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An Integrated Recirculating Aquaculture System (RAS) for Land-Based Fish

Farming: The Effects on Water Quality and Fish Production

Article in Aquacultural Engineering · November 2011

DOI: 10.1016/j.aquaeng.2011.08.001

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 Aquacultural Engineering 45 (2011) 93–102

Contents lists available at ScienceDirect

Aquacultural Engineering
journal homepage: www.elsevier.com/locate/aqua-online

An integrated recirculating aquaculture system (RAS) for land-based fish

farming: The effects on water quality and fish production
Shi-Yang Zhang a , Gu Li a,∗ , Hui-Bi Wu a , Xing-Guo Liu b , Yan-Hong Yao a , Ling Tao a , Huang Liu b
a
Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, China
b
Fishery Machinery and Instrument Research Institute, Chinese Academy of Fishery Sciences, Shanghai 200092, China

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

Article history: To mitigate the serious water pollution caused by the rapid expansion of the aquaculture industry in
Received 11 May 2011 recent years, the development of improved aquaculture systems with more efficient water usage and
Accepted 4 August 2011 less environmental impact has become essential. In this study, a land-based recirculating aquaculture
system (RAS) was established that consisted of purification units (i.e., a primary biological pond, two
Keywords: parallel horizontal subsurface flow constructed wetlands [CWs], and a long ecological ditch) and 4–5
Recirculating aquaculture system
series-connected recirculating ponds. This system was mainly designed to stock channel catfish (Ictalu-
Culture efficacy
rus punctatus), fifteen spine stickleback (Spinibarbus sinensis) and yellow catfish (Pelteobagrus fulvidraco),
Water quality
Constructed wetland
and the culture efficacy was evaluated based on a 2-year field experiment covering two growing seasons.
Sensitive species According to the results, the primary biological pond played a role in sedimentation or nutrient reten-
tion, although this was not as evident when the CWs were functioning. The water flowing through the
wetland system at a hydraulic loading rate (HLR) of 600 mm/day displayed lower values for the temper-
ature, pH, dissolved oxygen (DO), suspended solids, organic matter and nutrients, whereas the electrical
conductivity (EC) was higher, suggesting the accumulation of dissolved solids in the system. Due to the
recirculation treatment, the trophic status of the recirculating ponds increased gradually along the direc-
tion of the flow and was notably lower in comparison to the control. As a result, the fish production
responded to the variation of the water quality, which was reflected in the measurements of culture
efficacy (final weight, survival rate, SGR and yield). The three main rearing species showed a decreasing
trend along the direction of the flow, which was higher compared to the control, whereas an opposite
trend was observed for filter-feeding fish. A Pearson correlation analysis revealed that the main culture
species were inclined to live in meso- or oligotrophic conditions, and the silver carp adapted to more
eutrophic conditions. Because RAS can provide better environmental conditions year-round, the present
culture method could be more suitable for species that are sensitive to water quality in typical subtropical
areas.
© 2011 Elsevier B.V. All rights reserved.

1. Introduction mental issues, such as the large rate of water consumption

As the fastest-growing food-producing sector in the world,
aquaculture has received more attention over recent decades.
This is because aquaculture is a major mode of aquatic food
production that maintains the current per capita consump-
tion and its increased use is accompanied by continuous
ecological concerns. The concerns relate either to the quality
and safety of the products or the various other environ-
∗ Corresponding author. Present address: Yangtze River Fisheries Research Insti-
tute, Chinese Academy of Fishery Sciences, No. 8, 1st Wudayuan Road, Donghu
Hi-Tech Development Zone, Wuhan 430223, China. Tel.: +86 027 81780121;
fax: +86 027 81780088.
E-mail address: ligu667@yahoo.com (G. Li).
and the low-strength, untreated wastewater discharge, that
are inherent is such a system (Xie et al., 2004; Xie and Yu,
2007).
China is the world’s largest consumer of fish and seafood
and the largest producer of aquaculture products, accounting
for 67% of the global production in terms of quantity and 49%
of the global value in 2006 (FAO, 2008). However, with the
rapid expansion of aquaculture, China has also faced serious
challenges related to this industry in recent years, including
the limitations of finite land and water resources, the gradual
deterioration of aquatic ecosystems, frequent disease outbreaks,
and difficulties with sediment and wastewater treatment (Cao
et al., 2007). To solve these issues appropriately, an approach of
sustainable development must be adopted. Hence, it is impera-
tive to develop new culture methods to decrease the ecological

0144-8609/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaeng.2011.08.001
94 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102
Fig. 1. Diagram (a) of the recirculating aquaculture system (RAS) and the ichnography (b) of the wetland cell showing its partition and gravel size distribution (: diameter);
P1–P5 represents five recirculating ponds; arrows denote the direction of the water flow.
impact in terms of waste production, water use and fossil fuel
demands.
One effective solution is the rearing of fish in recirculating
aquaculture systems (RASs), which are land-based aquatic sys-
tems where the water is (partially) re-used after mechanical and
biological treatment in an attempt to reduce the consumption of
water and energy and the release of nutrients into the environment
(i.e., eutrophication) (Martins et al., 2010b). Catering to sustainable
aquaculture, RASs have been developed in response to the increas-
ing environmental regulations in nations with limited access to
land and water. RASs offer advantages in terms of reduced water
consumption (Verdegem et al., 2006), improved opportunities for
waste management and nutrient recycling (Piedrahita, 2003), bet-
ter hygienic and disease management (e.g., Summerfelt et al., 2009;
Tal et al., 2009) and biological pollution control (Zohar et al., 2005).
To date, the rearing organisms that have been implemented in
RASs have expanded to a diverse range of species, from freshwa-
ter to seafood products and from hatchery/fingerling to grow-out
production (Davis and Arnold, 1998; Lin et al., 2003; Lymbery
et al., 2006; Schulz et al., 2003; Zachritz et al., 2008). The ongoing
developments in RASs show two trends that focus on (1) technical
improvements within the recirculation loop and (2) the recycling
of nutrients through integrated farming, such as the application of
constructed wetlands (CWs) (Martins et al., 2010a).
CWs are low-cost treatment alternatives that have been proven
to reduce suspended solids, dissolved organic matter, nutrients and
heavy metals in wastewater from many sources (Tilley et al., 2002).
The nutrient removal and transformation processes in CWs include
microbial conversion, decomposition, plant uptake, sedimentation,
volatilisation and adsorption–fixation reactions (Tchobanoglous,
1993). Uptake by plants and denitrification are the main processes
of nitrate removal in CWs; suspended solids are mainly removed by
filtration, and phosphorus is removed via adsorption to a medium.
Recently, CWs have been extensively applied to the aquaculture
industry for wastewater treatment and reuse (Konnerup et al.,
2011; Li et al., 2007; Zachritz et al., 2008; Zhang et al., 2010b).
However, information on the integrated mode of CWs with other
purification facilities and their respective function in RASs remains
unclear.
In the work presented here, CWs that were coupled with a pri-
mary biological pond and an ecological ditch were integrated into a
nearly closed outdoor RAS to regulate the water quality for the rear-
ing of channel catfish (Ictalurus punctatus), fifteen spine stickleback
(Spinibarbus sinensis) and yellow catfish (Pelteobagrus fulvidraco).
The primary objectives were the following: (1) to investigate the
regulation effect of the combined treatment system on the water
quality in the RAS and (2) to examine the association of the water
quality improvement via recirculation with the culture efficacy of
the rearing species.
2. Materials and methods
2.1. System construction
The study site was located in the experimental base of the
Research Center for Pond Ecological Engineering, Chinese Academy
of Fishery Sciences, Jingzhou, Hubei Province, China. The RAS con-
sisted of purification units (i.e., a primary biological pond, two
parallel horizontal subsurface flow CWs [30 m in length, 8.5 m in
width for each] and an ecological ditch) and 4–5 series-connected
culture ponds (Fig. 1 a). The frame of the CWs was built using bricks
and mortar, whereas the bottom was reinforced with concrete as
an impermeable liner fixed to a slope of 0.5%. Each wetland cell
was partitioned into three subareas along the direction of the flow,
an inlet area, a wetland bed (A and B) and an outlet area, which
were all filled with different sizes of gravel to a depth of 0.6 m
 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102 95

Fig. 2. Snapshots of parts of the recirculating aquaculture system (RAS).

(Fig. 1b). At the inlet, a storing cistern was constructed with a ser- (area, 450 m2 ; depth, 1.5–2.0 m), Zizania aquatica and Phragmites
rated overflow weir on one side, which facilitated a horizontal flow australis were planted, and an appropriate quantity of filter-feeding
of the water (Fig. 2). In the bottom of the CWs near the outlet, a fish (∼45 silver carp and 15 bighead carp) was stocked. These bio-
system of perforated 160-mm (in diameter) PVC pipes was placed logical components were expected to play a role in promoting the
to ensure efficient drainage. The wetland was planted with a mix- sedimentation of suspended solids and the absorption of pollutants.
ture of Canna indica, Iris tectorum, Acorus calamus, Cyperus papyrus
and Thalia dealbata, which propagated rapidly and soon covered
2.2. Operation and management of the system
the entire surface of the CWs within a single growing season (see
Table 1 for details on the plants used). These perennial aquatic or
Before the stocking the fish, all of the ponds were drained, the
marsh plants have extended root systems and large biomass and
silt was removed, and the bottom of the ponds was disinfected
were easily obtained in this district. After the construction and
with lime. Water pumped from a nearby reservoir was then used
planting, the systems were allowed to acclimatise for 2 months to
to fill the culture pond to a depth of approximately 1.5 m; there-
let the plants and microorganisms develop. During this period, the
after, the replacement of the water lost due to evaporation was
CWs were loaded with water from the fishpond at loading rates that
mainly achieved from the groundwater and rainfall. In this study,
varied between 300 (153 m3 /day) and 600 (306 m3 /day) mm/day.
a polyculture strategy for the stocking of the fish was adopted.
In general, the dissolved oxygen (DO) in the effluent from the
Juvenile I. punctatus and S. sinensis, as the main culture species,
horizontal subsurface flow CWs was too low to meet the demands
mixed with a minor quantity of filter-feeding fish and grass carp
for aquaculture use. Thus, a long concrete ditch (150 m in length,
(Ctenopharyngodon idella) were raised in 2006; in 2007, the primary
0.5 m in width, 0.6 m in depth) was constructed based on the theory
species was changed to P. fulvidraco. These species were chosen
of periphyton bioreactors. In detail, a set of fixed devices that acted
because they are the major freshwater fish commercially cultured
as an artificial substrate for the development of periphyton was
in China and were appropriate for determining the different water
laid at the bottom of the ditch (Tao et al., 2011). The devices were
quality requirements for optimal production. The details for the fry
made of polyethylene net affixed to a wooden frame. At the end
stocking in each of the culture ponds are provided in Table 2.
of the ditch, weirs and steps were designed for passive aeration.
In 2006, the fish stocking began on May 20th, and the fish were
After oxygenation, the DO of the effluent prior to flowing into the
harvested on November 8th, corresponding to a rearing period of
recirculating pond reached levels up to >5 mg/L, which generally
172 days; in 2007, stocking began on March 17th and harvesting
satisfies the requirement for aquaculture.
on October 18th, which corresponded to a rearing period of 215
The culture ponds included 4–5 (4 in 2006 and 5 in 2007) series-
days. The ponds were harvested by complete drainage at the end
connected recirculating ponds, a static control pond and a primary
of the rearing period. During the study, the fish were fed to satia-
biological pond. Each of the culture ponds (except the biological
tion twice daily with a commercial diet, and the amount fed was
one) had an area of 1000 m2 and a mean water depth of approxi-
measured to determine the feeding efficiency. The feeds were sup-
mately 1.5 m, with a mud bottom. The recirculating ponds, namely,
plied by Tongwei Feedstuff Co., Ltd. (Dongxihu Development Zone,
the flow-through systems, were connected by culvert pipes across
Wuhan, China). In 2006, a commercial catfish floating feed (∼34%
the pond banks fixed to a slope of 50% that ensured a mixing of the
protein, 5% fat, 7% cellulose, 14% ash, 1.6% lysine and 1.2% TP) was
upper stratum water with the lower one so as to enhance the pas-
used, whereas in 2007, the fish were fed with a premix feed (∼38%
sive aeration. The control pond without recirculation corresponded
protein, 3.5% fat, 5% cellulose and 1.4% TP). A pump submerged
to the stagnant water conditions that are representative of tradi-
in the biological pond was used to recycle the RAS, which oper-
tional static aquaculture ponds. The biological pond was devised
ated daily between 8:00 a.m. and 6:00 p.m., resulting in a hydraulic
to pretreat the effluent from the last recirculating pond (P4 in
loading rate (HLR) of 600 mm/day and a 4.3-h hydraulic retention
2006 or P5 in 2007) because the CWs still require pretreatment
time. However, on each sampling day, the system operated approx-
and the removal or screening of solids. The placement of the bio-
imately 2 h earlier, before the sampling began. The water exchange
logical pond at the initial stage of the CWs had the potential to
rate for each recirculating pond was maintained at 20% per day. The
extend the operational life of the wetlands. In the biological pond
recirculating system was not in operation during rainy days.

Table 1 2.3. Methods for sampling and analysis

Composition of the plant community in the CWs investigated in 2006.

Canna indica Iris tectorum Acorus calamus Sampling was conducted every 2 weeks, from June 3th to
Density (ind./m2 ) 38 20 22 November 2th in 2006 and from April 6th to October 17th in 2007.
Height (cm) 1.4–1.8 80–60 70–50 The ponds were sampled by mixing the water collected from each
Biomass (kg/m2 ) 32.1 7.8 1.2 corner of the pond at different depths. Given the extreme day-
Note: Plant density and height investigation was completed in August, whereas the time temperatures in the region, sampling was typically conducted
biomass was obtained in November at the end of the experiment in 2006. in the early morning, between 7:00 and 8:00 a.m. on each occa-
96 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102
Table 2
Summary of fry stocking in each of the culture ponds over the two years.
2006
Density (ind./ha) Initial mean weight (g/ind.)
Ictalurus punctatus 16,000 25.6
Spinibarbus sinensis 6000 10.4
Pelteobagrus fulvidraco
Silver carp 2000 25.0
Bighead carp 700 146.0
Grass carp 200 135.0
Total 24,900
sion, stored in 2.5-L polyethylene bottles and taken to the lab for
analysis within 2 h. The temperature (Temp.), electrical conductiv-
ity (EC), pH and DO were measured immediately after sampling
by an Orion 5-Star Portable pH/ORP/DO/Conductivity Multimeter
(Thermo Fisher Scientific Inc. [NYSE: TMO], MA, USA) in situ. The
total suspended solids (TSS), chemical oxygen demand (CODMn ),
total ammonia nitrogen (TAN), nitrite (NO2 − –N), nitrate (NO3 − –N),
TN and TP were analysed following standard procedures (State
EPA of China, 2002). The chlorophyll a (Chl-a) content was deter-
mined spectrophotometrically after filtration through Whatman
GF/C glass filters and 24-h extraction with 90% acetone. The chl-a
content was not determined for 2006.
The specific growth rate (SGR) and feed conversion ratio
(FCR) were calculated according to the following formulae:
SGR = 100 × (ln Wfin − ln Win )/d and FCR = FI/W, where Wfin is the
final mean weight, Win is the initial mean weight, d is the dura-
tion of feeding (days), FI is the feed intake (kg) and W is the live
weight gain (kg).
2.4. Data analysis
The data were expressed as means ± standard deviation (SD).
Prior to performing all of the parametric tests, an exploratory
data analysis (EDA) was first performed to test the distribution
characteristics of each group of the datasets because the paramet-
ric tests were strictly based upon the assumptions of a normal
frequency distribution, a homogeneity of variance, a “similar”
size and an independence of the groups (Tomarken and Serlin,
1986; Zimmerman, 1998). Among the EDA, the normal distri-
bution was inspected by Shapiro–Wilks tests (sample size less
than 2000), whereas the homogeneity of variance was deter-
mined by Levene’s tests. Any data that violated the assumption
of normal distribution were logarithmically transformed, with
the exception of the percent reduction that was performed by
an arcsine-root transformation (Bartlett, 1947) to insure nor-
mality; for clarity, all of the data are presented untransformed.
The comparison of water quality between the inlet, outlet and
culture ponds differing by year was performed by a one-way
ANOVA, followed by LSD or Games–Howell tests, which were
selected based on the assumption of equal or unequal variances,
respectively. When the homogeneity of the variance among the
groups was not verified or the assumption of ANOVA was vio-
lated, the Welch and Brown–Forsythe options further displayed
alternative versions of the F statistic, which helped in interpret-
ing the outcome correctly (Myers and Well, 2003). In addition,
an independent t-test was used to compare the differences in
the percent reduction, mass loading rates and areal removal
rates between 2006 and 2007. The relationships between the
pond water quality and fish production were examined by Pear-
son correlations. All of the statistical analyses were performed
using the SPSS software (SPSS Inc., Chicago, IL, USA; Version
13.0).
2007
Biomass (kg) Density (ind./ha) Initial mean weight (g/ind.) Biomass (kg)
41.0
6.2
70,000 6.9 48.4
5.0 1500 100 15.0
10.2 500 50 2.5
2.7 200 50 1.0
65.1 72200 66.9
3. Results
3.1. Performance of the CWs and the biological pond
After the wetland treatment, the outlet water temperature was
slightly lowered in comparison to the inlet water temperature, an
opposite trend was observed for the EC, and the pH and DO were
both significantly reduced. The CWs showed significant purifica-
tion efficiencies for suspended solids, organic matter and nutrients.
The statistical analysis revealed that the TSS, CODMn , NO3 − –N,
TN, TP and Chl-a content in the outlet water were all signifi-
cantly lower than those in the inlet water for both 2006 and 2007.
The TSS, TN and TP in P4 and P5 were all reduced, as compared
to the inlet water, indicating that the biological pond, to some
extent, functioned as a sink for sedimentation or nutrient retention
(Table 3).
The CWs showed relatively higher removal efficiencies for the
Chl-a content and TSS, with the removal, in descending order,
of NO2 − –N, CODMn , TP, TAN and TN. The system showed unsta-
ble removal efficiencies for most of the indices, especially for
NO3 − –N (i.e., the outlet concentration was even higher than the
inlet concentration). The results of independent t-tests showed no
significant differences in the percent reduction, mass loading rates
or areal removal rates between the two years (Table 4).
3.2. Water quality in the culture ponds
With the recirculation treatment, a marked difference in the
water quality between the control and recirculating ponds was
found. The basic trend was that the trophic status (in terms of
organics and nutrients) of the recirculating ponds increased grad-
ually along the direction of the flow (i.e., P1 → P4 in 2006 and
P1 → P5 in 2007) and declined, as compared to the control pond.
The results of one-way ANOVA statistics revealed that the DO was
significantly (P < 0.05) lower in the control than in the recirculat-
ing pond (P1), whereas opposite trends for the TAN and TP were
observed in 2006. Similarly, the DO and EC were significantly lower
in the control than in the recirculating ponds; in contrast, opposite
trends for the CODMn , TN, TP and Chl-a content were found for 2007
(Tables 5 and 6).
3.3. Fish production
In 2006, there was no marked difference in the survival rate of
I. punctatus between the control and recirculating ponds; however,
the final weight, SGR and yield showed obvious decreasing trends
among the recirculating ponds, and these indices for P1 and P2 were
much larger or higher than those for the control. Similarly, the val-
ues for the final weight, survival rate, SGR and yield of S. sinensis
were all lower in the control than in the recirculating ponds, and
these indices also showed obvious decreasing trends. Conversely,
for the silver carp and bighead carp, these four indices all showed
 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102 97

Table 3
Composition of the water from the last recirculating pond (P4 in 2006 and P5 in 2007), the inflow and the outflow of the CWs differing by year (mean ± SD; n = 11 in 2006
and n = 14 in 2007) and the results of one-way ANOVA statistics (P-value). Different letter superscripts between columns indicate significant differences.

Parameters 2006 2007 P-value

P4 Inlet Outlet P5 Inlet Outlet

Temp. (◦ C) 25.4 ± 6.2 25.3 ± 7.8 24.8 ± 7.1 25.2 ± 4.5 24.7 ± 4.8 24.4 ± 4.5 0.998NS
EC (␮S/cm) 426 ± 54 441 ± 43 463 ± 50 420 ± 36 417 ± 37 439 ± 27 0.182NS
pH 7.5 ± 0.2a 7.4 ± 0.1a 7.1 ± 0.1b 7.7 ± 0.4a 7.5 ± 0.4a 7.3 ± 0.4ab 0.029*
DO (mg/L) 1.62 ± 0.48a 10.90 ± 2.48b 2.74 ± 1.10cd 4.21 ± 1.67c 2.97 ± 1.83d 0.97 ± 0.59e 0.000***
TSS (mg/L) 68.4 ± 24.6a 53.2 ± 17.8a 9.3 ± 2.1b 67.1 ± 13.1a 59.7 ± 15.7a 14.2 ± 6.0c 0.000***
CODMn (mg/L) 6.3 ± 2.6a 9.4 ± 1.7b 4.7 ± 1.4a 10.5 ± 3.0b 10.5 ± 2.8b 4.7 ± 1.5a 0.000***
TAN (mg/L) 0.74 ± 0.49 0.87 ± 0.63 0.47 ± 0.31 0.75 ± 0.42 0.82 ± 0.41 0.49 ± 0.19 0.066NS
NO2 − –N (mg/L) 0.033 ± 0.025a 0.032 ± 0.030ab 0.010 ± 0.005b 0.061 ± 0.077ab 0.064 ± 0.072a 0.016 ± 0.010ab 0.014*
NO3 − –N (mg/L) 0.10 ± 0.03a 0.08 ± 0.04ac 0.04 ± 0.04b 0.07 ± 0.03ac 0.08 ± 0.03ac 0.06 ± 0.03c 0.006**
TN (mg/L) 2.21 ± 0.76ab 1.92 ± 0.86b 1.16 ± 0.36c 3.16 ± 0.98d 2.73 ± 1.00ad 1.73 ± 0.68b 0.000***
TP (mg/L) 0.47 ± 0.15a 0.39 ± 0.14a 0.23 ± 0.08b 0.47 ± 0.10a 0.44 ± 0.12a 0.24 ± 0.10b 0.000***
Chl-a (␮g/L) 38.4 ± 5.6a 35.6 ± 12.0a 3.8 ± 1.4b 0.000***

NS: not significant.

*
P < 0.05.
**
P < 0.01.
***
P < 0.001.

Table 4
Mean treatment results for the various parameters of water quality by the horizontal subsurface flow CWs throughout the study (mean ± SD; n = 11 in 2006 and n = 14 in
2007) and results of independent t-tests (P-value).

Parameters Percent reduction (%) Mass loading rate (g/(m2 day)) Areal removal rate (g/(m2 day))

2006 2007 P-value 2006 2007 P-value 2006 2007 P-value

TSS 82.0 ± 1.9 75.4 ± 10.5 0.182NS 31.9 ± 10.7 35.8 ± 9.4 0.429NS 26.3 ± 9.5 27.3 ± 9.4 0.838NS
CODMn 50.1 ± 13.8 52.0 ± 21.8 0.844NS 5.6 ± 1.0 6.3 ± 1.7 0.363NS 2.8 ± 0.9 3.5 ± 2.0 0.428NS
TAN 40.9 ± 21.6 37.6 ± 15.6 0.718NS 0.52 ± 0.38 0.49 ± 0.24 0.852NS 0.24 ± 0.22 0.20 ± 0.18 0.939NS
NO2 − –N 60.7 ± 13.3 59.8 ± 23.7 0.940NS 0.019 ± 0.018 0.039 ± 0.043 0.443NS 0.013 ± 0.016 0.030 ± 0.039 0.508NS
NO3 − –N 43.8 ± 45.4 16.1 ± 33.2 0.143NS 0.05 ± 0.02 0.05 ± 0.02 0.864NS 0.02 ± 0.02 0.01 ± 0.02 0.119NS
TN 34.6 ± 16.0 35.6 ± 13.0 0.894NS 1.15 ± 0.51 1.64 ± 0.60 0.102NS 0.46 ± 0.33 0.60 ± 0.33 0.364NS
TP 40.4 ± 12.2 46.2 ± 11.0 0.316NS 0.24 ± 0.08 0.26 ± 0.07 0.500NS 0.10 ± 0.05 0.12 ± 0.04 0.302NS
Chl-a 88.6 ± 4.1 0.021 ± 0.007 0.019 ± 0.007

NS: not significant.

increasing trends and were all lower in the control than in the recir-
culating ponds (except P1 for bighead carp). The total yield was
much lower in the control than in the recirculating ponds (Fig. 3).
In 2007, the final weight, survival rate, SGR and yield of P. ful-
vidraco were all lower in the control than in the recirculating ponds,
whereas the final weight, SGR and yield values for the silver carp
and bighead carp were notably higher in the control than in the
recirculating ponds; the total yield was also lower in the control
than in the recirculating ponds (Fig. 4).
Over the two rearing periods, the feeding rate was based on 3–5%
of the body weight and was adjusted according to the intake rate
of the fish. Hence, there was a discrepancy of feed intake among
the culture ponds that was likely induced by the differences in the
water quality. The basic trend was that the feed intake quantity
decreased along the direction of the flow, which could also lead
to a difference in weight gain. Overall, the FCR was higher in the
control than in the recirculating ponds for both years (Table 7).
3.4. Correlations between water quality and fish production
Pearson correlation analysis was employed to depict the
relationships between fish production and the environmental
parameters in this study; the results indicated a strong associa-
tion between fish production and water quality parameters. The
specific relationships between the water quality parameters and

Table 5
Composition of the water in the recirculating (P1–P4) and control (P0) ponds in 2006 (mean ± SD; n = 11) and the results of one-way ANOVA statistics (P-value). Different
letter superscripts between columns indicate significant differences.

Parameters P0 P1 P2 P3 P4 P-value
◦
Temp. ( C) 25.3 ± 6.3 25.1 ± 6.4 25.2 ± 6.4 25.4 ± 6.3 25.4 ± 6.2 1.000NS
EC (␮S/cm) 398 ± 50 431 ± 49 430 ± 52 427 ± 52 426 ± 54 0.62NS
pH 7.62 ± 0.17 7.60 ± 0.18 7.59 ± 0.18 7.55 ± 0.17 7.46 ± 0.22 0.27NS
DO (mg/L) 1.44 ± 0.68a 3.40 ± 0.96b 1.83 ± 0.62a 1.64 ± 0.54a 1.62 ± 0.48a 0.000***
TSS (mg/L) 74.8 ± 21.2 69.9 ± 19.2 58.5 ± 17.9 69.7 ± 23.3 68.4 ± 24.6 0.49NS
CODMn (mg/L) 7.0 ± 2.6 5.0 ± 1.7 5.4 ± 2.2 5.5 ± 2.1 6.3 ± 2.6 0.26NS
TAN (mg/L) 0.88 ± 0.50a 0.42 ± 0.31b 0.60 ± 0.46ab 0.71 ± 0.50ab 0.74 ± 0.49a 0.044*
NO2 − –N (mg/L) 0.041 ± 0.037 0.026 ± 0.032 0.025 ± 0.023 0.027 ± 0.019 0.033 ± 0.025 0.65NS
NO3 − –N (mg/L) 0.095 ± 0.042 0.079 ± 0.030 0.080 ± 0.036 0.086 ± 0.027 0.098 ± 0.031 0.51NS
TN (mg/L) 2.73 ± 0.98 1.83 ± 0.59 1.98 ± 0.73 2.15 ± 0.80 2.21 ± 0.76 0.09NS
TP (mg/L) 0.55 ± 0.23a 0.37 ± 0.15b 0.36 ± 0.17b 0.40 ± 0.13ab 0.47 ± 0.15ab 0.043*

NS: not significant.

*
P < 0.05.
***
P < 0.001.
98 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102

Table 6
Composition of the water in the recirculating (P1–P5) and control (P0) ponds in 2007 (mean ± SD; n = 14) and results of one-way ANOVA statistics (P-value). Different letter
superscripts between columns indicate significant differences.

Parameters P0 P1 P2 P3 P4 P5 P-value

Temp. (◦ C) 25.2 ± 4.5 24.9 ± 4.5 24.8 ± 4.5 24.9 ± 4.5 25.1 ± 4.5 25.2 ± 4.5 1.00NS
EC (␮S/cm) 371 ± 40a 425 ± 23b 427 ± 21b 429 ± 30b 425 ± 32b 420 ± 36b 0.000***
pH 7.67 ± 0.27 7.65 ± 0.36 7.66 ± 0.30 7.73 ± 0.35 7.69 ± 0.36 7.68 ± 0.40 0.99NS
DO (mg/L) 2.94 ± 1.52a 4.29 ± 1.41b 4.16 ± 1.29b 3.96 ± 1.37b 4.35 ± 1.42b 4.21 ± 1.67b 0.041*
TSS (mg/L) 72.5 ± 27.0 55.2 ± 19.7 58.4 ± 17.0 63.9 ± 15.4 63.2 ± 13.1 67.1 ± 13.1 0.11NS
CODMn (mg/L) 12.8 ± 3.6a 7.3 ± 2.5b 8.0 ± 2.4bc 8.3 ± 2.2bc 9.6 ± 3.0cd 10.5 ± 3.0ad 0.000***
TAN (mg/L) 0.83 ± 0.47 0.72 ± 0.43 0.65 ± 0.36 0.73 ± 0.43 0.68 ± 0.40 0.75 ± 0.42 0.87NS
NO2 − –N (mg/L) 0.072 ± 0.055 0.039 ± 0.036 0.036 ± 0.032 0.041 ± 0.034 0.042 ± 0.045 0.061 ± 0.077 0.43NS
NO3 − –N (mg/L) 0.110 ± 0.109 0.060 ± 0.022 0.070 ± 0.025 0.066 ± 0.025 0.066 ± 0.021 0.069 ± 0.026 0.40NS
TN (mg/L) 4.03 ± 1.41a 2.35 ± 0.81b 2.43 ± 0.62b 2.59 ± 0.61b 2.95 ± 0.95ab 3.16 ± 0.98ab 0.000***
TP (mg/L) 0.58 ± 0.24a 0.39 ± 0.10b 0.44 ± 0.10bc 0.48 ± 0.12ab 0.49 ± 0.09ac 0.47 ± 0.10bc 0.009**
Chl-a (␮g/L) 84.1 ± 26.1a 21.2 ± 11.0b 29.0 ± 17.8b 35.9 ± 17.4b 43.7 ± 23.3b 38.4 ± 5.6b 0.000***

NS: not significant.

*
P < 0.05.
**
P < 0.01.
***
P < 0.001.

Fig. 3. Statistics for fish harvest in 2006.

Fig. 4. Statistics for fish harvest in 2007.

 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102 99

Table 7
Calculations for feed intake (FI), live weight gain (WG) and feed conversion ratio (FCR) during the two rearing periods.

Pond 2006 2007

FI (kg) WG (kg) FCR FI (kg) WG (kg) FCR

P0 1300 706 1.84 1100 641 1.72

P1 1500 1180 1.27 1100 720 1.53
P2 1400 993 1.41 1100 688 1.60
P3 1250 840 1.49 1100 735 1.50
P4 1300 825 1.58 1000 734 1.36
P5 1000 669 1.49

Table 8
Pearson correlation coefficients between water quality parameters and final weight. Only significant relationships are listed, as in Tables 9–11.

Parameters 2006 2007

Ictalurus punctatus Spinibarbus sinensis Silver carp Pelteobagrus fulvidraco Silver carp Bighead carp

Temp. −0.985** −0.908* 0.848*

pH −0.956*
DO 0.907*
EC 0.898* −0.856*
TSS −0.859* 0.834* 0.895*
CODMn −0.948** 0.961**
TAN −0.959* −0.831*
NO2 − -N −0.974** 0.852*
NO3 − -N −0.883* 0.840*
TN −0.946** 0.960**
TP 0.859*
Chl-a −0.864* 0.917*
*
P < 0.05.
**
P < 0.01.

culture efficacy (i.e., the final weight, survival rate, SGR and yield) Table 9
Pearson correlation coefficients between water quality parameters and survival
are listed in Tables 8–11.
rates.

2006 2007
4. Discussion Parameters Spinibarbus Bighead carp Pelteobagrus
sinensis fulvidraco
4.1. Regulation effect of the CWs pH −0.988**
EC 0.882*
In general, the dominant processes controlling the water tem- CODMn −0.934*
perature in wetlands are the energy absorbed from the incident TAN −0.949*
NO2 − –N −0.822*
solar radiation and convective heat transfer with the atmosphere
TN −0.958*
through evapotranspiration (Kadlec and Knight, 1996). Due to the
*
shading provided by plants of the incoming solar radiation and the P < 0.05.
**
P < 0.01.
dissipation of energy through transpiration, evaporative cooling
dominates the water energy balance in wetlands. For subsurface
flow CWs, there is likely an absorption of energy by the filter media

Table 10
Pearson correlation coefficients between water quality parameters and specific growth rates (SGRs).

Parameters 2006 2007

Ictalurus punctatus Spinibarbus sinensis Silver carp Pelteobagrus fulvidraco Silver carp Bighead carp

Temp. −0.990 **
0.834 *

pH −0.941*
*
DO 0.817
EC 0.915* −0.818*
TSS −0.859* 0.819* 0.882*
CODMn −0.946** 0.948**
TAN −0.963** −0.849*
NO2 − –N −0.975** 0.821*
NO3 − –N −0.915* −0.898* 0.814*
TN −0.949** 0.939**
TP 0.848*
Chl-a −0.876* 0.894*
*
P < 0.05.
**
P < 0.01.
100 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102
Table 11
Pearson correlation coefficients between water quality parameters and yields.
Parameters 2006
Ictalurus punctatus Spinibarbus sinensis Silver carp
Temp. −0.945*
pH −0.944*
DO 0.926* 0.962**
EC
TSS
CODMn
TAN −0.898* −0.982**
NO2 − –N
NO3 − –N
TN
TP
Chl-a
*
P < 0.05.
**
P < 0.01.
***
P < 0.001.
(Agudelo et al., 2010) due to the heat exchange with the ground-
water or soil across the liners. As a result, the average daily outflow
temperatures are generally lower than the inflow temperatures,
particularly in arid climates (Kadlec, 2006). Such was the case in the
present study, which, on average, showed a 0.3–0.5 ◦ C drop in tem-
perature between the inflow and outflow over the two relatively
warm growing seasons (Table 3).
In the CWs, the microbial decay of organic matter in shaded and
shallow waters led to elevated oxygen consumption and a decrease
in the DO concentration in the wetland waters by a mean reduc-
tion of 74.9% in 2006 and 67.3% in 2007 (Table 3). A number of
researchers have observed drops in the DO in horizontal subsur-
face flow CWs similar to those used in this study. For example,
Konnerup et al. (2011) have found that the mean DO declined from
6.3 to 2.3 mg/L through replicate horizontal subsurface flow CWs
treating low-strength fishpond water at a HLR of 750 mm/d. Simi-
larly, Agudelo et al. (2010) have reported a decrease in the DO from
5.4 to 2.5 mg/L when using four pilot-scale horizontal subsurface
flow CWs to remove chlorpyrifos and organic matter simultane-
ously. An obvious DO reduction from 3.17 to 0.22 mg/L has also been
reported by Zachritz et al. (2008) when they evaluated submerged
surface flow CWs for the treatment of tilapia production wastew-
aters. A more likely explanation for the reduction is based on the
degradation of organic compounds by aerobic, anaerobic and fac-
ultative bacteria within the vegetated beds. To a lesser extent, this
also may have decreased the solubility of oxygen due to the pres-
ence of salts (i.e., the EC increased after the wetland treatment) and
other compounds (Seoánez, 1999).
The slight increase in the EC of the effluent from the CWs (mean
increment: 22 ␮S/cm for both years) was due to the mineralisation
of organic compounds that contributed ions and salts and to the
CO2 , which then formed bicarbonates (Lahora, 2003). The EC could
also have increased as a result of the decomposition of submerged
roots and stems of dead plants, which formed humic acids, or by
the release of substances during the growth of roots and rhizomes
(Kadlec et al., 2000). This might have simultaneously contributed to
the slight drop in the pH (the mean value decreased by 0.3 in 2006
and 0.2 in 2007). In addition, nitrification that consumed alkalinity
in the wetland bed would make the effluent more acidic.
In this study, the wetland system showed relatively higher
removal efficiencies for particulate matter (in terms of the TSS
and Chl-a content), whereas lower, unstable removal efficiencies
for nutrients and organic matter were observed, which was in
agreement with the previous research of Zhang et al. (2010b). This
phenomenon could be ascribed to seasonal oscillations, including
physicochemical and biological variations within the CWs, influent
fluctuation, and climate changes. However, there was no distinct
2007
Other fishes Total yield Pelteobagrus fulvidraco Silver carp Bighead carp Total yield
0.863*
0.913*
0.833*
0.819* 0.895*
−0.879* −0.884* 0.954**
−0.995***
−0.916* 0.857* −0.826*
0.923* −0.896* −0.842*
−0.868* 0.941**
0.813*
0.867*
difference in the treatment performance of the CWs over the two
years, most likely due to the similar mass loading rates and climatic
conditions (Table 4). It should be pointed out that the pollutant
concentration in the influent from the biological pond that fed the
CWs was rather low compared to many other wetland treatment
systems (Konnerup et al., 2011; Lin et al., 2003; Zachritz et al., 2008).
4.2. Water quality comparison among the culture ponds
With the recirculation treatment, the water quality parameters
in the recirculating ponds were maintained at acceptable lev-
els (mean value: DO > 1.4 mg/L, CODMn < 13 mg/L, TAN < 0.9 mg/L,
NO2 − –N < 0.08 mg/L, TN < 4.1 mg/L and TP < 0.6 mg/L) for fish
growth over the two years. This was mainly attributed to the com-
bined treatment by the biological pond, the CWs and the long
ecological ditch and was further demonstrated by the lower trophic
status in the recirculating ponds, as compared to the control.
According to the research by Tao et al. (2011), a ditch significantly
purifies the effluent from the CWs, with a percent removal of 19.5%
for the TAN, 13.4% for the CODMn and 31.1% for the PO4 3− –P and
an increased DO within a range of 4.41–7.91 mg/L. The increas-
ing trophic status among the recirculating ponds could possibly
be interpreted by the fact that the first recirculating pond (P1) was
continuously replenished with clean water (i.e., the final effluent
after the combined treatment), which was diluted with the pond
water along the direction of the flow.
Based on our results, the DO was significantly lower in the con-
trol than in the recirculating ponds, and this seemed contradictory
with the Chl-a content, which was higher in the control than in the
recirculating ponds; this was likely due to the fact that the DO in
the culture pond was mainly derived from algal photosynthesis. For
instance, in channel catfish (I. punctatus) ponds, it has been reported
that most of the oxygen (76.9%) is produced by phytoplankton pho-
tosynthesis (Santa and Vinatea, 2007). Thus, a pond with higher
phytoplankton levels usually attains a higher daily DO. Neverthe-
less, in this study, the DO was monitored in the early morning when
the algal photosynthesis was at a low rate. After a night of respira-
tion, the pond DO would be at its lowest level at dawn and would
gradually recover in the daytime due to photosynthesis. In addi-
tion, passive aeration via water recirculation also increased the DO
stocks in the recirculating ponds, which might be another reason
for our observations. Similar to the DO, the EC was also lower in the
control than in the recirculating ponds. This was in accordance with
the wetland treatment performance, which might imply the accu-
mulation of dissolved solids in the system. As pointed by Martins
et al. (2010a), the potential accumulation of substances in the water
 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102
as a consequence of reduced water refreshment rates may pose new
challenges to the application of RAS.
4.3. Culture efficacy
According to the statistical analysis of the fish harvest, fish pro-
duction differed greatly among the culture ponds both between
different species and within the same species. I. punctatus grew
better in P1 and P2 compared to the control but grew less than
the control for P3 and P4, and their survival rates varied from
79.8% to 94.3%. In contrast, the survival rates of S. sinensis declined
notably (less than 80%), especially for the control (only 18.7%). The
extremely low survival rate in the control implied a failure of their
stocking in the static conditions that were used. Similar trends were
observed for P. fulvidraco, which grew much better in the recirculat-
ing ponds than in the control. Thus, we conclude that RAS might be
an appropriate rearing mode for S. sinensis and P. fulvidraco. How-
ever, a discrepancy was found for silver carp in that they grew better
in the recirculating ponds than in the control in 2006, whereas the
opposite was found for 2007; a similar trend was found for the
bighead carp. This discrepancy could be explained by the different
stocking structure, including the species combination, initial stock-
ing density, size, and feed type, and water quality variations over
the two years.
Because the feeding behaviour of fish is strongly influenced by
the environmental conditions, such as the water temperature, DO,
TAN, and NO2 − –N (Buentello et al., 2000; Meinelt et al., 2010;
Pang et al., 2011), water quality improvement in an RAS may
increase feed intake rates. The RAS provides better environmen-
tal conditions year-round, contributes to the health of the fish and
minimises the FCR, thus improving the feeding efficiency (Roque
d’Orbcastel et al., 2009). In the present study, a basic trend was
that the feed intake quantity decreased along the direction of the
flow, and the FCR was higher in the control than in the recircu-
lating ponds with a percent reduction of 21.9% in 2006 and 13.0%
in 2007 (mean value), as compared to the control. This has also
been reported in other studies. For example, Lin et al. (2003) have
reported a lower FCR in an RAS (1.65) than in the control (2.25)
when they utilised a combined wetland unit to recirculate wastew-
ater from a shrimp culture tank. Similarly, Li et al. (2007) have
demonstrated a favourably lower FCR in a recirculating pond (1.43)
than in a static pond (2.27) when they integrated vertical-flow CWs
into an outdoor RAS for culturing I. punctatus and Wuchangfish
(Megalobrama amblycephala).
4.4. Association of water quality with culture efficacy
As an important ecological factor, the temperature has a pro-
found effect on fitness and determines traits, such as growth,
metabolism and locomotion performance (Green and Fisher, 2004;
Jain and Farrell, 2003). According to our Pearson correlation analy-
sis, the values for the final weight, SGR and yield of I. punctatus were
all significantly and negatively correlated with the temperature, as
were the final weight values for S. sinensis. In contrast, the final
weight, SGR and yield of silver carp were all positively correlated
with the temperature, indicating that I. punctatus and S. sinensis
were inclined to live in cool conditions, whereas the silver carp
preferred the conditions of higher temperature. These observations
might be partly attributable to their different ecological habits. S.
sinensis is normally distributed in both the mainstream and trib-
utaries of the upper reaches of the Yangtze River, conditions that
usually correspond to a clean, flowing and cool habitat. Conversely,
silver carp are filter-feeding fish and are largely dependent on phy-
toplankton’ thus, they prefer conditions of higher temperature.
Nevertheless, it should be clarified that even if the temperature
variations among the culture ponds were not significant, the slight
101
differentiation possibly had an effect on the growth of the fish. The
final weight, survival rate, SGR and yield of the silver carp and big-
head carp negatively correlated with the pH, implying a preference
for more acidic conditions.
The DO is one of the most important abiotic factors determining
the growth and survival of fish in both the wild (Taylor and Miller,
2001) and aquaculture (Piper et al., 1982). The DO increases feed
consumption, feeding efficiency, metabolism and growth in fish
(Buentello et al., 2000; Jobling, 1993; Van Dam and Pauly, 1995).
Numerous studies have shown increases in oxygen consumption
after feeding due to the metabolic cost of digesting and assimilat-
ing the nutrients from the feed (Jobling, 1993). In this study, the
final weight of S. sinensis, the SGR of P. fulvidraco, and the yield of I.
punctatus and S. sinensis in addition to the total yield in 2006 were
all positively correlated with the DO, indicating a dependence on
the DO for these species. Moreover, a stronger association between
the rearing species and the DO was observed in 2006 in compari-
son to 2007. This could be partially explained by the lower DO level
in the culture ponds in 2006 than in 2007 and the difference in
the rearing species, which showed distinct DO requirements under
rearing conditions.
Similar to the temperature and DO, the suspended solids, dis-
solved organic matter and nutrient loadings are also important
ecological factors in aquaculture. Organic particulates may include
gill function and nourish facultative fish pathogens, in addition
to contributing to the biological oxygen demand and providing a
substrate for growth of heterotrophic microorganisms that may
displace the nitrifying bacteria (Nitrosomonas and Nitrobacter) that
are essential for the conversion of ammonia to nitrate (Summerfelt
and Penne, 2005). The suspended solids and dissolved organic mat-
ter in the rearing water will also cloud the water and increase the
oxygen consumption as the solids undergo bacterial decomposi-
tion. Nitrogen compounds, such unionised ammonia and nitrite,
are extremely harmful in aquaculture, and their detrimental effects
on rearing species have been well documented in the literature
(Jensen, 2003; Meinelt et al., 2010; Pinto et al., 2007; Spencer et al.,
2008). Phosphorus is generally considered as the limiting factor
for algal reproduction in eutrophic waters (Zhang et al., 2010a),
and an excess of phosphorus will lead to algal blooms that are also
detrimental to aquaculture. In the present study, the final weight,
survival rate, SGR and/or yield of the three main culture species
(i.e., I. punctatus, S. sinensis and P. fulvidraco) were negatively cor-
related with the suspended solids, organic matter and/or nutrients,
whereas the silver carp showed the opposite trend, indicating that
the main culture species were inclined to live in meso- or olig-
otrophic conditions that corresponded to superior water quality
and the silver carp adapted to the more eutrophic conditions that
matched poor water quality. In addition, through the association
of the water quality with fish production, the extent of sensitivity
to the water quality for the three main species can be ordered as
follows: I. punctatus < S. sinensis < P. fulvidraco.
5. Conclusions
In the present study, we utilised a primary biological pond, two
parallel subsurface flow CWs and a long ecological ditch as purifica-
tion units in combination with culture ponds to establish an RAS for
fish farming. According to the results, the primary biological pond
functioned, to some extent, as a sink for sedimentation or nutrient
retention. The water flowing through the CWs displayed a lower
temperature, pH, DO, suspended solids, organic matter and nutri-
ents but a higher EC, which largely contributed to the lower trophic
status of the recirculating ponds, as compared to the control. Due
to the strong association between the water quality and fish pro-
duction, an RAS that can provide better environmental conditions
102 S.-Y. Zhang et al. / Aquacultural Engineering 45 (2011) 93–102

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