 and WQC (Xing et al., 2012a), the WQC were derived as a function of pH. Eqs. (7)–(8) (Eqs. (7) and (8) were equations for acute
and chronic criteria as a function of pH):
CMC ðμg=LÞ ¼ exp:ð0:7330 pH 1:769Þ
ð7Þ
CCC ðμg=LÞ ¼ exp:ð0:7330 pH 5:135Þ
ð8Þ
Site-specific WQC derived during this study were compared to
the current threshold value of 9 μg/L specified by water quality standard
(WQS) for surface water source for drinking water (ChinaEPA. GB38382002, 2002) (Table 4, Fig. 6). The current national criteria of 9 μg/L,
Fig. 5. Acute (a) and chronic (b) unweighted (orange) and weighted (green) pentachlorophenol species sensitivity distributions (SSDs) for aquatic organisms in Tai Lake, China. The SSDs
were derived using the 1980s species composition data. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
72
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
Table 3
Acute toxicity of pentachlorophenol during in situ exposures of nine aquatic species at pH
= 7.80.
Sites
Speciesa
In situ
EC50/LC50
(μg/L)
EC50/LC50
(μg/L)
Water effect
ratio (WER)
Final
WER
Chendong
D. magna
L. hoffmeisteri
R. chensinensis
S. obliquus
H. molitrix
C. idellus
H. nobilis
P. fulvidraco
N. denticulate
D. magna
L. hoffmeisteri
R. chensinensis
S. obliquus
H. molitrix
C. idellus
H. nobilis
P. fulvidraco
N. denticulate
D. magna
L. hoffmeisteri
R. chensinensis
S. obliquus
H. molitrix
C. idellus
H. nobilis
P. fulvidraco
N. denticulate
D. magna
L. hoffmeisteri
R. chensinensis
S. obliquus
H. molitrix
C. idellus
H. nobilis
P. fulvidraco
N. denticulate
1640.19
5703.22
1470.04
12,774.40
120.66
2081.39
904.95
482.64
444.93
1360.43
5116.84
1121.85
8177.80
138.13
1657.54
546.23
295.09
433.22
2295.05
7181.03
1767.27
14,394.05
282.53
866.44
1406.39
539.95
596.46
2119.78
7032.76
1691.23
11,999.31
131.98
1370.58
558.39
380.72
568.54
210.02
792.79
433.91
1841.21
17.00
290.68
143.00
77.94
120.06
210.02
792.79
433.91
1841.21
17.00
290.68
143.00
77.94
120.06
210.02
792.79
433.91
1841.21
17.00
290.68
143.00
77.94
120.06
210.02
792.79
433.91
1841.21
17.00
290.68
143.00
77.94
120.06
7.81
7.19
3.39
6.94
7.10
7.16
6.33
6.19
3.71
6.48
6.45
2.59
4.44
8.13
5.70
3.82
3.79
3.61
10.93
9.06
4.07
7.82
16.62
2.98
9.83
6.93
4.97
10.09
8.87
3.90
6.52
7.76
4.72
3.90
4.89
4.74
5.98
Dapu
Fenshui
Huannian
Fig. 6. Comparison among water quality criteria (WQC) derived from the present study,
the current water quality standard (WQS) in China and WQC provided by U.S. EPA.
4.72
water_sanitation_health/en/). Unlike the criteria of PCP in US EPA, all
of these general criteria values do not take into account the effect of
pH on toxicity. Our results indicate that species compositions and the
physicochemical properties of the local basins should be considered in
the derivation of WQC so that site-specific water standards can be obtained to address the protection goals for a particular site.
7.21
4. Conclusions
5.81
a
Endpoints for S. obliquus, D. magna and other species are 24 h EC50, 48 h EC50 and
96 h EC50s, respectively.
which directly referred to the guideline value of World Health Organization (WHO) (9 μg/L) (http://www.who.int/water_sanitation_health/
en/), would not be sufficient to protect the biotic community present
in Tai Lake during the 1980s (1.79 μg/L). Due to slightly acidic conditions, the current Chinese WQS would be under-protective of the
adverse effects of PCP on a more integrated community in the 1980s.
According to directive of European Union, the annual average of environmental quality standards for PCP in surface waters was 0.4 μg/L,
and the maximum allowable concentration was 1 μg/L (EP and EU,
2008), which were stricter than the criteria used by US EPA and the
criteria derived for Tai Lake at a pH of 7.8 from the current study. As
for the trigger values of PCP for freshwater in Australian and New
Zealand, the 95% protection level trigger value of PCP was 10 μg/L
(ANZECC and ARMCANZ, 2000). And the guideline value given
by WHO, as mentioned above, was 9 μg/L (http://www.who.int/
In conclusion, without considering the species composition and sitespecific water effect in Tai Lake, the acute water quality criteria of PCP in
Tai Lake was determined to be 18.11 μg/L, and the chronic criteria
derived with only experimental data only and experimental and ACRderived data combined were 1.74 and 2.33 μg/L, respectively. In order
to restore the aquatic ecological community of the 1980s, SSDs taking
the species composition in the 1980s into consideration were generated. The acute and chronic criteria derived from these SSDs were 10.99
and 0.38 μg/L, respectively. Finally, a WER of 4.72 was obtained which
resulted in a final acute criterion of 51.87 μg/L and a final chronic criterion of 1.79 μg/L. Our results suggest that the use of laboratory and in
situ toxicity data with further consideration of site-specific species composition generate most appropriate WQC for Tai Lake and the current
national criteria of 9 μg/L would not be sufficient to protect the biotic
community present in Tai Lake.
Acknowledgements
This work has been co-financially supported by theNational Natural
Science Foundation (No. 21377053) and Major National Science and
Technology Projects (No. 2012ZX07506-001 and 2012ZX07501-00302) of China. Dr. Giesy was supported by the program of 2012 “High
Level Foreign Experts” (#GDW20123200120) funded by the State
Administration of Foreign Experts Affairs, the P.R. China to Nanjing
University and the Einstein Professor Program of the Chinese Academy
of Sciences. He was also supported by the Canada Research Chair
program, a Visiting Distinguished Professorship in the Department of
Biology and Chemistry and State Key Laboratory in Marine Pollution,
City University of Hong Kong. In addition, the authors would like to
thank Allen Burton for his help in English.
Table 4
Water quality criteria (μg/L) for pentachlorophenol based on species compositions in Tai Lake during 1980s at different pH values.
a
a
pH=6.00
pH=6.50
pH=7.50
pH=8.00
pH=8.50
pH=9.00
CMC/bCCC
CMC/CCC
CMC/CCC
CMC/CCC
CMC/CCC
CMC/CCC
CMC/CCC
13.86/0.48
20.00/0.69
28.85/0.99
41.62/1.44
60.04/2.07
86.62/2.99
124.96/4.31
pH=7 .00
CMC = criteria maximum concentration, bCCC = criteria continuous concentration. The data in red were less than current water quality criteria 9 μg/L in China.
Y. Chen et al. / Science of the Total Environment 541 (2016) 65–73
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.scitotenv.2015.09.006.
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Supplementary data
Table S1 Average life expectancy of tested species
Species
Silver carp (Hypophthalmichthy smolitrix)
Yellow catfish (Pelteobagrus fulvidraco)
Shrimp (Neocaridina denticulate)
Bighead carp (Hypophthalmichthys nobilis)
Grass carp (Ctenopharynodon idellus)
Water flea (Daphnia magna)
Wood frog (Rana chensinensis)
Oligochaete (Limnodrilus hoffmeisteri)
Average Life Expectancy
7-8 Years
2-4 Years
12-15 months
7-8 Years
7-8 Years
68.40±9.82 Days
7-8 Years
80 Days
1
Sources
https://en.wikipedia.org/
https://en.wikipedia.org/
https://en.wikipedia.org/
https://en.wikipedia.org/
https://en.wikipedia.org/
(Zhuang and Liang, 1986)
https://en.wikipedia.org/
https://en.wikipedia.org/
Table S2. Acute toxicities, expressed a median lethal concentrations of PCP to aquatic organisms.
Species
Endpoint
Effect
L. hoffmeisteri
LC50
MORT
L. hoffmeisteri
LC50
Ceriodaphnia reticulata
Exposure
Concentration
method
pH
4
R, U
7.00
500.00
(Chapman et al., 1982)
MORT
4
S, U
8.12
884.18
This study
LC50
MORT
2
F, M
7.30
150.00
(Hedtke et al., 1986)
Ceriodaphnia dubia
LC50
MORT
2
F, M
8.00
307.00
(Hedtke et al., 1986)
Daphnia carinata
LC50
MORT
2
R, U
7.90
570.00
(Hickey, 1989)
D. magna
LC50
MORT
2
S, M
8.58
145.00
(Spehar et al., 1985)
D. magna
LC50
MORT
2
S, U
6.50
55.00
(Oikari et al., 1992)
D. magna
LC50
MORT
2
S, U
6.50
38.00
(Oikari et al., 1992)
D. magna
LC50
MORT
2
S, U
6.50
55.00
(Oikari et al., 1992)
D. magna
LC50
MORT
2
S, M
8.00
860.00
(Kim et al., 2006)
D. magna
LC50
IMBL
2
S, U
7.10
62.00
(Xing et al., 2012)
D. magna
LC50
IMBL
2
S, U
8.00
346.00
(Xing et al., 2012)
D. magna
EC50
IMBL
2
S, U
8.80
1232.00
(Xing et al., 2012)
D. magna
EC50
IMBL
2
S, U
8.12
450.08
This study
Simocephalus vetulus
LC50
MORT
2
F, M
7.30
160.00
(Hedtke et al., 1986)
Simocephalus vetulus
LC50
MORT
2
F, M
7.70
250.00
(Hedtke et al., 1986)
Simocephalus vetulus
LC50
MORT
2
F, M
8.00
255.00
(Hedtke et al., 1986)
Simocephalus vetulus
LC50
MORT
2
F, M
8.30
364.00
(Hedtke et al., 1986)
Mesocyclops leuckarti
LC50
MORT
2
S, U
7.30
138.00
(Willis, 1999)
Mesocyclops leuckarti
LC50
MORT
2
S, U
7.30
173.00
(Willis, 1999)
Chironomus riparius
LC50
MORT
1
S, U
9.00
1948.00
(Warwick and Wadleigh, 1986)
Chironomus riparius
LC50
MORT
1
S, U
4.00
384.00
(Warwick and Wadleigh, 1986)
(d)
2
(μg/L）
Reference
Species
Endpoint
Effect
Chironomus riparius
LC50
MORT
Macrobrachium superbum
LC50
N. denticulate
Exposure
Concentration
Reference
method
pH
1
S, U
6.00
465.00
(Warwick and Wadleigh, 1986)
MORT
4
R, M
7.24
140.00
(Jin et al., 2012)
LC50
MORT
4
S, U
8.12
151.80
This study
Corbicula fluminea
LC50
MORT
4
R, M
7.24
230.00
(Jin et al., 2012)
Lymnaea acuminata
LC50
MORT
2
R, U
7.90
228.00
(Gupta and Durve, 1984)
Viviparus bengalensis
LC50
MORT
2
S, U
7.90
1570.00
(Gupta and Durve, 1984)
Brachionus calyciflorus
EC50
HTCH
2
S, U
7.50
1310.00
(Radix et al., 2000)
Lemna minor
LC50
MORT
3
S, U
5.10
190.00
(Blackman et al., 1955)
Soirodela polyrhiz
LC50
GGRO
4
R, M
7.24
1120.00
(Jin et al., 2012)
Chlamydomonas reinhardtii
EC50
PGRT
4
F, U
7.00
410.00
(Schafer et al., 1994)
Chlorella kessleri
EC50
ABND
4
S, U
8.00
34300.00
(Mostafa and Helling, 2002)
S. obliquus
EC50
GGRO
1
S, U
6.50
261.00
(Xing et al., 2012)
S. obliquus
EC50
GGRO
1
S, U
7.50
927.00
(Xing et al., 2012)
S. obliquus
EC50
GGRO
1
S, U
9.00
24063.00
(Xing et al., 2012)
S. obliquus
EC50
MORT
1
S, U
8.12
1861.58
This study
Carassius auratus
LC50
MORT
4
S, U
7.30
23.00
(Inglis and Davis)
Carassius auratus
LC50
MORT
4
S, U
7.70
49.00
(Inglis and Davis)
Carassius auratus
LC50
MORT
4
S, U
7.50
55.00
(Inglis and Davis)
Carassius auratus
LC50
MORT
4
S, U
7.30
56.00
(Inglis and Davis)
Carassius auratus
LC50
MORT
4
F, M
7.84
200.00
(Thurston et al., 1985)
Carassius auratus
LC50
MORT
4
F, M
7.94
328.00
(Thurston et al., 1985)
C. idellus
LC50
MORT
4
S, U
8.12
367.52
This study
Erythroculter ilishaeformis
LC50
MORT
4
R, M
7.24
130.00
(Jin et al., 2012)
(d)
3
(μg/L）
Species
Endpoint
Effect
H. smolitrix
LC50
MORT
H. nobilis
LC50
Mylopharyngodon piceus
Exposure
Concentration
Reference
method
pH
4
S, U
8.12
21.63
This study
MORT
4
S, U
8.12
181.10
This study
LC50
MORT
4
R, M
7.24
95.00
(Jin et al., 2012)
Plagiognathops microlepis
LC50
MORT
4
R, M
7.24
90.00
(Jin et al., 2012)
Oncorhynchus mykiss
LC50
MORT
4
S, NR
7.40
115.00
(Mayer and Ellersieck, 1986)
Oncorhynchus mykiss
LC50
MORT
4
S, NR
7.40
34.00
(Mayer and Ellersieck, 1986)
Oncorhynchus mykiss
LC50
MORT
4
S, NR
7.40
52.00
(Mayer and Ellersieck, 1986)
Oncorhynchus mykiss
LC50
MORT
4
S, NR
7.40
121.00
(Mayer and Ellersieck, 1986)
Oncorhynchus mykiss
LC50
MORT
4
F, U
7.40
66.00
(Dominguez and Chapman, 1984)
Oncorhynchus mykiss
LC50
MORT
4
F, M
7.85
115.00
(Thurston et al., 1985)
Oncorhynchus mykiss
LC50
MORT
4
S, U
8.00
160.00
(Sappington et al., 2001)
Oncorhynchus mykiss
LC50
MORT
4
R, NR
6.22
153.00
(1991)
Oncorhynchus mykiss
LC50
MORT
4
S, U
8.00
160.00
(Dwyer et al., 2005)
Ictalurus punctatus
LC50
MORT
4
S, NR
7.40
66.00
(Mayer and Ellersieck, 1986)
Ictalurus punctatus
LC50
MORT
4
S, NR
7.40
68.00
(Mayer and Ellersieck, 1986)
Ictalurus punctatus
LC50
MORT
4
F, M
7.71
132.00
(Thurston et al., 1985)
P. fulvidraco
LC50
MORT
4
S, U
8.12
98.54
This study
R. chensinensis
LC50
GGRO
4
S, U
8.12
548.62
This study
(d)
4
(μg/L）
Table S3. Chronic toxicities, expressed as the maximum allowable toxicant concentration (MATC) or EC10 during chronic exposure
of aquatic organisms to PCP.
Species
Endpoint
Effect
Exposure (d)
Method
pH
Concentration (μg/L）
Reference
Ceriodaphnia dubia
MATC
PROG
14
R, U
7.90
158.00
(Hickey, 1989)
Daphnia carinata
MATC
PROG
14
R, U
7.90
354.00
(Hickey, 1989)
D. magna
EC10
PGRT
21
S, U
8.12
4.79
This study
Simocephalus vetulus
MATC
PROG
14
R, U
7.90
71.00
(Hickey, 1989)
Mesocyclops leuckarti
MATC
MORT
6
S, U
7.30
104.00
(Willis, 1999)
Macrobrachium superbum
MATC
SURV
21
R, M
7.24
12.00
(Jin et al., 2012)
Corbicula fluminea
MATC
SURV
21
R, M
7.24
70.00
(Jin et al., 2012)
Brachionus calyciflorus
EC10
HTCH
2
S, M
7.50
600.00
(Radix et al., 2000)
Soirodela polyrhiz
MATC
CHLO
10
R, M
7.24
350.00
(Jin et al., 2012)
Chlamydomonas reinhardtii
NOEC
PGRT
10
F, M
7.00
360.00
(Schafer et al., 1994)
Chlorella kessleri
EC10
ABND
2
S, U
8.00
8650.00
(Mostafa and Helling, 2002)
S. obliquus
EC10
GGRO
3
S, U
6.50
174.00
(Xing et al., 2012)
S.obliquus
EC10
GGRO
3
S, U
7.50
301.00
(Xing et al., 2012)
S. obliquus
EC10
GGRO
3
S, U
9.00
12440.00
(Xing et al., 2012)
Erythroculter ilishaeformis
MATC
GGRO
28
R, M
7.24
25.00
(Jin et al., 2012)
Mylopharyngodon piceus
MATC
GGRO
28
R, M
7.24
14.00
(Jin et al., 2012)
Plagiognathops microlepis
MATC
GGRO
28
R, M
7.24
14.00
(Jin et al., 2012)
Oncorhynchus mykiss
EC10
DBMS
30
F, M
8.30
60.00
(Besser et al., 2005)
Oncorhynchus mykiss
MATC
DWGT
30
F, M
8.30
51.00
(Besser et al., 2005)
Note: * Results from the present study; F-flow through; R-renewal; S-static; NR-not reported; U-not measured; M-measured; LC50-lethal concentration; EC10/EC50-effect
concentration for 10% and 50% of the population; MATC-maximum acceptable toxic concentration; NOEC-no observed effect concentration; MORT-mortality; IMBL-immobility;
GGRO-general growth；GGRT-growth rate；SURV-survival；WGHT-weight；CHLO-chlorophyll；HTCH-hatchability；ABND-abundance；PGRT-population growth rate;
DWGT-dry weight；DBMS-dry biomass
5
Table S4. Number of taxa of phytoplankton in various families occurring in Tai Lake a---from
historical survey.
Phyla
1960
1980
1987
2010
Chlorophyta
48
54
39
131
Aulacoseira
18
25
25
75
Cyanophyta
15
17
19
20
Chrysophyta
1
3
5
3
Xanthophyta
2
3
0
2
Cryptomonas
0
2
3
3
Pyrrophyta
2
4
3
8
Euglenophyta
5
6
3
36
Total
91
114
97
278
a
Note： (Ni and Zhu, 2005; Sun and Huang, 1993; Xu and Zhang, 2012)
6
Table S5. Number of species of aquatic macrophytes in several families found to be occurring in
Tai Lake during historical surveys b.
Phyla
1960
1981
1996
2002
Pteridophyta
4
4
4
4
Dicotyledonous
24
31
31
31
Monocotyledonous
38
31
39
40
Total
66
66
74
75
b
Note: (Liu et al., 2007; Nanjing Institute of Geography, 1965; Sun and Huang, 1993; Zhang and Qian, 1999)
7
Table S6. Number of taxa of zooplankton of several families found in Tai Lake during historical
surveys c.
Phyla
1980
1987
2007
Protozoa
41
22
13
Trochelminthes
42
30
34
Arthropoda
39
27
24
Total
122
79
71
c
Note: (Ni and Zhu, 2005; Sun and Huang, 1993; Zheng et al., 2007)
8
Table S7. Number of taxa in several families of benthic invertebrates identified during historical
surveys of Tai Lake d.
Phyla
1980
1987
2008
Coelenterata
1
1
0
Aschelminthes
11
0
0
Annelida
7
8
14
Mollusca
24
23
12
Arthropoda
25
27
14
Total
68
59
40
Note: d (Cai et al., 2010; Chen and Liu, 2003; Sun and Huang, 1993)
9
Table S8. Number of fishes in several families as determined during historical surveys of Tai
Lake e.
Order
1981
2006
Gadiformes
1
0
Anguilliformes
1
1
Clupeiformes
2
1
Cypriniformes
65
37
Siluriformes
10
4
Osmeriformes
4
4
Mugiliformes
2
0
Beloniformes
1
1
Cyprinodontiformes
1
1
Symbranchir
1
1
Scorpaeniformes
1
0
Perciformes
16
10
Pleuronectiformes
1
0
Tetraodontiformes
1
0
Total
107
60
Note: e (Chen and Liu, 2003; Sun and Huang, 1993; Zhu, 2004; Zhu and Liu, 2007)
10
Table S9. Fish species changed from 1980 to 2006 as determined during historical surveys of
Tai Lake f.
Species found in 1986
Species found in 2006
Acipenser sinensis
Macrura reetesii
Coilia ectenes
Coilia ectenes
Coilia ectenes taihuensis
Coilia brachygnathus
Coilia brachygnathus
Reganisalanx brachyrostratis
Protosalanx
hyalocranius
Protosalanx hyalocranius
Neosalanx tanghahkeii taihuensis
Neosalanx tanghahkeii
taihuensis
Neosalanx oligodontis
Neosalanx oligodontis
Anguilla japonica
Cyprinus carpio
Cyprinus carpio
Carassius auratus
Carassius auratus
Pseudorasbora parrva
Pseudorasbora parrva
Sarcocheilichtys siensis
Sarcocheilichtys siensis
Sarcocheilichtys
nigripinnis
Sarcocheilichtys nigripinnis
Abbottina rivularis
Abbottina rivularis
Abbottina fukiensis
Saurogobio dabryi
Saurogobio dumerili
Squalidus noteas
Paracanthobrama
guichenoti
Paracanthobrama guichenoti
11
Rhinogobio typus
Coreius heterodon
Gnathopogon argentatus
Gnathopogon sihuensis
Gnathopogon wolteisorffi
Hemibarbus maculatus
Hemibarbus maculatus
Hemibarbus labeo
Hemibarbus labeo
Aphyocypris chinensis
Elopichthys bambusa
Elopichthys bambusa
Opsariichthys uncirostris bidens
Squaliobarbus
curriculus
Squaliobarbus curriculus
Ochetobibus elongatus
Mylopharyngodon piceus
Mylopharyngodon
piceus
Ctenopharyngodon idellus
Ctenopharyngodon
idellus
Toxabramis swinhonis
Toxabramis swinhonis
Parabramis pekinensis
Pseudobrama simoni
Megalobrama
amblycephala
Megalobrama amblycephala
Megalobrame terminalis
Hemicculter leuciclus
Hemicculter leuciclus
Hemiculter bleekeri
Culter erythropterus
Culter erythropterus
Erythroculter
ilishaeformis
Erythroculter ilishaeformis
12
Erythroculter
mongolicus
Erythroculter mongolicus
Erythroculter dabryi
Erythroculter
Parapelecus argenteus
Parapelecus engraulis
Distoechodon tumirostris
Acanthobrama simoni
Plagiognathops microlepis
Xenocypris davidi
Xenocypris argentea
Acheilognathus
Acheilognathus gracilis
Acanthorhodeus macropterus
Acanthorhodeus
macropterus
Acanthorhodeus barbatutus
Acanthorhodeus
barbatutus
Acanthorhodeus tonkinensis
Acanthorhodeus
tonkinensis
Acanthorhodeus taenianalis
Acanthorhodeus chankaensis
Pararsilurus fangi
Rhodeus sinensis
Rhodeus ocellatus
Rhodeus light
Rhodeus light
Aristichthys nobilis
Aristichthys nobilis
Hypohthalmichthys molitrix
Hypohthalmichthys
molitrix
13
Sinilabeo decorus tungting
Myxocypriuus asiaticus
Cobitis taenia
Cobitis taenia
Botia xeaiithi
Botia wui
Paramisgurnus
dabryanus
Misgurnus mizolepis
Pararhychobdella
sinemsis
Misgurnus
anguillicaudatus
Misgurnus anguillicaudatus
Pseudobagrus
fulvidraco
Pseudobagrus fulvidraco
Pseudobagrus eupogon
Pseudobagrus nitidus
Leiocassis longirostris
Leiocassis ussuriensis
LeiocassisL albomargintus
LeiocassisL taeniatus
LeiocassisL adiposalis
Silurus asotus
Silurus asotus
Oryzias latipes
Hemirhamphus
intermedius
Hemirhamphus intermedius
Mugil cephalus
Mugil soiuy
Monopterus albus
Monopterus albus
14
Siniperca scherzeri
Siniperca chuatsi
Siniperca chuatsi
Siniperca kneri
Lateolabrax japonicas
Lateolabrax japonicus
Hypseleotris
swinhnonis
Hypseleotris swinhnonis
Odontobutis obscurus
Odontobutis obscurus
Odontamblyopus rubicundus
Ctenogobius giurinus
Ctenogobius giurinus
Ctenogobius cliffordpopei
Taenioides cirratus
Macropodus chinensis
Macropodus chinensis
Caltionymus olidus
Ophicephalus argus
Ophicephalus argus
Channa asiatica
Mastacembelus aculeatus
Trachidermus fasciatus
Cynoglessus graclfls
Cynoglossus trigrammus
Cynoglossus purpureomaculatus
Fugu obscurus
Fugu ocellatus
Total 107
60
Note: f (Zhu, 2004; Zhu and Liu, 2007)
15
Table S10. Information of sample sites in the most contaminated area in West Tai Lake.
Coordinates
Location
Sample ID
Sampling Date
N
E
Huangnian
HN0408
31°31.158’
120°00.978’
April 8, 2013
Huangnian
HN0726
31°31.158’
120°00.978’
July 26, 2013
Huangnian
HN1201
31°31.158’
120°00.978’
December 1, 2013
Fenshui
FS0408
31°29.513’
120°01.573’
April 8, 2013
Fenshui
FS0726
31°29.513’
120°01.573’
July 26, 2013
Fenshui
FS1201
31°29.513’
120°01.573’
December 1, 2013
Chendong
CD0408
31°19.345’
119°55.342’
April 8, 2013
Chendong
CD0726
31°19.345’
119°55.342’
July 26, 2013
Chendong
CD1201
31°19.345’
119°55.342’
December 1, 2013
Dapu
DP0408
31°19.074’
119°55.237’
April 8, 2013
Dapu
DP0726
31°19.074’
119°55.237’
July 26, 2013
Dapu
DP1201
31°19.074’
119°55.237’
December 1, 2013
16
Table S11. Acute toxicities of PCP to aquatic species inhabiting Tai Lake (pH = 7.8).
Species
Concentration (μg/L)
H. smolitrix
17.00
P. fulvidraco
77.94
Carassius auratus
90.70
Ictalurus punctatus
104.39
N. denticulate
120.06
Oncorhynchus mykiss
124.63
Plagiognathops microlepis
135.68
H. nobilis
143.00
Mylopharyngodon piceus
143.22
Erythroculter ilishaeformis
195.98
D. magna
210.02
Macrobrachium superbum
211.06
Lymnaea acuminata
211.89
Ceriodaphnia reticulata
216.40
Mesocyclops leuckarti
222.91
Simocephalus vetulus
242.36
Ceriodaphnia dubia
265.14
Ctenopharynodon idellus
290.68
Corbicula fluminea
346.73
R. chensinensis
433.91
Daphnia carinata
529.71
Chlamydomonas reinhardtii
736.98
Limnodrilus hoffmeisteri
792.79
Lemna minor
1374.88
Viviparus bengalensis
1459.04
Brachionus calyciflorus
1632.20
Soirodela polyrhiz
1688.45
S. obliquus
1841.21
Chironomus riparius
2060.72
Chlorella kessleri
29622.83
17
Table S12. Chronic toxicities of PCP to aquatic species inhabiting Tai Lake (pH =
7.8).
Concentration (μg/L)
Species
D. magna
3.79
Macrobrachium superbum
18.09
Mylopharyngodon piceus
21.11
Plagiognathops microlepis
21.11
Oncorhynchus mykiss
38.34
Erythroculter ilishaeformis
37.69
Simocephalus vetulus
65.98
Corbicula fluminea
105.53
Ceriodaphnia dubia
146.83
Mesocyclops leuckarti
150.04
Daphnia carinata
328.98
Soirodela polyrhiz
527.64
Chlamydomonas reinhardtii
647.10
Brachionus calyciflorus
747.57
S. obliquus
955.92
Chlorella kessleri
7470.48
18
Table S13. Acute-Chronic Ratios (ACR) of all species available.
Species
Acute Concentration (μg/L)
Chronic Concentration (μg/L)
Acute-Chronic Ratios
Final ACR
Oncorhynchus mykiss
Plagiognathops microlepis
Mylopharyngodon piceus
Erythroculter ilishaeformis
Daphnia magna
Macrobrachium superbum
Mesocyclops leuckarti
Simocephalus vetulus
Ceriodaphnia dubia
Corbicula fluminea
Daphnia carinata
Chlamydomonas reinhardtii
Brachionus calyciflorus
Soirodela polyrhiz
Scenedesmus obliquus
Chlorella kessleri
124.63
135.68
143.22
195.98
210.02
211.06
222.91
242.36
265.14
346.73
529.71
736.98
1632.20
1688.45
1841.21
29622.83
38.34
21.11
21.11
37.69
3.79
18.09
150.04
65.98
146.83
105.53
328.98
647.10
747.57
527.64
955.92
7470.48
3.25
6.43
6.79
5.20
55.43
11.67
1.49
3.67
1.81
3.29
1.61
1.14
2.18
3.20
1.93
3.97
3.75
19
Table S14. Chronic toxicities of PCP with ACR method.
Species
Daphnia magna
Hypophthalmichthy smolitrix
Macrobrachium superbum
Pelteobagrus fulvidraco
Mylopharyngodon piceus
Plagiognathops microlepis
Carassius auratus
Ictalurus punctatus
Neocaridina denticulate
Erythroculter ilishaeformis
Hypophthalmichthys nobilis
Oncorhynchus mykiss
Lymnaea acuminata
Ceriodaphnia reticulata
Simocephalus vetulus
Ctenopharynodon idellus
Corbicula fluminea
Rana chensinensis
Ceriodaphnia dubia
Mesocyclops leuckarti
Limnodrilus hoffmeisteri
Daphnia carinata
Lemna minor
Viviparus bengalensis
Soirodela polyrhiz
Chironomus riparius
Chlamydomonas reinhardtii
Brachionus calyciflorus
Scenedesmus obliquus
Chlorella kessleri
20
Concentrations (μg/L)
3.79
4.56
18.09
20.78
21.11
21.11
24.19
27.84
32.02
37.69
38.20
38.34
56.50
57.71
65.98
77.51
105.53
115.71
146.83
150.04
211.41
328.98
366.64
389.08
527.64
549.53
647.10
747.57
955.92
7470.48
Table S15. Acute toxicity of pentachlorophenol to nine aquatic species during in situ
incubations to determine the water effects ratio.
Species
H. smolitrix
P. fulvidraco
N. denticulate
H. nobilis
C. idellus
D. magna
Water
Duration
Endpoints
pH
Concentration (95% C.I.)
(μg/L)
Aerated water
4d
LC50
8.1
21.63 (18.64-26.63)
Huangnian
4d
LC50
6.9
69.24 (63.92-74.57)
Fenshui
4d
LC50
6.6
119.84 (103.86-135.82)
Dapu
4d
LC50
6.6
58.59 (50.60-66.58)
Chendong
4d
LC50
6.4
42.61 (34.62-53.26)
Aerated water
4d
LC50
8.1
98.54 (85.22-111.85)
Huangnian
4d
LC50
6.9
199.74 (170.44-231.70)
Fenshui
4d
LC50
6.6
229.04 (199.74-260.99)
Dapu
4d
LC50
6.6
125.17 (111.85-141.15)
Chendong
4d
LC50
6.4
170.44 (151.80-189.09)
Aerated water
4d
LC50
8.1
151.80 (135.82-173.11)
Huangnian
4d
LC50
6.9
298.28 (263.66-340.89)
Fenshui
4d
LC50
6.6
253.00 (223.71-287.63)
Dapu
4d
LC50
6.6
183.76 (154.47-218.38)
Chendong
4d
LC50
6.4
157.13 (141.15-175.77)
Aerated water
4d
LC50
8.1
181.10 (165.12-197.08)
Huangnian
4d
LC50
6.9
292.95 (258.33-330.24)
Fenshui
4d
LC50
6.6
596.56 (529.98-673.79)
Dapu
4d
LC50
6.6
231.70 (199.74-268.98)
Chendong
4d
LC50
6.4
319.58 (287.63-356.87)
Aerated water
4d
LC50
8.12
367.52 (351.54-386.16)
Huangnian
4d
LC50
6.92
719.06 (673.79-767.00)
Fenshui
4d
LC50
6.63
367.52 (351.54-386.16)
Dapu
4d
LC50
6.6
703.08 (652.48-759.01)
Chendong
4d
LC50
6.4
735.04 (703.08-772.33)
Aerated water
2d
LC50
8.1
450.08 (412.80-476.71)
21
R. chensinensis
L. hoffmeisteri
S. obliquus
Huangnian
2d
LC50
6.4
737.71 (636.50-857.55)
Fenshui
2d
LC50
6.3
764.34 (663.14-881.52)
Dapu
2d
LC50
6.9
713.74 (612.54-830.92)
Chendong
2d
LC50
6.5
641.83 (537.97-769.66)
Aerated water
4d
LC50
8.1
548.62 (503.34-599.22)
Huangnian
4d
LC50
6.4
588.57 (561.94-615.20)
Fenshui
4d
LC50
6.3
588.57 (561.94-615.20)
Dapu
4d
LC50
6.9
588.57 (561.94-615.20)
Chendong
4d
LC50
6.5
575.25 (540.63-612.54)
Aerated water
4d
LC50
8.1
884.18 (761.68-1028.00)
Huangnian
4d
LC50
6.4
2447.48 (2154.53-2780.38)
Fenshui
4d
LC50
6.3
2391.55 (2122.57-2695.16)
Dapu
4d
LC50
6.9
2684.51 (2442.15-2950.83)
Chendong
4d
LC50
6.5
2231.76 (1925.49-2585.97)
Aerated water
1d
EC50
8.1
1861.58 (1720.43-3542.06)
Huangnian
1d
EC50
6.4
4175.90 (3424.88-5089.38)
Fenshui
1d
EC50
6.3
4793.76 (4490.16-5116.01)
Dapu
1d
EC50
6.9
4290.42 (4002.79-4599.35)
Chendong
1d
EC50
6.5
4998.83 (4700.55-5315.75)
22
Table S16. The physical and chemical characteristics of samples of water.
Temp
Turbidity
Chl a
(NTU+)
(ug/L)
pH
Sample
(℃)
HN0408
17.06
6.4
38.4
3.9
HN0726
30.75
6.9
38.6
9.9
HN1201
10.30
6.7
58.2
5.7
FS0408
16.95
6.3
1.3
10.5
FS0726
27.68
6.6
53.0
1.1
FS1201
10.20
6.7
170.9
9.1
CD0408
15.73
6.5
217.5
95.4
CD0726
30.92
6.4
44.9
12.1
CD1201
9.10
6.9
38.4
13.3
DP0408
17.13
6.9
15.6
45.1
DP0726
31.56
6.6
41.4
11.3
DP1201
9.21
6.8
37.2
10.3
23
Table S17. Concentrations (μg/L) of inorganic elements in samples of water.
Sample
Cr
Mn
Cu
Ni
Pb
V
Fe
Co
Zn
As
Se
Ag
Ba
HN0726
0.37
2.02
0.94
0.9
0.07
0.09
15.27
0.02
1.71
0.04
0.02
0.01
0.1
HN1201
0.19
0.17
0.83
0.86
0.04
0.03
3.84
0.01
1.47
0.01
0.03
0.01
0.84
CD0726
0.23
2.14
0.83
0.86
0.08
0.1
19.77
0.02
1.64
0.03
0.03
0.01
1.28
CD1201
0.18
0.16
0.79
0.81
0.04
0.04
3.95
0.01
1.5
0.01
0.02
0.01
0.92
FS0726
0.26
1.35
0.84
0.83
0.05
0.05
8.53
0.01
1.545
0.02
0.02
0.01
0.6
FS1201
0.19
0.16
0.82
0.83
0.04
0.03
3.78
0.01
1.51
0.01
0.03
0.01
0.74
DP0726
0.38
1.91
0.87
1.02
0.09
0.1
18.82
0.03
3.06
0.03
0.02
0.01
1.13
DP1201
0.20
0.20
0.81
0.84
0.05
0.05
5.17
0.01
1.72
0.02
0.03
0.01
1.25
24
Figure S1. Species numbers of three taxonomic groups in Tai Lake
25
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