Biorremediacion_Gracilaria

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Improvement of Water Quality by the Macroalga, Gracilaria

lemaneiformis (Rhodophyta), near Aquaculture Effluent Outlets

YONGJIAN XU1

Faculty of Life Science and Biotechnology, Ningbo University, Ningbo 315211 China

JIANGUANG FANG AND QISHENG TANG

Yellow Sea Fisheries Research Institute, CAFS, Qingdao 266071 China

JUNDA LIN

Department of Biology Sciences, Florida Institute of Technology,Melbourne, Florida 32901 USA

GUANZONG LE AND LV LIAO

Faculty of Life Science and Biotechnology, Ningbo University, Ningbo 315211 China

Abstract

Raft culture of the seaweed, Gracilaria lemaneiformis (Bory) Dawson, was used as biofilter for

purifying effluent and removing nutrients from the nearby animal aquaculture. The results showed

that the cultivated seaweed grew well outside effluent discharge outlets for growout ponds and

a hatchery plant. The biomass (fresh weight) of Gracilaria from the 0.5-ha area outside the growout

ponds increased about 60 times, from 80 to 4750 g/m during the 65 d of experiment (with the daily

special growth rate [SGR] of 3.87%/d); the yield was 30.4 tons and 93.97 kg N and 12.81 kg P were

removed; the seaweed biomass from the 0.2-ha area outside the hatchery outlet increased 37.5 times,

from ,100 to 3600 g/m (with SGR of 3.4%/d); the yield was 10.4 tons and 31.7 kg N and 4.33 kg Pwere removed. Several water quality parameters such as dissolved oxygen, secchi disk depth, and pH

value in the algal cultivation area were substantially higher than those in the noncultivation zone,

whereas chemical oxygen demand, dissolved inorganic nitrogen, and dissolved inorganic phosphorous

at both areas were similar.

Rapid development of intensive aquaculture

in coastal areas throughout the world has raised

increasing concerns on its environmental im-

pacts (e.g., Wu 1995; Mazzola et al. 1999).

Organic and inorganic inputs of fish culture feedhave lead to a substantial increase of organic

matter and nutrient loading in coastal waters.

In general, 5295% of the nitrogen and about

85% of the phosphorus input into a marine fish

culture system as feed may be lost into the

environment through feed wastage, fish excre-

tion, and feces production, which may lead to

eutrophication, harmful algal blooms (HAB),

and anoxia (Wu 1995). In China, effluent from

shrimp culture ponds often exceeds the purify-

ing capacity of local coastal sea or bay and ac-

celerates the eutrophication and results in HAB

(Sun et al. 1990; Sheng and Shi 1996). Annually,

about 4.4 billion tons of effluent, including

17,000 tons of organic matter, from 8000-hashrimp culture ponds in Yantai, Shandong Prov-

ince, China, were discharged (Zhai 1996). The

negative economic and environmental impacts

of monospecific (especially of high trophic level)

aquaculture operations are being recognized

and their sustainability questioned (Naylor et al.

2000; Chopin et al. 2001; Neori et al. 2004).

In recent years, there has been increasing

emphasis on developing sustainable approaches

to coastal aquaculture (Folke and Kautsky 1989;Wurts 2000; Frankic and Hershner 2003; Neori

et al. 2004). Polyculture of different trophic

levels is the basis of environmentally friendly1 Corresponding author.

JOURNAL OF THE

WORLD AQUACULTURE SOCIETY

Vol. 39, No. 4

August, 2008

Copyright by the World Aquaculture Society 2008

549


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aquaculture (Chopin et al. 2001; Neori et al.

2004). By integrating fed mariculture (e.g., fish

and shrimp) with inorganic and organic extrac-

tive mariculture (seaweed and filter-feeding

bivalve), the waste of one resource consumerbecomes a resource (fertilizer or food) for the

other in the system. Such a balanced ecosystem

approach provides mutual benefits to cocultured

organisms, economic diversification by produc-

ing value-added products, nutrient bioremedia-

tion capacity, and environmental sustainability

(Chopin et al. 2001; Schuenhoff et al. 2003;

Neori et al. 2004).

In the past several decades, large-scale sus-

pended seaweed farming has been commercial-ized (Tseng and Fei 1987; Petrell et al. 1993;

Troell et al. 1997; Chopin et al. 1999; Neori

et al. 2004). However, there are only few species

of macroalgae that are suitably cocultured with

animals, especially in ponds. The genus Graci-

laria (Rhodophyta) has been demonstrated to

be an attractive candidate for intensive culture

because of its value as human food and its ability

to achieve high yields and to produce commer-

cially valuable products (Chopin et al. 2001;

Fei 2004; Neori et al. 2004). The edible red alga,

Gracilaria lemaneiformis, occurs naturally in

coastal areas of Shandong Peninsula, north China.

This species has been successfully introduced to

subtropical coastal waters in south China where

it is also cultivated widely (Fei et al. 2000). In

this study, we investigated the algal growth

and bioremediation potential near effluent out-

lets of animal culture ponds and a hatchery plant.

Materials and Methods

Study Site

The study was carried out in Xiangshan Bay

(29299320N, 121339590E), Zhejiang Province,

China. Raft culture of the red alga, G. lemanei-

formis, was established at two sites. The first one

was a 0.5-ha (50 3 100 m) area in the bay out-

side an outlet (PM) that discharged the effluent

(directly to the bay without treatment) from

about 15-ha aquaculture growout ponds whereseveral fed animals (Pacific white shrimp, Lito-

penaeus vannamei; mud crab, Scylla serrata;

swimming crab, Portunus trituberculatus; and

crab, Nibea miichthioides) and filtered animals

(cockle, Tegillarca granosa Linnaeus; clam,

Cyclina sinensis; and razor clam, Sinonovacula

constricta) were cultured. Another 0.2-ha (40 3

50 m) algae cultivation area was similarly estab-lished in the bay outside another outlet (HM)

that discharged effluent from a hatchery of the

shrimp, L. vannamei, and the crab, P. trituber-

culatus. The untreated aquaculture effluent was

discharged directly to the bay during ebb tide

of spring tide and water depth in the area during

low tide is about 2 m. The bay area has a regular

semidiurnal tide of about 1.2- to 1.5-m ampli-

tude with the tidal flow of about 0.30.5 cm/sec.

Cultivation of Gracilaria

The alga, G. lemaneiformis, provided by the

Hutoudu Aquaculture Company in Xiangshan

Bay was inserted into polyethylene ropes that

were supported by the rafts. A suspension cul-

ture unit was composed of four rafts, each in

turn was composed of eight ropes. Each rope

(about 10 m long and 6 cm diameter) was in-

serted with a piece of alga (about 15 g at the

PM site and 20 g at the HM site) every 15

20 cm. Distance between adjacent ropes was

4050 cm and between adjacent units was 2

3 m. Twenty units (with 640 ropes and 500 kg

algal seedling) and 8 units (with 256 ropes and

250 kg algal seedling) were established at the

PM and HM sites, respectively.

Ten (at the PM site) and five (at the HM site)

ropes with Gracilaria were randomly selected

and weighted every 15 d between March 2 and

May 7, 2006. The weights of the polyethylene

ropes without the algae were the same beforeand after the study. Average daily specific

growth rates (SGRs) were calculated as

SGR 5 (100 ln (Wt/W0))/t, where W0 is initial

wet weight and Wt is the wet weight at day

t(Lobban and Harrison 1994; Yang et al. 2006).

Water Quality Sampling

For both growout pond (PM) and hatchery

(HM) sites, two transects were similarly estab-

lished (Fig. 1). Transects A and B radiated fromthe effluent outlet, with Transect A passed

through the algal cultivation area, whereas

Transect B did not. Sampling stations were set

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up every 1525 m along each transect, with

a total of seven stations along Transects A (with

A11A17 and A21A27 for PM and HM sites,

respectively) and B (with B11B17 and B21

B27 for PM and HM sites, respectively).Between March 2 and May 7, 2006, water

samples were taken every 78 d at Transects

A and B (total 10 times) during effluent dis-

charge when tide flow ebbed. During each sam-

pling, several water quality parameters such as

water temperature (WT), salinity (S), secchi disk

depth (SD), pH, dissolved oxygen (DO), chem-

ical oxygen demand (COD), dissolved inorganic

nitrogen (DIN; NH3N + NO2N + NO3N),

and dissolved inorganic phosphorous (DIP)were measured. WT, S, SD, pH, and DO of

surface water were measured using YSI-85

(YSI, Marion, MA, USA) in the field; COD

was estimated following the JGOFS Protocol

No. 19 (JGOFS International Project Office

1994). NO3N, NO2N, NH4N, and PO4P

were determined with a Skalar San and Plus

Flow Analyzer (Skalar, Delft, Holland). Sam-

ples were collected and placed into a foam box

with ice and then transported to the laboratory

for immediate analysis.

FIGURE 1. Map of the study area. For both growout pond

(PM) and hatchery (HM) sites, four transects were

similarly established. Transects A and B radiated from

the effluent outlet; Transect A passed through the algal

cultivation area, whereas Transect B did not. Sampling

stations were set up every 1525 m along each transect,

with a total of seven stations along Transects A (with

A11A17 and A21A27 for PM and HM sites, respectively)

and B (with B11B17 and B21B27 for PM and HM sites,

respectively).

Time (Day)300 15 45 65

SGR(%/d)

0

2

4

6

8

10

Density(Kg/m)

0

1

2

3

4

5SGR-PM

SGR-HM

Density-PM

Density-HM

FIGURE 2. Changes of the daily specific growth rate (SGR) and unit density of the red alga, Gracilaria lemaneaformis, at

the growout pond (PM) and hatchery (HM) sites during the 65-d study.

IMPROVEMENT OF WATER QUALITY BY MACROALGA 551


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Statistical Analysis

Results were analyzed with the software

Sigmaplot 8.0 and SPSS 12.0. Mean and stan-

dard deviation of each treatment (n 5 3) were

calculated. The corresponding stations of Trans-

ects A and B within each site (PM or HM) were

compared using Students t test.

Results

Growth of Gracilaria

Changes in SGR and density of the seaweed,

G. lemaneiformis, over the study period are

shown in Figure 2. The patterns were similar

between the two sites (PM and HM). The aver-

age SGRs during the 65-d study period were

3.87%/d and 3.40%/d at the PM and HM

sites, respectively. The densities increased

from 80 to 4750 g/m and from ,100 to3600 g/m at the PM and HM sites, respec-

tively. The biomass (fresh weight) increased

59.4 and 37.5 times (Fig. 2), and the yield

was 30.4 and 10.4 tons at the PM and HM sites,

respectively.

Environmental Parameters

During the study period, WT varied from 13.2

to 20.7 C with an average of 18.8 C. WT at the

Site of pond outlet (PM)

0

0.2

0.4

0.6

0.8

1

1.2

A11

A13

A15

A17

B11

B13

B15

B17

SD(m)

0

2

4

6

8

10

12

14

A11

A13

A15

A17

B11

B13

B15

B17

DO(mg/L)

8.1

8.2

8.3

8.4

8.5

A11

A13

A15

A17

B11

B13

B15

B17

Sampling Sites

pH

Site of hatchery outlet (HM)

0

0.2

0.4

0.6

0.8

1

1.2

A21

A23

A25

A27

B21

B23

B25

B27

SD(m)

0

2

4

6

8

10

12

A21

A23

A25

A27

B21

B23

B25

B27

DO(mg/L)

8

8.1

8.2

8.3

8.4

8.5

A21

A23

A25

A27

B21

B23

B25

B27

Sampling Sites

pH

FIGURE 3. Average (6SD) of secchi disk depth (SD), pH, and dissolved oxygen (DO) in the surface water at the growout

pond (PM) and hatchery (HM) sites during the study period. d represents AV1 (from March 2 to April 15, 2006); s

represents AV2 (from April 16 to May 7, 2006).

552 XU ET AL.


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HM site was slightly higher than that at the PM

site because of the input of heated wastewater

from the hatchery plant. Salinity was stable,

ranged from 24.7 to 26.6&.

SD, DO, and pH values from March 2 to April15 (AV1) were similar between A and B transects

at both PM and HM sites (P . 0.05) (Fig. 3).

However, between April 15, when the seaweed

density reached about 2000 g/m, and May 7

(AV2), each parameter was significantly higher

at Transect A (within the algal culture area) than

at Transect B (no algal culture) for both PM and

HM sites (P , 0.05) but similar between the cor-

responding stations within both the PM and the

HM sites (P . 0.05) (Fig. 3). COD, DIN, and

DIP at both Transects A and B were similar

between AV1 and AV2 (P . 0.05), as well asbetween the corresponding stations within both

PM and HM sites (P . 0.05) (Fig. 4).

Discussion

Species of the genus Gracilaria are com-

monly cultured for food, commercial products,

as well as bioremediation (Troell et al. 1997,

Site of Pond outlet (PM)

0

1

2

3

A11

A13

A15

A17

B11

B13

B15

B17

COD(mg/L)

Site of Pond outlet (HM)

0

1

2

3

A21

A23

A25

A27 B

21B23

B25

B27

COD(mg/L)

20

30

40

50

60

A11

A13

A15

A17

B11

B13

B15

B17

Dissolvedinorganicnitrogen

(mol/L)

20

30

40

50

A21

A23

A25

A27

B21

B23

B25

B27

Dissolvedinorganicnitrogen

(mol/L)

0

0.4

0.8

1.2

1.6

A11

A13

A15

A17

B11

B13

B15

B17

Sampling Sites

Dissolvedinorganicphosphate

(mol/L)

0

0.4

0.8

1.2

1.6

2

A21

A23

A25

A27

B21

B23

B25

B27

Sampling Sites

Dissolvedinorganicphosphate

(mol/L)

FIGURE 4. Average (6SD) of dissolved inorganic nitrogen, dissolved inorganic phosphorous, and chemical oxygen

demand (COD) in the surface water at the growout pond and hatchery sites during the study period. d represents AV1(from March 2 to April 15, 2006); s represents AV2 (from April 16 to May 7, 2006).



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1999; Chopin et al. 2001; Fei 2004; Neori et al.

2004). Gracilaria grows fast and can uptake

large quantities of nutrient from the water.

Troell et al. (1997, 1999) estimated that 1 ha

of another cultured red alga, Gracilaria chilen-sis, had the potential to remove at least 5% of

DIN and 27% of DIP released from a fish farm.

In the two studies conducted in Jiaozhou Bay,

north China, 1 ha of the alga, G. lemaneiformis,

cultivated at the fish and bivalve culture area

yielded an estimated 70 tons (0.22 tons N and

0.03 tons P removal) (Zhou et al. 2006) and

258 tons (1.02 tons N removal) of fresh weight

annually (Yang et al. 2006). In the present study,

0.5 (PM) and 0.2 ha (HM) of the culture areayield an estimated 30.4 and 10.4 tons of fresh

weight, respectively, resulting in a production

of about 5060 tons/ha in the 65-d study period.

The alga, G. lemaneiformis, can grow all year

round in the Xiangshan Bay area (it does not

grow well in the winter and summer in north

and south China, respectively). Seaweed culture

outside the aquaculture discharge outlets may be

an effective way of treating the effluent as well

as enhancing seaweed growth.

The seaweed cultivation can also improve

other aspects of water quality, such as increasing

DO and SD (Fig. 2). Even though the efficiency

of organic uptake by the seaweed is low (Xu

et al. 2004), its photosynthesis produces DO that

accelerates decomposition of organics. On the

other hand, high-density raft culture of Graci-

laria impedes the water circulation and may

decrease COD in the water column. Several spe-

cies of Gracilaria can produce oxygen under

low light conditions, such as in rainy days, andremediate anoxia (Xu et al. 2004).

Methods for treating effluents from maricul-

ture systems with macroalgae were initiated

in the mid-1970s and developed in recent years

(Neori et al. 1996, 2000; Neori and Shpigel

1999; Troell et al. 1999; Chow et al. 2001;

Nelson et al. 2001; Neori et al. 2004; Zhou

et al. 2006). However, how to achieve an appro-

priate balance of animal/algae ratio (biomass or

density) is still a challenge. Troell et al. (1997,1999) suggested a biomass ratio of animal to

seaweed to be 1:4. Yang et al. (2006) speculated

that the fish/seaweed biomass ratio at approxi-

mately 1:1 was optimal for efficient nutrient

uptake and for maintaining low nutrient levels.

Many factors affect the optimal ratio. For exam-

ple, changes in temperature affect growth and

excretion rates of both animals and seaweed.Trophic levels of animals (e.g., filter-feeding

species vs. carnivorous species) would have a

profound impact on the waste production. In

addition, both the economic factors and the

capacity of nutrient bioremediation by seaweed

should be considered (Chopin et al. 2001; Neori

et al. 2004).

Acknowledgments

This research was financed by the National

Basic Research Program of China (no. 2006CB

400608), Ningbo Science and Technology

Bureau (2005A610025; 2006A610087), and

Young College Faculty Foundation of Zhejiang

Province (2005757). This research was also

sponsored by K.C.Wong Magna Fund in Ningbo

University. The manuscript was greatly im-

proved by the constructive comments of several

reviewers.

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