Science of the Total Environment 599–600 (2017) 721–731

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

A water quality management strategy for regionally protected water

through health risk assessment and spatial distribution of heavy metal
pollution in 3 marine reserves
Yinan Zhang, Chunli Chu ⁎, Tong Li, Shengguo Xu, Lei Liu, Meiting Ju
College of Environmental Science and Engineering, Nankai University, Jinnan District, Tianjin, China

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

• A watershed management method is

explored to assess the heavy metal pol-
lution and human health risk in water.
• Nemerow and USAEPA models were
used to evaluate the pollution and health
risk of three natural reserves in Tianjin.
• Cluster analysis and GIS can determine
the sequence and location of pollution
treatment.
• Reserves are subject to varying degrees of
pollution or health risks.
• A new perspective of water quality ori-
ented watershed management is advised
at the regional scale.

a r t i c l e i n f o a b s t r a c t

Article history: Severe water pollution and resource scarcity is a major problem in China, where it is necessary to establish water
Received 6 February 2017 quality-oriented monitoring and intelligent watershed management. In this study, an effective watershed man-
Received in revised form 7 April 2017 agement method is explored, in which water quality is first assessed using the heavy metal pollution index and
Accepted 28 April 2017
the human health risk index, and then by classifying the pollution and management grade based on cluster anal-
Available online 9 May 2017
ysis and GIS visualization. Three marine reserves in Tianjin were selected and analyzed, namely the Tianjin An-
Editor: D. Barcelo cient Coastal Wetland National Nature Reserve (Qilihai Natural Reserve), the Tianjin DaShentang Oyster Reef
National Marine Special Reserve (DaShentang Reserve), and the Tianjin Coastal Wetland National Marine Special
Keywords: Reserve (BinHai Wetland Reserve) which is under construction. The water quality and potential human health
Heavy metal Nemerow index risks of 5 heavy metals (Pb, As, Cd, Hg, Cr) in the three reserves were assessed using the Nemerow index and
USEPA model USEPA methods. Moreover, ArcGIS10.2 software was used to visualize the heavy metal index and display their
Clustering analysis spatial distribution. Cluster analysis enabled classification of the heavy metals into 4 categories, which allowed
GIS visualization for identification of the heavy metals whose pollution index and health risks were highest, and, thus, whose con-
Watershed management
trol in the reserve is a priority. Results indicate that heavy metal pollution exists in the Qilihai Natural Reserve and
in the north and east of the DaShentang Reserve; furthermore, human health risks exist in the Qilihai Natural Re-
serve and in the BinHai Wetland Reserve. In each reserve, the main factor influencing the pollution and health
risk were high concentrations of As and Pb that exceed the corresponding standards. Measures must be adopted
to control and remediate the pollutants. Furthermore, to protect the marine reserves, management policies must
be implemented to improve water quality, which is an urgent task for both local and national governments.
© 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author.
E-mail addresses: zhangyn2011@whu.edu.cn (Y. Zhang), chucl@nankai.edu.cn (C. Chu), xushengguo@mail.nankai.edu.cn (S. Xu), helenbooster@163.com (L. Liu),
jumeit@nankai.edu.cn (M. Ju).

http://dx.doi.org/10.1016/j.scitotenv.2017.04.232
0048-9697/© 2017 Elsevier B.V. All rights reserved.
722 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
1. Introduction
Environmental pollution by heavy metals has attracted much atten-
tion worldwide because they rapidly accumulate in the natural environ-
ment (Kavcar et al., 2009; Mahato et al., 2014; Tiwari et al., 2015;
Nguyen et al., 2016). Heavy metals in aquatic environments enter the
ocean by direct emissions or by surface runoff and can come from natu-
ral sources, such as geologic weathering and atmospheric inputs, or
from human activities, such as industrial and agricultural sewage dis-
charge (Bradl, 2005; Sharifi et al., 2016; Tiwari et al., 2016a, 2016b;
Tiwari et al., 2016a, 2016b; Tiwari et al., 2017). Furthermore, some
heavy metals such as mercury, cadmium, chromium, lead (Campbell
and Gailer), and metalloid arsenic can transform into persistent metallic
compounds with high toxicity (Cao et al., 2016). They are a major source
of water pollution and have long been considered critical contaminants
in aquatic ecosystems because of their toxicity, persistence, non-
degradability and bioaccumulation characteristics. (Page et al., 2014;
Spanopoulos-Zarco et al., 2014). Bioaccumulation of these compounds
in organisms' results in magnified toxicity along the food chain
(Chang et al., 2014), thereby threatening both aquatic ecosystems and
human health (Van Hook, 1979). Heavy metals can accumulate in the
adipose tissue and livers of humans and animals (Bhuiyan et al.,
2010), which adversely effects the nervous, circulatory, and immune
systems (Lauwerys, 1979; Straif et al., 2009). Moreover, some heavy
metals, such as Cadmium (Mielke and Reagan, 1998) and Chromium
(Bonsignore et al., 2016) can be carcinogenic when stored in the body
for long periods of time. Due to their damaging effects on the ecological
environment and in human health, it is necessary to include heavy
metal contamination in aquatic (Zhang, Qin et al. 2014).
Marine protected areas are part of intertidal or sub-tidal environ-
ments, and encompass the overlying water; other geographical features,
such as the coast, estuarine, wetlands, and islands; and all associated
flora and fauna. These environments have been protected by law
(Ervin et al., 2010) to conserve and protect marine biodiversity
(Gaines et al., 2010); enhance ecological functions(Hastings and
Botsford, 1999); reduce the decline of biomass of the oceans (O'Leary
et al., 2012); and to ameliorate the negative impacts of human
activities(Wells et al., 2007). Protected marine areas in China are divid-
ed into marine natural reserves, which are established to protect
cherished, primitive marine areas; and marine special reserves (China,
1998), which are established to protect marine ecosystems that are
used by people and to develop sustainable utilization practices for the
marine resources (Zeng et al., 2016). There are two national marine re-
serves in Tianjin: the Tianjin Ancient Coastal Wetland National Nature
Reserve and the Tianjin DaShentang Oyster Reef National Marine
Special Reserve. Another special reserve, known as the Tianjin Coastal
Wetland National Marine Special Reserve, is currently under construc-
tion. As an important trade port in northern China, Tianjin has a large
number of industrial, agricultural and fishery activities that utilize the
abundant marine resources in the area (Weizhen, 2016). These activi-
ties result in large amounts of heavy metals being discharged into the
aquatic environment (Zhang et al., 2016), thereby polluting the seawa-
ter and threatening the health of local people and the environmental
security in Tianjin's marine reserves (Zhang Qin and Mengxuan, 2015).
To meet the challenge of severe water pollution and resource scarcity,
water quality-oriented management and intelligent watershed manage-
ment are needed in China. It is a new and core watershed management
module of water quality-oriented management and intelligent water-
shed management for the water pollution control strategy of the 13th
Five Year planning in China (Zhang, Liang et al. 2014). The total pollutant
load control program currently implemented in China will be supple-
mented by the water quality target-oriented management to form the
framework for future watershed management (Sheng et al., 2013).
Existing research on water of marine reserves mainly focuses on surface
water quality assessment of lake, river, et al. For example, a study was
focused on the water quality prediction in Yuqiao reservoir by BP neural
network method (Zhao et al., 2007), Wang X et al. investigated the zoo-
plankton and water quality in Tuanbo reservoir (Wang et al., 2008), Cao
Z et al. studied the occurrence and distribution of polycyclic aromatic hy-
drocarbons in reclaimed water and surface water of Tianjin, including the
river of Haihe, Beiyun, Ziya, etc. (Cao et al., 2005). Integrated watershed
management should be explored to serve the watershed management
measures based on water quality monitoring and analysis. Therefore,
three marine reserves protected in Tianjin were selected for heavy
metal pollution assessment according to their water quality target. And
differentiated management measures for different protected marine re-
serves were explored according to clustered categories based on the
heavy metal pollution and health risk index.
Many studies assessing heavy metal pollution in marine reserves
concentrate on qualitative and quantitative evaluation of heavy metals
in sediments (Caeiro et al., 2005). These studies mainly compare moni-
toring data with water quality standards and then further analyze the
pollution sources and elucidate protection measures by assessing the
given results (Hambaryan, 2013), however, they lack adequate assess-
ment of heavy metals to which humans are easily exposed (Bonanno
et al., 2017). For example, Mohsen Nowrouzi et al. (Nowrouzi et al.,
2014) assessed heavy metal pollution in the sediments of the Iran
Halak biosphere reserve and found that the concentration of Al, Zn, Cu
and Cr were affected by pH and human activity. David Haynes et al.
(Haynes and Johnson, 2000) analyzed the changes in heavy metal con-
centrations from several sources, such as water, sediment, mangroves
and fish, in the Great Barrier Reef Reserve, and found that the primary
sources of heavy metal pollution were urban runoff, and agricultural
and industrial waste water emissions. Furthermore, many investiga-
tions regarding heavy metal pollution in the water and sediment of riv-
ers, groundwater, lakes, and estuaries have been conducted using
varying assessment techniques. For example, Nguyen Thi Thuong et al.
(Thuong, 2013) assessed the heavy metal pollution in the To Lich
River using the single factor index method for water analysis and the
geo-accumulation index and enrichment factor methods for sediment
analysis. Their results indicate that industrial discharge and the fertilizer
application were the main pollution sources; they further concluded
that suitable environmental protection regulations were necessary to
protect the river environment.
Evaluation methods for aquatic heavy metal pollution mainly in-
clude the single factor index method and the comprehensive index
method (Chen et al., 2011). The former is a simple method that com-
pares monitoring data to water quality standards (Gummadi et al.,
2015). The later considers multiple factors, which mainly include the
Nemerow index, grey correlation analysis method, fuzzy comprehen-
sive evaluation method, and principal component analysis (Sönmez et
al., 2013; Ali et al., 2016; Yang et al., 2016). The Nemerow index method
highlights the role of the maximum and the average index, which can
direct focus to the major pollutants (Yan et al., 2016). Grey correlation
analysis regards water as a grey box, and evaluates the mutual relation-
ship and influence of various factors on water (Tan et al., 2015). Fuzzy
comprehensive analysis classifies the degree of heavy metal pollution,
thus determining the extent of heavy metal pollution in the water (Gu
et al., 2016). Principal component analysis uses multidimensional fac-
tors, which allows for identification of the main contributors to environ-
mental pollution (Yalcin et al., 2016). In this study, the Nemerow index
method is used to analyze heavy metal pollution in Tianjin marine re-
serves because it is simple and flexible, and also reveals the conspicuous
role of the pollutants of higher concentration. The health risk assess-
ment aims to correlate human health with water pollution by relating
each quantitative index to human health (Li et al., 2014). Currently,
the most commonly used method is the human health risk assessment
model, as recommended by the U.S. Environmental Protection Agency
(USEPA) (Su et al., 2006). Many studies concentrate on assessing the
health risk of heavy metals in water, sediments, and fishes, but there
are few health risk assessments on heavy metals in marine reserve
water (Qi et al., 2014). For example, the USEPA model was used to
 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
determine that arsenic was the pollutant that posed the most risk to
humans in the Weihe River (Yang et al., 2015). This model was also
used to analyze trace metals in the drinking water of Izmir Province,
Turkey, where results showed that 90% of the population were exposed
to carcinogenic risk (Kavcar et al., 2009).The health risk of heavy metals
can be divided into non-carcinogenic risk and carcinogenic risk (Liang et
al., 2011), but due to the undefined toxicity value for carcinogenic risk,
only the non-carcinogenic risk is discussed in our study.
Geographic information system (Hu, Wan et al.) is a widely-used
method of data visualization (Hu, Wan et al.), which acts as a bridge be-
tween databases and management practices (Papadopoulou-Vrynioti et
al., 2014; Ghosh et al., 2015). With respect to environment manage-
ment, GIS is utilized as a technique to interpret and analyze environ-
mental damage, waste and pollution. It can also be used to assess and
plan land use for ecological and socio-economic needs (Alinejad et al.,
2016). This information can help policy makers to better understand
the environment situation, thus allowing for quicker decision making
(Tiwari et al., 2016a, 2016b). Research into the application of GIS to an-
alyze aquatic heavy metal pollution focuses mainly on the analysis and
visualization of pollution assessment results (Zazouli et al., 2014; Tiwari
et al., 2015). For example, geospatial mapping can be used to compli-
ment GIS data and to monitor and assess the different pollution types
(Arnous and Hassan, 2015). Additionally, GIS can be used in conjunction
with the Water Quality Index to assess the effects of different variables
on water quality. For example, Sadat-Noori, S M et al. used this method
to investigate the influence of land use and groundwater depth on
groundwater quality (Sadat-Noori et al., 2014). Thus, in this study we
use GIS to compliment the heavy metal pollution and human health
risk assessment results; thereby determining the geographical location
of heavy metal pollution and health risks, and demonstrating the
power of GIS for use in water quality management.
Few studies have investigated heavy metal pollution in reserve
waters, which are important ecosystems, worldwide. Specifically, the
marine reserves of Tianjin are impacted by industrial and agricultural
runoff; therefore, it is necessary to monitor and analyze the heavy
metal pollution and human health risk in these environments. The
purpose of this paper is to establish monitoring methods and provide
management guidelines for local governments to evaluate the degree
of pollution and health risk of heavy metal in marine reserve waters.
With this information, effective and scientifically-based measures can
be implemented to protect the reserves. By using GIS, we explore differ-
entiated management measures to improve water quality and alleviate
the health threat posed by heavy metals in the marine reserves of Tian-
jin province. The impact of pollution on the environment and human
health are equally important, thus both factors need to be considered
in water quality management; therefore, the Nemerow index and
USEPA model are employed to analyze heavy metals pollution and
human health risk, respectively. Clustering analysis was then employed
to group the results into 4 categories, in order to determine what com-
pounds caused the most pollution and posed the greatest health risks.
Although, these methods are commonly applied to water management
of various bodies of water, such as rivers, lakes and reservoirs, few arti-
cles focus on the perspective of regionally protected waters or water ba-
sins, as was done in this study. More importantly, the main goal of this
study is not to the improve current evaluation methods, but to create
a work-flow that identifies appropriate water pollution treatment op-
tions by investigating the relationship between heavy metal pollution
and health risk. Thus, the order in which the pollutants should be treat-
ed is determined more simply and conveniently, while at the same time
taking into consideration both the degree of heavy metal pollution and
the health risk, rather than simply trying to control a selected pollutant.
Moreover this study uses ArcGIS software (v. 10.2) to map the assess-
ment results using the spatial interpolation method, with different
colors expressing the degree of pollution. This allows for a more intui-
tive and convenient technique for identifying pollution of primary
concern. Through the above methods, we not only evaluate the state
723
of water pollution and health risks, but we can also identify what
heavy metals are problematic and where water quality management
is needed the most. Therefore, the objectives of this study are as follows:
(a) To evaluate heavy metal pollution of three marine reserve waters
in Tianjin;
(b) To assess the human health risk of heavy metals in marine re-
serve waters of Tianjin;
(c) To identify the connection between various metal pollution and
health risks using the cluster analysis method;
(d) To propose water quality management methods according to the
marine reserve assessment results.
2. Materials and methods
2.1. Site description
Heavy metals pollution and health risk were assessed for three na-
tional marine reserves of Tianjin (Fig. 1), which included one reserve
under construction. The Tianjin Ancient Coast and Wetlands National
Nature Reserve (Qilihai Natural Reserve) is situated in eastern Tianjin,
and encompasses the Ninghe District, the Jinnan District and part of
the Binhai New Area. The Qilihai Natural Reserve was approved as a na-
tional nature reserve in 1992 with the missions of protecting the shell
embankment and the oyster reef of rare ancient coastal relics and wet-
lands. It is a discontinuous reserve with an area of 359.13 km2, including
the core area (45.15 km2), the buffer area (43.34 km2), and the experi-
mental area (270.64 km2). Our study site was the core area, which rep-
resents the most important part of the Qilihai Natural Reserve and, as
such, human activity is prohibited by law. This area is located in the
Ninghe District, which is surrounded by 5 towns, 25 administrative vil-
lages, and has a population of 87,000 inhabitants. The soil type in the
Qilihai Natural Reserve is dominated by salinized fluvo-aquic soil and
wet fluvo-aquic soil (Lie, 2012). Many heavy metals, such as Cu and
Zn, in the reserve sediment exceed the soil background values of both
Tianjin and China (Ji-Guo et al., 2013). Qilihai Wetland Reserve, a semi
enclosed lagoon, relies on external water supplementation (Sun et al.,
2015). Most of the residents depend on the wetland resources to
make a living through industrial, agricultural, fishery, and tourism activ-
ities. This has resulted in a decrease in the natural wetland area, an in-
crease in the aquaculture area, and a polluted aquatic environment.
Both of the DaShentang Reserve and the BinHai Wetland Reserve are
located in the Bohai Bay, which is a semi-closed continental shelf mar-
ginal sea (Gao and Chen, 2012). The Bohai Sea is mainly affected by
monsoon conditions, which causes seasonal changes in wind and
wave direction (Zou et al., 2011). Due to abundant marine resources
and an excellent natural port, the coast of Bohai Bay is densely populat-
ed, resulting in a large amount of pollution being discharged into the
ocean. Moreover, the local river flow has decreased, which has adverse-
ly affected the marine environment (Hu et al., 2005). The Tianjin
DaShentang Oyster Reef National Marine Special Reserve (34 km2) is lo-
cated in the southern region of Tianjin Binhai New Area, and consists of
the Key Protected Area (16.93 km2), Ecology and Resource Restoration
Area (8.87 km2), and the Moderate Developing Area (8.61 km2). The
DaShentang Reserve was established as a national marine special re-
serve in 2012, with the aim of recovering the ecosystem and protecting
the living oysters and oyster reef resources, which are situated primarily
in the northeast and southwest parts of the Key Protected Area. There is
only one village near the DaShentang Reserve; however, some industri-
al and fishery activities exist there, such as the BeiJiang Power Plant and
the HanGu Industrial Park. Furthermore, tourist attractions have been
built along the reserve coastline, such as the Coastal Tourist Resort
and Hangu Binhai Aircraft Carrier Park. In addition, the Centre Fishing
Port is the primary aquatic product processing center and yacht indus-
try center in northern China, consisting of 14 berths and having the
throughput capacity of 17 million tons annually. These industries
724 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
Fig. 1. The location map and monitoring points in the three marine reserves.
produce enormous economic benefits for Tianjin, but they also nega-
tively impact the DaShentang marine environment by discharging
wastewater and exploiting marine resources.
The Tianjin Coastal Wetland National Marine Special Reserve is cur-
rently under construction. As a national marine reserve, it aims to pro-
tect the marine ecosystem and aid in the strategic development of a
sustainable marine economy in Tianjin. The BinHai Wetland Reserve
(76.33 km2) encompasses the southern tip of Tianjin, the southern por-
tion of the NanGang Industrial Zone, and the eastern MaPengkou coast-
line, and includes both terrestrial and marine areas. There are two
villages, MaPengkou and New MaPengkou, that are associated with
the BinHai Wetland Reserve. The residents make their living in the fish-
ing, marine breeding, and salt industries. These practices have caused
some pollution of the marine reserve; however, the greater contributors
stem from other projects and industries, such as the MaPengkou Off-
shore Wind Farm, built in 2011, which consists of 88 wind turbines
and has a total installed capacity of 132. Furthermore, the NanGang In-
dustrial Zone, which borders the reserve, supports several industries, in-
cluding manufacturing, warehousing and logistics, marine chemical,
and ecological fisheries. Both of these projects, along with development
of the tourism and real estate industry around the reserve, have
Table 1
The monitoring information of three Tianjin marine reserves.
Marine reserve Index Monitoring time
The Qilihai Natural Reserve 2014.5–6
The DaShentang Reserve 2014.9
The BinHai Wetland Reserve 2014.10
Pb, As, Cd, Hg, Cr
produced large economic benefits to local inhabitants, but have ad-
versely affected the BinHai Wetland Reserve ecosystem.
2.2. Sampling and analysis
Five heavy metals (Pb, As, Cd, Hg, and Cr) were selected for assess-
ment because they are non-essential elements for organisms and have
a strong toxicity to human (Amiard et al., 1987; Campbell and Gailer,
2016). They are also the most commonly assessed heavy metals for pol-
lution and health risk assessment (Chowdhury et al., 1997; Xie et al.,
2010; Pan et al., 2014). Water samples were monitored in three marine
reserves in 2014, although the monitoring months were different in
June, September and October which are all wet seasons in Tianjin
(Table 1), so the assessment results are comparable. All the sample col-
lection, management, and analysis methods in ocean were executed ac-
cording to Specification for offshore environment monitoring (HJ 442-
2008) in the DaShentang Reserve and the Binhai Wetland Reserve sea
water; and the sampling and monitoring method of terrestrial water
body were executed according to Surface water environmental quality
standard (GB3838-2002) in the Qilihai Wetland Reserve and the Binhai
Wetland Reserve fresh water. Monitoring data from the three marine
Monitoring points Water quality Standard
24 Fresh water Surface water environmental quality standard (GB3838-2002)
I
22 Sea water Seawater quality standard (GB3097-1997)
I
35 Fresh water (GB3838-2002)
II
Sea water GB3097-1997
II
 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731 725

reserves were provided by the Tianjin Ancient Coast and Wetland The exposure assessment is calculated as follows:
National Nature Reserve Management Office, which is a national admin-
istrative organization responsible for the protection and management of IR  EF  ED
CDIin ¼ C i  ð3Þ
Tianjin national natural reserves. So the data used in this paper is truly BW  AT
reliable. The specific monitoring sites are shown in Fig. 1, with more de-
SA  Kp  ET  EF  ED  CF
tails provided in Table 1. CDId ¼ C i  ð4Þ
BW  AT
2.3. Assessment methods where CDIin (μg/(Kg day)) refers to the chronic daily intake through in-
gestion of water and CDId (μg/(Kg day)) refers to the chronic daily intake
2.3.1. The Nemerow index method through dermal absorption; other parameters can be seen in Table 2.
The Nemerow index is one of the most frequently used methods to In this study, non-carcinogenic risks were assessed using the hazard
calculate the comprehensive pollution index (Jie et al., 2012). This quotient (HQ). The total non-carcinogenic risk of each heavy metal was
method first calculates the single factor index (Pi), then obtains the expressed as a hazard index (HI) in two exposure ways, which are
average value of Pi, and, finally, uses the maximum index value and defined as:
the average value to calculate the composite index (Pn), as per the
following formula: CDIin
HQ in ¼ ð5Þ
RfDin
P i ¼ C i =Si ð1Þ
CDI d
sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi HQ d ¼ ð6Þ
2 RfDd
P i þ P i max 2
Pn ¼ ð2Þ
2 RfDd ¼ RfDin  ABSg ð7Þ

where Pi represents the single factor index that refers to the exceeding
multiple of each index. Pn represents the composite index, which indi-
cates the degree of heavy metal pollution in the water. Ci represents
the measured concentration of the 5 heavy metals. Si represents the
standard value of every heavy metal, whose values are different in
each reserve, as shown in Table 4. Pi represents the average value of
Pi, and Pimax is the maximum value of Pi. Thus, Pn reflects the interaction
between the average pollution level and the maximum pollution factor.
Moreover, the Nemerow index method divides water quality into three
categories where a Pn b0.7 represents uncontaminated water, 0.7 ≤ Pn
≤ 1 signifies that the water is under the threat of contamination, and a
Pn N 1 represents heavily contaminated water (Liu et al., 2015).
2.3.2. Human health risk assessment
The human health risk assessment, as calculated by the USEPA risk
assessment model, is a 4-step process involving data collection and
analysis; exposure assessment; toxicity assessment; and risk character-
ization (US Environmental Protection Agency, 2013). Exposure assess-
ment involves calculating the daily exposure value of the human body
to heavy metals. The main exposure pathways include direct ingestion,
inhalation and dermal absorption (Drew et al., 2006; Koki et al., 2015;
Mahato et al., 2016). In this study, exposure assessment was conducted
using the ingestion and dermal pathways because they are the two pri-
mary modes of heavy metal exposure from water sources (EPA, 2004).
HI ¼ HQ in þ HQ d ð8Þ
where HQin is the hazard quotient through ingestion of water and HQd is
the hazard quotient through dermal absorption. The other parameters
can be seen in Table 2. This assessment method divides health risks
into two categories, where HI b 1 means that the tested metals have lit-
tle adverse health effects on local residents and HI ≥ 1 indicates a higher
probability of adverse health effects.
2.3.3. Cluster analysis
Cluster analysis refers to the grouping of similar objects from data
sets (Muller, 1969) that have used different analytical techniques
(Guan et al., 2014). In this study, cluster analysis was used to classify 5
heavy metals into 4 groups, thereby distinguishing the degree of
pollution and health risks of each tested metal (Table 3). This allows
for investigation into the relationship between the tested metals and
identification of the metal groups (Eq. (9)) whose presence in the
environment requires immediate attention due to their high degree of
pollution and health risk. Here, we define a polluted environment (P)
if the value of Pn exceeds 1, and an unpolluted environment (UNP) if
Pn is below 1 (Papadopoulou-Vrynioti, Alexakis et al.). We classify
health risks (HR) in water when the value of HI exceeds 1; otherwise
there is no health risks (NOHR). Thus, the 5 heavy metals can be divided
into 4 categories as follows:

Si ¼ ðPni ; HIi Þ ð9Þ

Table 2
The parameters of exposure assessment for Tianjin marine reserves.

Parameter Meaning Value Unit 2.3.4. Spatial analysis

IR Ingestion rate 2.2 L/day Based on the assessment results of Pn and HI in the three marine re-
EF Exposure frequency 365 day/year serves, we used the Spatial Analyst module of ArcGIS (v. 10.2) to achieve
ED Exposure duration 70 year
BW Body weight 60 kg
AT Average time 365 × 70 day
SA Skin-surface area 18,000 cm2 Table 3
Kp Permeability coefficient Cr:0.002 cm/h The 4 categories in water as determined by cluster analysis.
Others: 0.001
ET Exposure time 0.58 h/day HI
CF Conversion factor 1000 L/cm3
Pn ≥1 b1
RfDin Reference dose of heavy Pb: 1.4; As:0.3; Cd: 0.5; μg/(Kg day)
metals through ingestion Hg:0.3; Cr:3 ≥1 Existence of heavy metal pollution Existence of health risk without the
ABSg Gastrointestinal absorption Pb: 0.3; As:1; Cd: 0.05; – and health risk (P-HR) presence of heavy metal pollution
factor Hg:0.07; Cr:0.025 (UNP-HR)
b1 Existence of heavy metal pollution No heavy metal pollution or health risk
The data references above are from (EPA, 2004; Kavcar et al., 2009; USEPA, 2010; Yang et
without health risk (P-NOHR) (UNP- NOHR)
al., 2015).
726 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731

spatial visualization. The spatial interpolation of Pn and HI at all moni- Table 5

toring points were completed using the inverse distance weighted The values of Pn and HI of the three marine reserves in Tinajin.

method and the spatial distribution maps of Pn and HI. This analysis Marine The Qilihai Natural The DaShentang The BinHai Wetland
was performed according to the interpolation results, with different reserves Reserve Reserve Reserve
colors representing the degree of heavy metal pollution and health risk. Pn Maximum 3.21 7.62 0.32
Minimum 1.48 0.23 0.09
3. Results Average 2.40 2.02 0.15
HI Maximum 3.99 0.83 2.72
Minimum 1.89 0.12 0.71
3.1. Heavy metal pollution assessment Average 2.50 0.35 1.07

The heavy metals concentrations of Pb, Cd and Cr have exceeded the

first grade of the surface water quality standards (GB3838-2002) in the in the NO.1 monitoring site of the Key Protected Area and highlights
Qilihai Natural Reserve (Table 4, Table 5). Moreover, levels of Cd and the seriousness of the pollution. Other sites exceeding the standard
Cr exceed the standards at almost all monitoring sites. The maximum ranged from Pis of 2 to 6, thereby inflating the overall Pb concentration
value of Cr was measured in the East Sea reservoir, with other high far beyond the limit in the DaShentang Reserve. The Hg concentration
values detected in the West Sea fishpond. The maximum value of Cd exceeded standards at three monitoring points, two of which were in
was measured in the Bird Island of East Sea. Similarly, the monitoring the Key Protected Area. Again, the maximum value (1.7) was measured
points with which Pb concentrations exceeded standards were also lo- in the NO.1 monitoring site, and resulted in the largest Nemero index of
cated in the above two positions, which are highly influenced by 7.62. Moreover, within the DaShentang Reserve, the Pn values decreased
human activities. The West Sea fishpond is an aquaculture area for from north to south, and also from west to east (Fig. 2). The high Pn in
fish, shrimp, and crab. These activities can lead to water pollution, the north of reserve might be caused by Pb leakage from batteries and
such as eutrophication and heavy metal contamination (Tao et al., cables at the BeiJiang Power Plant; whereas the high Pn in the east
2011). The excess of heavy metals may also be associated with high might be caused by oil spills from fishing and sightseeing vessels origi-
levels of the compounds in the sediment or with the use of heavy nating from the Centre Fishing Port and tourist spots (Deng et al., 2017).
metal-containing food and medicines (Xu et al., 2014). The Nemerow In addition, the pollution may be exacerbated by coastal industry
index (Pn) values of all monitoring sites in the Qilihai Natural Reserve
core area exceeded 1, indicating the seriousness of the heavy metal pol-
lution; therefore, measures must be taken to recover this area as soon as
possible. The maximum Pn value was 3.21, which was detected in the
East Sea reservoir, with the single factor index values (Pi) of Pb, Cr,
and Cd also exceeding 1; other highly polluted monitoring points
were situated in the West Sea fishpond and the Bird Island of East Sea.
The outcome of Pn indicates that human activity seriously affects and
destroys the aquatic environment of the Qilihai Wetland reserve core
area. In a word, the heavy metal pollution seen in the reserve far ex-
ceeds the water quality requirements of the nature reserve, and the in-
flux of pollution needs to be strictly controlled.
The index of Pb and Hg in the DaShentang Reserve exceeded the nor-
mal values, with concentrations being higher than that of the first grade
seawater quality standard (GB3097-1997). The Pi index of Pb was N 1 in
73% of the monitoring sites. The maximum value (10.47) was detected

Table 4
Contents of heavy metals in water of the three marine reserves from Tianjin(μg/L).

Marine reserves Pb As Cd Hg Cr

The Qilihai Natural GB3838-2002 10.00 50.00 1.00 0.05 10.00

Reserve I grade
standard
Maximum 30.60 25.60 3.80 0.016 42.10
Minimum 0 8.40 1.40 0.001 2.80
Average 10.20 13.30 2.60 0.006 23.80
The DaShentang Reserve GB3097-1997 1.00 20.00 1.00 0.05 5.00
I grade
standard
Maximum 10.47 6.55 0.42 0.09 1.64
Minimum 0.04 0.47 0.02 0 0
Average 2.69 2.10 0.11 0.02 0.46
The BinHai Wetland GB3838-2002 10 50 5 0.05 50
Reserve II grade
(fresh water) standard
Maximum 1.11 22.02 0.19 0.008 0.86
Minimum 0.19 6.04 0.006 0 0.48
Average 0.40 10.31 0.038 0.0008 0.60
The BinHai Wetland GB3097-1997 5 30 5 0.2 10
Reserve II grade
(sea water) standard
Maximum 0.51 6.61 0.05 0.01 0.93
Minimum 0.11 5.68 0.02 0 0.43
Average 0.23 6.29 0.03 0.0009 0.56
Fig. 2. The outcome of Pn in the three marine reserves.
 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
Fig. 3. The outcome of HI in the three marine reserves.
emissions, atmospheric emissions, and heavy metals in marine sedi-
ments (Zheng and You, 2013).
All marine indicators in the BinHai Wetland Reserve were in accor-
dance with the second grade of Seawater quality standard (GB3097-
1997) and the fresh water complied with the second grade of surface
water quality standards (GB3838-2002), which indicates that the BinHai
Wetland Reserve wasters are not polluted by heavy metals. All
Nemerow indices were lower than 0.7 (ranging from 0.09 to 0.32);
however, the Pn values of terrestrial fresh water were generally greater
than the Pn values of seawater, demonstrating that the seawater quality
was better than the fresh water quality. These results remind us that we
should protect water quality from development projects in future.
3.2. Human health risk assessment
All hazard index (HI) values in the Qilihai Natural Reserve core area
were higher than 1, indicating a high non-carcinogenic hazard. The
Table 6
the cluster analysis group in the three marine reserves in Tianjin.
Marine reserves Pb
The Qilihai Natural Reserve (2.27,0.26)
The DaShentang Reserve (7.64,0.07)
The BinHai Wetland Reserve(fresh water) (0.08,0.01)
The BinHai Wetland Reserve(sea water) (0.08,0.006)
727
maximum value (3.99) was detected in the ChaoBaixin River. Other ele-
vated monitoring points were located in the West Sea fishpond, where
Pn values were higher than 3. For all of the 5 tested heavy metals, the haz-
ard quotients through dermal absorption (HQd) were lower than the haz-
ard quotient through ingestion of water (HQin); for example, the maximal
HQd value of Hg is 1.33E-04, and the maximal HQd value of all metals is 0.2
from Cr. However, the hazard quotient through ingestion of water were
not so. All HQin values of As exceeded 1 at all monitoring sites, directly
resulting in HI values higher than 1, and suggesting that As may threaten
the health of the residents. Furthermore, the maximum HQin of Pb was
0.8, which had a strong effect on HI. The HQin values of Hg were smallest
among the 5 tested metals. These data suggest that the health risks asso-
ciated with Cd, Cr, Pb and Hg may be minimal because their concentra-
tions were below 1, especially with respect to Hg. Conversely, the health
risk assessment indicated that As is the most important pollutant and
public health hazard in the Qilihai Wetland Reserve, and needs to be con-
trolled for the purpose of the public safety.
The HI values of all monitoring sites were lower than 1 in the
DaShentang Reserve, and ranged from 0.12 to 0.83, thus demonstrating
that heavy metals in reserve are not likely to threaten local residents.
The HQ values of the 5 tested heavy metals were low for both the dermal
absorption and the ingestion pathways. The maximum value came from
As, which accounted for a large proportion of the HI. HI values in the
northern and central sections of the DaShentang Reserve were lower
than in the southern region, and an obvious stratification can be seen
(Fig. 3). The HI values in the Key Protected Area were lower than 0.25, in-
dicating that little health threat to the local population existed. The HI
values for the Moderate Developing Area ranged from 0.7 to 0.83. Because
some of these values are close to 1, continued monitoring and analysis is
needed to ensure that the standard level is not exceeded, which would be
harmful to human health. Overall data suggests that the DaShentang Re-
serve posed little threat to the health of local residents.
The hazard index in the BinHai Wetland Reserve (Fig. 3) ranged from
0.71 to 2.72, indicating that some monitoring sites in the reserve existed
health risks. The sites in which the HI values exceeded 1, including the
maximum value, were mainly located in the terrestrial fresh water
area. The highest values were located primarily in the southwest terres-
trial areas, including in MaPengkou Village. Only one seawater monitor-
ing site exceeded 1, thus indicating that the human health risk was
lower in seawater than in fresh water. The HQd of the 5 tested metals
were low, showing little health threat to the local population through
dermal absorption. However, the HQin of As exceeded 1, thereby leading
to higher HI values.
3.3. Cluster analysis
In this study, the Pn and HI values of each tested metals were classi-
fied (Table 6, Fig. 4, Fig. 5, Fig. 6). Control of the yellow, orange, and red
labeled metals is of primary concern, as their index was over 1. In the
Qilihai Natural Reserve core area, As is categorized as UNP-HR; whereas
Cr, Cd and Pb are categorized as P-NOHR. If improvement of water qual-
ity is the priority, management of these four metals could be accom-
plished together; however, if control of these 4 metals with respect to
human health protection is the priority, As should be of primary con-
cern. In the DaShentang Reserve, Hg and Pb should be targeted for con-
trol as they are categorized as P-NOHR; the high Pn value of Pb makes its
control especially important. Within the fresh waters of the BinHai
As Cd Hg Cr
(0.41,1.63) (3.27,0.21) (0.24,0.001) (3.42,0.71)
(0.24,0.26) (0.31,0.008) (1.32,0.002) (0.24,0.008)
(0.34,1.27) (0.03,0.003) (0.11,0.0003) (0.015,0.008)
(0.22,0.77) (0.008,0.003) (0.02,0.0001) (0.08,0.009)
728 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
Fig. 4. The cluster analysis group in the Qilihai Wetland reserve.
Wetland Reserve, the only metal of concern is As because of its high haz-
ard index. There was neither heavy metal pollution nor health risk in the
BinHai Wetland reserve seawater; thus, there is no need to reduce the
concentrations of the tested metals here.
4. Discussion
4.1. Control sequence of heavy metals
This study used classification and ArcGIS interpolation results to de-
termine the order in which control and remediation of heavy metal
should be undertaken. First, by using cluster analysis results, the
heavy metals were divided into four categories. Priority control shall
be given to the H-HR category, as it signifies both a high health risk
and heavy metal pollution. The following categories are UNP-HR and
P-NOHR, as they both possess an index value over 1. When prioritizing
these two categories, we argue that priority should be given to the un-
polluted-health risk category (UNP-HR), in an effort to ameliorate im-
mediate health risks to the local population. Alternatively, we can
judge the control sequence of these two categories according to the
order of the numerical values. Meanwhile, UNP-NOHR represents a
heavy metal that does not require control. More significantly, we can
control and recover all the categories with exceeding values together,
or we can prioritize the metals in a given category by their numerical
values. The resulting interpolation map displays the outcomes using
Fig. 5. The cluster analysis group in the DaShentang reserve.
Fig. 6. The cluster analysis group in the BinHai Wetland reserve.
descriptive colors to indicate sites that require controlling (i.e.: sites
where the Pn or HI exceed 1 are labeled as red and yellow). In addition,
priority should be given to the heavily polluted areas (red color) of con-
taminated sites.
Analysis shows that all the Pn and HI values exceeded normal stan-
dards in the Qilihai Natural Reserve core area, which suggests significant
heavy metal pollution and potential health risk. This contradicts the
purpose of the reserves, which is to protect the environment from dam-
age. Therefore, local governments should take measures to control
heavy metal pollution and repair the environment within the Qilihai
Natural Reserve core area. As, Cr, and Cd are in most need of urgent re-
mediation as the HI value of As, and the Pn values of Cr and Cd exceed
standards at every monitoring point. Pb should be controlled next be-
cause Pn values exceed standards in some monitoring points. High Pn
and HI values were mainly located in the West Sea fishpond, Bird Island
of the East Sea and the East Sea reservoir. Thus, repair and protection
should start with As, Cr, Cd and Pb in these areas, followed by gradual
remediation of other contaminated areas. Although the DaShentang Re-
serve did not pose a threat to human health, it was beset by heavy metal
pollution in the north and east regions, especially in the NO.1 monitor-
ing points of the Key Protected Area. Priority control of heavy metals
should focus on Pb, followed by Hg, due to their high Pn values. There-
fore, in order to quickly restore the water environment, the local gov-
ernment should concentrate on removal of Pb and Hg in the northern
and eastern areas of reserve. The heavy metal pollution of the BinHai
Wetland Reserve is not serious; however, priority governance should
be given to As in terrestrial fresh water, especially MaPengkou Village.
4.2. Management and measures
The Regulations of the People's Republic of China on Nature Reserves
and the Administration Regulations of marine natural reserves prohibits
all activities that could potentially damage the core area of nature re-
serves, or reduce their ecological quality; therefore, the presence of
heavy metals that exceed standard values is not consistent with the
management requirements of the Qilihai Natural Reserve core area. In
order to achieve the standards outlined in GB3838-2002, control and re-
covery measures are required to reduce heavy metal concentrations in
the Qilihai Natural Reserve core area; for example, regulation and con-
trol of pollutant sources (Wang et al., 2015); and remediation of the
water using techniques appropriate to the given wetland type and the
water characteristics. (Mitsch et al., 2015). Moreover, the local
 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
government should prohibit any human activities within the core area,
such as fishing, agriculture and tourism; these activities can be diverted
out of the Qilihai Wetland Reserve and into the surrounding regions of
Bird Island and Tianjin Qilihai Wetland Park, which is also beautiful nat-
ural environment. Moreover, the dispersed inhabitants around the core
area should also be moved to a specially constructed eco-town (Zuo and
Yan, 2012).
With respect to the DaShentang Reserve and the BinHai Wetland Re-
serve, the Administration Measures of Special Marine Reserve stipulates
that protection of special marine reserves is of first priority, after
which moderate development is allowable. It also prohibits construc-
tion activities that are unrelated to protection in the Key Protected
Area; however, proper use of marine resources under the premise of en-
suring the safety of marine ecosystems in the Moderate Developing
Area is allowable. Moreover, within the Ecology and Resource Restora-
tion Area, appropriate artificial ecological remediation and restoration
measures can be undertaken to restore the marine ecology, resources,
and key habitats according to scientifically-based techniques. This
study found that heavy metal pollution and health risks exist in two of
Tainjin's marine special reserves. These ecosystems need to be repaired
and protected, especially in the DaShentang Reserve Key Protected Area
and in the BinHai Wetland Reserve. In addition, ecological breeding and
eco-tourism industries should be encouraged to operate without
harming the original ecosystem. It is noteworthy that the water quality
of the BinHai Wetland Reserve was much better than the second grade
of Surface water environmental quality standard and Seawater quality
standard, even better than the first grade of these two standards, there-
fore we suggest that it is necessary to improve its water quality to first
grade of corresponding standards in order to avoid the destruction of
their existing good environmental quality. Moreover, the BinHai Wet-
land Reserve should consist of a key protected area, an ecology and re-
source restoration area, and a moderate developing area, similar to the
DaShentang Reserve, for better protection and management.
It is very important to unify management from the regional perspec-
tive because improvement of the overall water quality is the actual goal
of water quality protection. Furthermore, the unified water manage-
ment of a region is very convenient, as it allows for one set of laws
and strategies and their synchronous implementation. In addition,
water pollution control requires macro-policy support. For national nat-
ural reserves, some measures can be taken simultaneously to protect
the water environment. First, local government should formulate a rel-
evant management system to identify what human activities cannot be
conducted within the reserve, and where more protection is needed.
Second, the government should construct infrastructure and protection
facilities to protect the natural reserves (Carpenter et al., 2009). Third,
the government should establish a continuous water quality monitoring
system for the purpose of monitoring and analyzing the water quality
and the health status of protected areas. Moreover, the government
should strengthen the publicity and education of local people, in order
to stress the importance of protected areas to the ecosystems' health
and biodiversity, and teach residence how to avoid damaging the re-
serves' environment and resources in daily life. Only by increasing the
awareness of residents can we achieve long-term protection of the re-
serve environment. In addition, the protection and management of
aquatic environments should not be limited to nature reserves or cer-
tain regions. Due to the mobility and connectivity of water, it should en-
compass the entire drainage basin; this would not only allow for control
of pollution in a specific water, but also prevent the flow and diffusion of
pollution from various sources.
5. Conclusion
The objectives of this study were to assess the water quality and po-
tential health risks in three marine reserves in Tianjin, and propose rea-
sonable management strategies to ameliorate pollution and health
concerns. To that end, heavy metal pollution was assessed using the
729
Nemerow index method, the risk to human health was assessed with
the USAEPA model, and a cluster analysis method was used to classify
the assessment results of the two aforementioned methods. According
to the results, the highest heavy metal pollution was found in the Qilihai
Natural Reserve core area, followed by the DaShentang Reserve, and
then the BinHai Wetland Reserve. Alternatively, the highest degree of
potential human health risk was identified in the Qilihai Natural Re-
serve core area, followed by the BinHai Wetland Reserve and then the
DaShentang Reserve. This assessment highlights the adverse effects
that human activities have on the aquatic environment in the Tianjin
marine reserves. The most intensive human activities are situated
around the Qilihai Natural Reserve, with less anthropogenic influences
associated with the other two national marine reserves. Results also re-
veal that As has the greatest impact on health of local residents around
the Tianjin reserves, whereas Pb pollution was the highest of all the test-
ed heavy metals; therefore, control and remediation these two metals is
of utmost importance. Sources of excessive heavy metal contamination
mainly came from agriculture, industry, fisheries, tourism and ship oil
spills around the marine reserves; however, a more in-depth investiga-
tion into the specific pollution sources is warranted. We have proposed
ways to improve water quality for the marine reserves, such as reducing
human activities, and strengthening governmental management, pub-
licity and education. However, these recommendations should be car-
ried out according to the environmental quality characteristics of the
different reserves.
As an important ecosystem, more attention and proper protection
should be given to marine reserves. The aim of this paper is to provide
scientific assessment methods to analyze and evaluate heavy metal pol-
lution and health risk in marine reserves, and to gain the attention of
local governments and stakeholders. The two methods used in this
paper are not complex, but can truly reflect the state of heavy metals
in water. We can easily determine which metals, and which areas, re-
quire priority remediation by using the cluster analysis and interpola-
tion map. In short, the methods and ideas of this paper are very
effective and convenient in assessing heavy metal pollution and health
risk. They also allow for prioritization of pollutants that are most in
need of control. However, it should be noted that some limitations
exist in this study. First, the data were sampled only during the 2014
wet season, which increases the assessment uncertainty. Second, due
to the lack of data, we did not assess the carcinogenic risk, which may
downplay the results of the human health risks. Third, by only assessing
5 heavy metal species, the state of heavy metal pollution in the reserves
cannot be fully defined. Thus, in order to more comprehensively reflect
the status of heavy metals in marine reserves, future studies should
allow for longer continuous monitoring periods, include more heavy
metal categories, and calculate the carcinogenic risk. In addition, future
research should also focus on applying this method to water quality
management of the river basin, and using this method to identify the
main factors affecting the water quality and the relationship between
heavy metals.
Acknowledgements
The authors would like to acknowledge the “National Science &
Technology Pillar Program of China” (2015BAJ01B03) for the
funding support. The authors would also like to thank the editors
and anonymous reviewers for their insightful comments and
suggestions.
Appendix A. Supplementary data
Supplementary data associated with this article can be found in
the online version doi: http://dx.doi.org/10.1016/j.scitotenv.2017.
04.232. These data include the Google maps of the most important
areas described in this article.
730 Y. Zhang et al. / Science of the Total Environment 599–600 (2017) 721–731
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